Post on 16-Jul-2016
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transcript
ORIGINAL ARTICLE
doi101111evo12787
Congruent phylogenetic and fossilsignatures of mammalian diversificationdynamics driven by Tertiary abiotic changeJuan L Cantalapiedra123 Manuel Hernandez Fernandez45 Beatriz Azanza6 and Jorge Morales2
1Museum fur Naturkunde Leibniz Institute for Evolution and Biodiversity Science Invalidenstraszlige 43 Berlin 10115
Germany2Departamento de Paleobiologıa Museo Nacional de Ciencias Naturales Consejo Superior de Investigaciones Cientıficas
Pinar 25 28006 Madrid Spain3E-mail jlopezcantgmailcom
4Departamento de Paleontologıa Facultad de Ciencias Geologicas Universidad Complutense de Madrid Jose Antonio
Novais 2 28040 Madrid Spain5Departamento de Cambio Medioambiental Instituto de Geociencias (UCM CSIC) Jose Antonio Novais 2 28040 Madrid
Spain6Departamento de Ciencias de la Tierra Facultad de Ciencias Universidad de Zaragoza Pedro Cerbuna 12 50009
Zaragoza Spain
Received February 11 2015
Accepted September 22 2015
Computational methods for estimating diversification rates from extant species phylogenetic trees have become abundant in
evolutionary research However little evidence exists about how their outcome compares to a complementary and direct source
of information the fossil record Furthermore there is virtually no direct test for the congruence of evolutionary rates based on
these two sources This task is only achievable in clades with both a well-known fossil record and a complete phylogenetic tree
Here we compare the evolutionary rates of ruminant mammals as estimated from their vast paleontological recordmdashover 1200
species spanning 50 myrmdashand their living-species phylogeny Significantly our results revealed that the ruminantrsquos fossil record
and phylogeny reflect congruent evolutionary processes The concordance is especially strong for the last 25 myr when living
groups became a dominant part of ruminant diversity We found empirical support for previous hypotheses based on simulations
and neontological data The pattern captured by the tree depends on how clade specific the processes are and which clades are
involved Also we report fossil evidence for a postradiation speciation slowdown coupled with constant moderate extinction in
the Miocene The recent deceleration in phylogenetic rates is connected to rapid extinction triggered by recent climatic fluctuations
KEY WORDS Diversification evolutionary rates fossil record mammals phylogeny turnover
The study of diversification patterns through time is of major im-
portance for understanding macroevolutionary and macroecologi-
cal processes (Benton and Emerson 2007 Morlon 2014) Mostly
diversification through time has been estimated from fossilsmdash
using taxa occurrences (Foote 2000 Alroy 2008) or placing
fossil ranges on evolutionary trees (Smith 1988 Wagner 1995
Mannion et al 2010)mdashor from calibrated phylogenies of living
taxa (Mooers and Heard 1997 Stadler 2011a) Usually fossils
have been recognized as evidence of the antiquity of life as well
as the succession and evolution of organisms on planet Earth
Patterns of fossil preservation are usually employed as a reliable
source of information on past diversity patterns and processes
2 9 4 1Ccopy 2015 The Author(s) Evolution Ccopy 2015 The Society for the Study of EvolutionEvolution 69-11 2941ndash2953
JUAN L CANTALAPIEDRA ET AL
such as origination extinction dispersal and turnover (Alroy
2009 Ezard et al 2011 Domingo et al 2014) On the other hand
living species phylogenies also provide valuable information on
such evolutionary processes (Ricklefs 2007 Jetz et al 2012) Be-
sides depicting evolutionary relationships among extant species
dated extant-taxa trees contain valuable information on the pro-
cesses that have shaped the evolutionary history of a group and
have given rise to its extant species These evolutionary processes
are responsible for phylogenetic trees being far from balanced
and presenting odd distributions of splitting times (Nee et al
1992 Harvey et al 1994a Mooers and Heard 1997) Interest-
ingly these footprints on the topology of trees are quantifiable
(Mooers and Heard 2002 Stadler 2011a) and recent methods
allow for statistical analyses of such patterns by fitting and com-
paring different macroevolutionary models of diversification in
highly resolved phylogenies (Rabosky 2006 Rabosky and Lovette
2008 Alfaro et al 2009 Paradis 2011 Stadler 2011b)
In most cases scholars are limited to one of the two
approachesmdashfossils or extant-taxa trees For instance reason-
able phylogenetic information may be available for extant groups
lacking an adequate fossil record In those circumstances the
study of evolutionary patterns through phylogenetic approaches
might be especially helpful (Fordyce 2010) On the other hand
the study of evolutionary patterns of extinct or severely impov-
erished groupsmdashfor example rhinoceros with a 40 myr history
and only six surviving speciesmdashmust rely on the fossil record
(Lloyd et al 2008 Silvestro et al 2014b) In a few cases both
comprehensive fossil and phylogenetic information are available
for a group and the comparison of the two proxies is desirable
(Simpson et al 2011 Etienne et al 2012) Exploring and con-
trasting the outcome of both methods may help us to overcome
their particular limitations (Fritz et al 2013) Additionally such
comparison might shed some light on the particular processes be-
hind tree shape beyond the pure fitting of evolutionary models
For instance a given turnover pulsemdashfaunal replacementmdashwith
both elevated origination and extinction rates may have resulted in
high origination of lineages leading to extant species thus being
recovered as a diversification pulse if only phylogenetic informa-
tion is used However studies comparing evolutionary rates from
trees of living taxa with the fossil record are few Furthermore
these typically focus solely on fossil taxonomic diversity (Quen-
tal and Marshall 2010 Morlon et al 2011 Springer et al 2012)
rather than assessing fossil-based rates (but see Simpson et al
2011) Directly testing the similarity between evolutionary rates
estimated from fossil occurrences and living species trees is the
goal of this contribution
To this aim we focus on ruminants because they provide
an ideal study group for testing the congruence between these
two sources Their fossil record is extensivemdashover 1200 species
spanning the last 50 myrmdashand reasonably well known (see the
50 40 30 20 10 0
Time before present (Ma)
EOCENE OLIGOCENE MIOCENE PLI PL
Hypertragulidae
Leptomerycidae
Blastomerycidae
Dremotheriidae
Moschidae
Gelocidae
Climacoceratidae
Archaeomerycidae
Andegamerycidae
Lophiomerycidae
Hoplitomerycidae
Bachitheriidae
daggerdaggerdaggerdagger
dagger
daggerdaggerdaggerdaggerdagger
dagger
Sp
ecie
s D
ive
rsity
30
20
10
0
s
s
s
Sp
ecie
s D
ive
rsity
0
100
200
300
400 Bovidae
Cervidae
Giraffidae
Antilocapridae
Tragulidae
Palaeomerycidae
Dromomerycidaeothers (below)
daggerdagger
A
B
Figure 1 Ruminants diversity through time Raw species diver-
sity of the 19 ruminant families through time plotted in 1 myr
time bins Families are ordered by species richness (A) Small fami-
lies are plotted in detail in plate (B) dagger extinct clade ϒ clade with
horned forms s stem group according to Metais and Vislovokowa
(2007) Pli Pliocene Pl Pleistocene Ma million years ago Note the
change of scale between plates A and B
Methods section Figs 1 and S1) Also their most complete phy-
logeny to date comprises all known species and is relatively well
resolved (12 of the nodes are polytomies Hernandez Fernandez
and Vrba 2005 Cantalapiedra et al 2014b) and newer phyloge-
netic hypotheses for the group have been published recently (Bibi
2013 2014) In this study we estimated diversification from two
large distributions of ruminant treesmdashwhich cover a wide array
of node-age configurationsmdashas well as from fossil species oc-
currence data using two different approaches We then tested for
a common signal in the rate-through-time curves from paleonto-
logical and neontological data while assessing which node-age
arrangements improved the fit against the fossil-derived rates
2 9 4 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Molecular estimates suggest that crown ruminants probably ap-
peared in the Eocene 45ndash40 Ma (Meredith et al 2011 Bibi
2013) but the radiation of the living groups mainly took place
in the last 30ndash20 myr (DeMiguel et al 2014) Thus we expect
higher concordance between rates from the two sources during the
last half of the study interval Furthermore the characterization
of the speciation-extinction interplay across such radiation using
living-taxa trees and extensive fossil datamdashboth at the species
levelmdashmay sum to the debate on ecological limits and their im-
pact on postradiation evolutionary rates (Rabosky and Lovette
2008 Moen and Morlon 2014 Harmon and Harrison 2015)
Ruminants have played a paramount role in terrestrial ecosys-
tems and their evolutionary history is relatively well known (for
recent reviews see Cantalapiedra et al 2014a Clauss and Rossner
2014 DeMiguel et al 2014) Due to their sensitivity to habitat
change ruminants have being commonly used as paleoecologi-
cal proxies (Bobe and Eck 2001 Hernandez Fernandez and Vrba
2006 Kaiser and Rossner 2007) However their macroevolution-
ary patterns are only known from raw diversity curves that are
temporal and spatially fragmentary (Vrba 1995 Blondel 2001
Costeur and Legendre 2008 Maridet and Costeur 2010 Clauss
and Rossner 2014) We here present the first estimate of diver-
sification trends of this large clade of terrestrial mammals at the
global scale Because ruminants are a habitat-informative clade a
detailed study of their diversification patterns may also have im-
portant implications for unveiling past environmental shifts within
mammalian communities during the Cenozoic
MethodsTIME SERIES OF DIVERSIFICATION FROM THE TREE
OF LIVING RUMINANTS
For comparison we estimated phylogenetic speciation rates
through time from two different tree distributions First we drew
on a recently published distribution of resolved and recalibrated
trees (Cantalapiedra et al 2014b) based on the topology pre-
sented by Hernandez Fernandez and Vrba (2005) which includes
all living ruminant species This tree distribution was obtained
by randomly resolving polytomies and recalibrating the nodes
using the extensive fossil and molecular dates of the original
papermdashavailable for 80 of the nodesmdashin a Bayesian frame-
work (see supplementary methods in Cantalapiedra et al 2014b)
Interestingly by using this tree distribution we incorporate broad
topological and temporal uncertainties into our phylogenetic-rates
analyses Second we estimated speciation rates from the Bayesian
tree distribution in Bibirsquos recent study (2013) Twelve percent of
the nodes were calibrated using priors based on a conservative in-
terpretation of the fossil record Thus the node ages in Bibirsquos tree
are significantly younger than those obtained by Cantalapiedra
et al (2014b) We used two tree distributions with different node-
age arrangements to identify how disparate node-age configura-
tions may impact the fit with the fossil record For simplicity we
will refer to these two datasets as ldquoBibirdquo and ldquoCantalapiedrardquo
To estimate time series of phylogenetic diversification dy-
namics we carried out a time windows analysis (Simpson et al
2011) We estimated speciation every 1 myr window For each
window speciation rate was calculated using the yuleWindow
function in the LASER (Rabosky 2006) package in R (R Devel-
opment Core team 2015) in which yuleWindow fits a pure birth
Yule model based on the distribution of nodes and branch lengths
(Simpson et al 2011) This means it does not estimate an ex-
tinction parameter Nevertheless the waiting times contained in
evolutionary trees that yuleWindow measures should reflect net
diversification (speciation minus extinction λ minus μ Harvey et al
1994a) Other available maximum likelihood methods (Stadler
2011b) allow estimating extinction directly However to estimate
accurate rates such methods require at least 30 branching events
per time slice (Jetz et al 2012) In our dataset this would imply
limiting our analyses interval to the last 10 myrmdashwith two 5 myr
time slicesmdashor the last 6 myrmdashwith three 2 myr times slices A
speciation time series was calculated for 500 trees of each tree
distributions Each of the 1000 curves was retained for plotting
and for individual correlation test with fossil-derived rates
ANALYSIS OF THE RUMINANT FOSSIL RECORD
Information of ruminant species occurrences in the fossil record
was compiled from the New and Old Worlds (NOW) database
(Fortelius 2015) and the Paleobiology Database (Alroy 2015)
both accessed in July 2014 Taxa not identified at the species level
were excluded (1763 occurrences see Supporting Information for
their temporal distribution) Subsequently the combined database
was completed and refined with information from the literature
(see Supporting Information) and information on synonyms pro-
vided by the NOW collaborators Finally we gathered a database
containing 9234 occurrences of 1246 ruminant species whose
record spans the last 50 myr (Fig 1 see also Dataset S1 in Dryad
repository) Species belonging to the six extant families (8558
occurrences of 1100 species) represent around 88 of ruminant
fossil diversity being recorded continuously since around 24 Ma
and making most of the ruminant fossil record since around 20
Ma (Fig 1) Significant gaps in the fossil record were identified
for Tragulidae Leptomerycidae Gelocidae Blastomerycidae
and Moschidae (noncontinuous colors in Fig 1) We performed
an estimation of the quality of the ruminant fossil record by
exploring the temporal distribution of fossil occurrences their
assigned temporal range and the preservation rate through time
(Alroy 2008 Simpson et al 2011 Supporting Information
Fig S1)
EVOLUTION NOVEMBER 2015 2 9 4 3
JUAN L CANTALAPIEDRA ET AL
FOSSILS-BASED EVOLUTIONARY RATES
We assessed relevant evolutionary rates (speciation and extinc-
tion) from the ruminant fossil record using two methods First
we used the most recent version of Alroyrsquos ldquothree-timersrdquo-based
equations (Alroy 2014) This method uses a four-interval moving
window that has been proved to be robust toward noise produced
by high turnover andor poor sampling The method incorporates
the interval-to-interval variation of preservation rate (see Sup-
porting Information) Alroyrsquos rates were estimated after dividing
the analysis interval in 1 myr bins To test the significance of
the evolutionary rates our dataset was bootstrapped with replace-
ment 5000 times using species occurrences as sampling units
Because occurrence data are usually assigned to temporal ranges
broader than 1 myr for each bootstrap occurrences were randomly
assigned to one of the 1 myr bins falling within their temporal
ranges We did this to include all the temporal uncertainty in our
analyses For each time bin we estimated the mean rate (Finarelli
and Badgley 2010)
Additionally to the bin-based method (three-timers) we es-
timated speciation extinction and net diversification from the
fossil record using a birthndashdeath MCMC analyses in a Bayesian
framework (BDMCMC as implemented in PyRate Silvestro et al
2014ab) The BDMCMC algorithm uses fossil occurrences data
to simultaneously estimate speciation and extinction times for
each species while finding the birthndashdeath model that better fits
the fossil record (Silvestro et al 2014ab) The model also incorpo-
rates sampling and the BDMCMC algorithm explores alternative
diversification models with different number of rate shifts (Silve-
stro et al 2014b) Importantly the method is robust toward data
incompleteness and is capable to recover a wide array of rates-
shift scenarios We randomly resampled the age of fossil occur-
rences from the occurrence intervals (from uniform distributions)
10 times using the R function extractages included in the PyRate
files Each replicate was analyzed independently for 10000000
generations using Python 26 in the Computational Cluster Trueno
at the CSIC We set the extant number of species to 197 the num-
ber of species of our bigger tree and allowed the preservation
rates to change across lineages following a gamma distribution
Mean rates through time were estimated after discarding the 20
of the logged rate estimates as burn-in and combining the results
from the 10 independent runs
Both Alroyrsquos method and the BDMCMC algorithm were used
to analyze the complete fossil record of crown ruminants (9186
occurrences see Fig 1) and the fossil record of the six living
ruminant families (8558 occurrences) We followed Metais and
Vislovokowa (2007) and considered crown ruminants all families
except Hypertragulidae Lophiomerycidae and Archaeomeryci-
dae (Fig 1) Some authors have considered the Eocene forms
Archaeotragulus and Krabitherium to belong to the extant family
Tragulidae (but see Sanchez et al 2010) thus implying a 10 myr
gap in the fossil record (from around 33 to 24 Ma see Fig 1) that
would certainly yield misleading rate estimates from this time
interval Thus we exclude these two genera from the six living
families fossil occurrences subset
We used PyRate to estimate fossil-based origination times
of the crown ruminants the pecoransmdashthe ldquomodern ruminantsrdquo
which usually have horns and include five of the six living fam-
ilies (Bibi 2014)mdashand the groups with horned forms (Fig 1)
This was done by extracting the posterior samples of the ages
of origin of the fossil species of interest derived from all occur-
rences replicates after modeling the fossil sampling process and
accounting for the uncertainties around the estimated ages of first
occurrences (Silvestro et al 2015) Thus these estimates predate
the oldest fossil occurrence of each group Then we fitted normal
lognormal and gamma distributions to these dates and choose the
best fit based on the Akaike Information Criterion (Burnham and
Anderson 2002) In this way we obtain origin age estimates that
may ease the discussion on evolutionary patterns and distribution
parameters that may be used in future phylogenetic analyses as
node-age priors (Silvestro et al 2015)
Net diversification was estimated as speciation minus ex-
tinction When the term ldquonet diversificationrdquo is used we refer to
this balance The term ldquodiversificationrdquo may be sometimes used
regarding evolutionary rates in a broader sense
CORRELATION OF THE TREE-BASED AND
FOSSILS-BASED CURVES
So far comparisons between evolutionary rates from fossil oc-
currence data and living species phylogenies have mostly relied
on pure visual and descriptive inspections (Simpson et al 2011)
Here to test whether curves are in phase with one another we
used Kendallrsquos correlation tests (Hammer and Harper 2006) This
method has been extensively applied to temporal series (Hammer
and Harper 2006 Mannion et al 2010) and assesses whether
the peaks and troughs correspond between two curves That is
it will here measure the concordance in shifts in evolutionary
rates
Because we aim to explore the impact of different node-age
configurations on the fit with fossil-derived curves we estimated
Kendallrsquos correlations between each of the 1000 rate curves ob-
tained from living-species phylogenies (500 from the trees in
Cantalapiedra and 500 from Bibi) and the mean fossil-derived
speciation and net-diversification curves estimated for the crown
ruminants using Alroyrsquos method and PyRate The correlation tests
were repeated using the fossil-derived curves (speciation and net
diversification from Alroyrsquos method and the BDMCMC analysis)
obtained from the fossil record of the six surviving ruminant fam-
ilies This was done to empirically assess whether the congruence
between fossil-based and tree-based rates is independent of the
inclusion of clades without phylogenetic representation in cases
2 9 4 4 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
where the extant families hold much of the fossil record A total
of 8000 Kendallrsquos correlations were estimated
To visualize the results we plotted the density distributions of
the P-values (for significance) and Kendallrsquos taus (τ for the sense
of the correlation) To explore whether different node-age arrange-
ments influence the correlation with the fossil record we plotted
P-values and taus obtained from each correlation test against the
mean node age of the 25 older and 25 younger nodes of the tree
involved To help data interpretation we fitted loess curves with
smoothing parameters estimated by generalized cross-validation
to avoid over-fitting to the data (Kohn et al 2000)
ResultsPHYLOGENETIC RATES
The two tree distributions encompass a wide array of node-age
configurations (Fig 2A) Nevertheless both datasets show a very
similar profile The speciation curves obtained from the two tree
distributions show a first pulse related to pecoran and tragulid
basal splits and a second part corresponding with the large radi-
ation within the six living families The deepest trees place the
first pulse in the early Oligocene (32 Ma) and the beginning
of within-family radiations in the Oligocene-Miocene (24 Ma)
The trees with younger node agesmdashmainly Bibirsquos distributionmdash
place these events in the early Miocene (20 Ma) and middle
Miocene (15 Ma) respectively In both tree distributions a slow-
down follows the second big burst followed by a recoverymdashwith
a synchronic peak in both datasets around 7 Mamdashand a final
slowdown toward the present (Bibirsquos dataset shows a recovery in
the Plio-Pleistocene Fig 2A)
RATES FROM FOSSIL OCCURRENCES
Rates estimated from fossil occurrences (net diversification spe-
ciation and extinction) obtained from the ldquothree-timersrdquo method
and the BDMCMC are depicted in Fig 2B and C respectively
Patterns of net diversification are congruent between both ap-
proaches although the speciation and extinction processes differ
in some aspects
According to the ldquothree-timersrdquo method important speci-
ation pulses are recovered during the middle and late Eocene
(45 Ma Fig 2B) and the Eocene-Oligocene boundary (34 Ma)
featured high extinction and speciation The early Oligocene is
characterized by overall neutral net diversification and turnovermdash
low extinction and very slow speciationmdash(Fig 2B) At the
end of the Oligocene net-diversification rates peaked again re-
maining high across the Oligocene-Miocene boundary (around
24 Ma) Speciation decelerated afterwards From about 20 Ma
onwards several speciation and extinction peaks render a rela-
tively constant turnover A negative net-diversification peak is
recovered around 15 Ma followed by a recovery between 12 and
10 Ma The Miocene to Pliocene transition marks a peak of the
replacement rate stemming from an episode of elevated specia-
tion and extinction rates (Fig 2B) Afterwards net diversification
increased again in part due to low extinction at the beginning
of the Pliocene Due to the ldquothree-timersrdquo methodology net di-
versification cannot be recovered from the last three bins of the
analysis interval
The BDMCMC analyses reveal high and maintained specia-
tion rates of crown ruminant lineages throughout the Eocene the
Oligocene and the earliest Miocene (Fig 2D) This high specia-
tion was coupled with elevated extinction rates particularly severe
in the late Eocene and much of the Oligocene (between 47 and
26 Ma) The confidence intervals are broad until around 26 Ma
probably due to the large occurrence temporal ranges (Fig S1)
The diversification maximum at the Oligocene-Miocene bound-
ary is here a result of decelerating extinction and sustained
high speciation The end of the net-diversification pulse around
20 Ma was rendered by a slowdown in speciation rates Moderate
speciation and extinction characterized much of the Miocene Ex-
tinction and speciation recovered around 8 and 6 Ma respectively
Whereas speciation stayed constant until the present extinction
intensely peaked during the last two million years resulting in the
most severe negative net-diversification pulse of the analysis in-
terval Gamma distributions best fitted the time of origin of crown
ruminants (offset = 4263 shape = 176 rate = 046 mean =4647 95 highest posterior density (HPD) = 4285ndash5224) pec-
orans (offset = 2696 shape = 168 rate = 057 mean = 2990
95 HPD = 2704ndash3330) and groups with horned forms (offset
= 2649 shape = 202 rate = 196 mean = 2751 95 HPD =2656ndash2906 Fig 2C)
CURVE CORRELATIONS
The results of the 8000 Kendallrsquos correlations are shown in
Figure 3 When the ldquothree-timersrdquo were used to estimate fossil-
based evolutionary rates the speciation rates based on the deepest
treesmdashfrom Cantalapiedrarsquos tree distributionmdashshowed high con-
gruence with the speciation in fossil crown Ruminantia and with
speciation and net diversification in the fossil lineages of the liv-
ing groups These correlations seemed unaffected by the different
node ages of the tree set Only the rate curves obtained from
the oldest trees showed significant correlationmdashand high positive
tausmdashwith the net-diversification curve of the crown fossil ru-
minants Speciation rates estimated from Bibirsquos trees correlated
positively with speciation in the fossil lineages of the living ru-
minant families This correlation is weaker for the trees whose
deeper nodes are younger
Rates calculated from tree distribution in Cantalapiedra cor-
related positively with speciation and net diversification in the
fossil record of the six living families as estimated by the BDM-
CMC algorithm (Fig 3GndashL) Only rates in Bibirsquos deepest trees
EVOLUTION NOVEMBER 2015 2 9 4 5
JUAN L CANTALAPIEDRA ET AL
groups withhorned forms
crown pecoranscrown ruminantsfirst fossil horns
times of origin(density)
05
0
A
B
C
D
00
01
02
03
04
05
50 40 30 20 10 0
tree-
base
d sp
ecia
tion
EOCENE OLIGOCENE MIOCENE PLI PL
50 40 30 20 10 0
50 40 30 20 10 0
EOCENE OLIGOCENE MIOCENE PLI PL
BibiCantalapiedra et al
-025
000
025
050
075
lsquothre
e-tim
ersrsquo
rate
s net-diversificationnet-div living familiesspeciationextinction
-03
00
03
06
Time (Ma)
PyR
ate
rate
s
inception offirst C3 grasslands
inception offirst C4 grasslands
permanentEAIS
onset ofmodern glaciations
Bering Strait
ArabianConnection
net-diversificationnet-div living familiesspeciationextinction
Figure 2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants (A) Tree-based speciation
rates estimated from 1000 living species phylogenies from Bibi (2013) and Cantalapiedra et al (2014b) The shadowed area represents the
95 confidence intervals (B) Net diversification speciation and extinction in fossil crown ruminants estimated using the ldquothree-timersrdquo
method (Alroy 2014) (C) Estimated times of origins of crown ruminants pecorans (advanced ruminants) and groups with horned forms
according to PyRate (D) Net diversification speciation and extinction in fossil crown ruminants estimated using PyRate (Silvestro et al
2014a) In (B) and (D) net diversification in fossil lineages of the living groups is shown in light blue Shadowed areas in (B) and (D)
represent the 95 confidence interval for the net diversification The first record of horned ruminants (gray) is based on DeMiguel et al
(2014) Mayor tectonic climatic and ecological episodes (Cerling et al 1997 Zachos et al 2008 Stromberg 2011) are shown in colors
EAIS East Antarctic Ice Sheet Pli Pliocene Pl Pleistocene Ma million years ago
showed a significant positive correlation with PyRatersquos speciation
and net diversification in the fossil record of the living groups
Phylogenetic rates from this tree set correlated negatively with
speciation in fossil crown ruminants A negative correlation was
found also with the net diversification of the fossil crown rumi-
nants for the younger trees in Bibirsquos dataset
DiscussionPast evolutionary processes left a congruent signal in the fossil
record and the phylogeny of the living ruminants The concor-
dance was stronger when fossil-based rates were estimated from
paleontological data of the living groups only (Figs 2 and 3) We
2 9 4 6 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Figure 3 Congruence of tree-based and fossils-based rates from the ldquothree-timersrdquo method (AndashF) and PyRate (GndashL) Density plots of
P-values (A) P-values from Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (B) and younger nodes (C)
of each tree Density plots of ldquotausrdquo (τ) (D) ldquotausrdquo Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (E)
and younger nodes (F) of each tree Same plots for P-values and taus when phylogenetic rates were compared with PyRate results (GndashL)
In each plot continuous LOESS lines represent results for trees in Cantalapiedra et al (2014b) and dashed lines results for Bibirsquos trees
(Bibi 2013) Dark blue and light blue fits of phylogenetic rates with net diversification in fossil lineages of crown ruminants and living
groups respectively Dark green and light green fits of phylogenetic rates with speciation in fossil lineages of crown ruminants and
living groups respectively Circles and triangles in plates A D G and J represent the medians of the parameter values of correlations for
trees in Cantalapiedra et al (2014b) and Bibi (2013) respectively
found less agreement in comparisons that used the entire fossil
record of crown ruminants where correspondences among dif-
ferent phylogenetic datasets and fossil-based methodsmdashldquothree-
timersrdquo and PyRatemdashperformed disparately (Fig 3) This is not
surprising given the nature of the evolutionary processes them-
selves and the particularities and limitations of each of the meth-
ods used in this study to recover the past Despite the many com-
parisons among rate profiles conducted here (ie two different
tree distributions two fossil-based methods two different fossil
subsets) we obtained unambiguous results about their fit through
a large array of different phylogenetic trees (Fig 3)
The capacity of living ruminant phylogenies to reconstruct
the most basal events of ruminant evolution (the Eocene and
Oligocene from around 50 to 24 Ma) critically determines the
extent to which they match evolutionary rates estimated from
the fossil record Reconstructed branching events in living ru-
minant trees are scarce during this early stage of the analysis
interval yielding very low speciation rates (Fig 2A) On top
of this different interpretations of our large fossil data (ie a
discrete-bin-based approach and a birthndashdeath Bayesian algo-
rithm) portrait disparate evolutionary scenarios for this period
(especially regarding speciation rates green curves in Fig 2B and
D) The ldquothree-timersrdquo approach reconstructed overall low specia-
tion and moderate-to-negative net diversification in the 50ndash24 Ma
temporal span Only one relevant speciation event was estimated
around 40 Ma (Fig 2B) This is a more literal read of the fossil
EVOLUTION NOVEMBER 2015 2 9 4 7
JUAN L CANTALAPIEDRA ET AL
record than that offered by PyRate (see below) The interpretation
of an early evolutionary calm before the big Miocene radiation
fits better the classic paleontological view (based on fossil ranges
and raw diversity curves Janis et al 2000 Costeur and Legendre
2008 Maridet and Costeur 2010) and the phylogenetic inferences
(Fig 2A and B) The two tree distributions yielded confidence
intervals that overlap with zero in this temporal span Thus when
the ldquothree-timersrdquo method was used the correlation between tree-
based rates and fossil speciation of the crown ruminants was
strong for most of the trees in the Cantalapiedra dataset and some
of Bibirsquos trees
PyRatersquos BDMCMC algorithm estimates a different scenario
for the first 25 myr of ruminant evolution especially with respect
to speciation rates (compare green curves in Fig 2B and D)
Unsurprisingly this notably influenced the congruence with phy-
logenetic rates (Fig 3GndashL) The BDMCMC approach places the
highest speciation rates in the Eocene Oligocene and earliest
Miocene (45ndash22 Ma Fig 2D) As a result PyRate speciation and
diversification estimates for the fossil crown ruminants yielded
a poor fit with our phylogenetic rates which show their low-
est values in this temporal span (Fig 2A) This striking differ-
ence with respect to the ldquothree-timersrdquo rates could be explained
by a deficient sampling rate (especially low for the Oligocene
Fig S1) Surprisingly although the BDMCMC algorithm (after
modeling the sampling to estimate the corrected life span of each
lineage Silvestro et al 2014a) showed high speciation rates it
still estimated accelerated extinction rates between 37 and 26 Ma
(Fig 2C) In this regard both methods agree suggesting that we
are recovering a true macroevolutionary signal and that the esti-
mate of high extinction rates is probably robust toward sampling
Although Alroyrsquos method yielded negative Eocene and
Oligocene diversification rate and subsequent diversity lossmdash
also visible in the raw diversity plot (Fig 1)mdashPyRate revealed
a scenario where net diversification slowed down but remained
positive Nonetheless PyRate yielded broad confidence intervals
for this temporal span suggesting other scenarios should not be
discarded The high Eocene-Oligocene speciation and extinction
rates should have rendered a profound replacement in ruminant
faunas This result is consistent with the high turnover previously
reported in Eurasian faunas (the so-called ldquoGrand Coupurerdquo
Janis 2008 Springer et al 2012) which has been associated with
cooler and more arid conditions in early Oligocene terrestrial
habitats (Mosbrugger et al 2005 Zachos et al 2008) However
understanding the impact of the Oligocene new environmental
context in mammalian communities demands further exploration
A comprehensive characterization of dietary shifts in Oligocene
ruminant lineages will be very insightful in this regard (Blondel
2001) Interestingly the Oligocene extinction peak is clearly
reflected by the trees as a prolonged period of low branching
rate (Fig 2A) We suggest that this lineage depletion marked the
shape of the living ruminants tree to a great extent restricting
the number of lineages that it recovers from the Eocene and
Oligocene (Fig 2) This provides an empirical proof of the
footprint that prolonged and high extinction rates leave in living
species phylogenies (Harvey et al 1994b Morlon et al 2011)
A major net-diversification pulse is robustly recovered from
both the fossil record and the phylogenetic trees during the
late Oligocene and early Miocene (27ndash22 Ma Fig 2) Al-
though the two fossil-based approaches show an increase in net-
diversification rates paired with low extinction they differ in
the macroevolutionary context of such major net-diversification
peaks Alroyrsquos method depicts accelerating speciation rates as ru-
minant lineages approached the Oligocene-Miocene limit PyRate
suggests that the high speciation rates represent continuity with
regard to Eocene and Oligocene times and that extinction would
have dropped as modern groups evolved around 27 Ma (Fig 2C
and D) This moment marked the shift toward a second major
stage of ruminant evolution the dominion of the ldquoadvancedrdquomdash
mostly hornedmdashruminants the pecorans (see Fig 1 and further
discussion below) The major radiation encompassed the appear-
ance of several living and extinct groups and a rapid accumulation
of species diversity (Fig 1) Extant groups may have exhibited
early Miocene rates above those estimated for the crown group
as a whole (Fig 2D) As a result ruminant diversity was rapidly
dominated by living groups since the early Miocene until today
(Fig 1 Costeur and Legendre 2008 Maridet and Costeur 2010)
Indeed diversification rates in fossil lineages of the crown and the
living families are very similar for the rest of the analysis interval
(Figs 2 and S2) This preponderance is also congruent with the
high agreement found between fossil-derived rates and phylo-
genetic rates in the last 25 myr of the study interval Correla-
tions showed significant concordance among curves from differ-
ent fossil-based methods and tree distributions when the fossil
record of the living groups was used (Fig 3) Only the youngest
trees from Bibirsquos dataset show nonsignificant fits Overall as early
Miocene net diversification recovered after a prolonged period of
high extinction the concordance between the macroevolutionary
signal in the fossil record and our phylogenetic data significantly
increased
After the Oligocene-Miocene diversification burst specia-
tion and net diversification significantly declined However only
trees from the dataset in Cantalapiedra et al show a comparable
pattern (Fig 2) There are two potential explanations for this out-
come First the middle Miocene (17ndash12 Ma) was indeed a period
of relatively low macroevolutionary rates and the younger trees
within Bibirsquos dataset are simply too young to reflect the true trend
Second Bibirsquos trees correctly reflect the timing of speciation of
crown living lineages whereas the other sources are recovering
the speciation of stem and crown living families combinedmdash
our fossil data include stem forms If true this second scenario
2 9 4 8 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
implies that high branching rates in living species trees may not
fit the rates estimated from the fossil record where a distinction
of crown and stem forms is very problematic even in a group with
a well-known fossil record as the ruminants (Sanchez et al 2011
Bibi 2014) Thus in cases where there is a significant temporal
lag between the diversification of stem and crown lineagesmdashas it
may be the case heremdashthe selection of true crown fossil calibra-
tion points is crucial (Bibi 2013) In this regard new total-evidence
methods (ldquotip-datingrdquo Ronquist et al 2012 Grimm et al 2015)
are contributing to overcome this issue by placing fossils within
the phylogenetic trees based on morphology while using them
to estimate divergence times (Ronquist et al 2012) Future total-
evidence analyses based on molecular data and morphology of
living and fossil ruminants will clarify this disagreement
The great diversification pulse of the Oligocene-Miocene
and the following deceleration of speciation rates may contribute
a first-hand empirical proof of the impact of ecological limits on
postradiation evolutionary rates (Moen and Morlon 2014 Harmon
and Harrison 2015) According to paleontological and paleocli-
matic evidences the Paleogene-Neogene transition was a period
of profound change in terrestrial ecosystems New available adap-
tive space was probably created by important shifts in Oligocene
and early Miocene climate (Bruch et al 2007 Eronen et al 2010)
environments (Stromberg 2011) and tectonicsmdashfor example ru-
minants entered Africa for the first time (Maglio 1978) Under this
view speciation rates would have slowed down as the adaptive
space filled Importantly extinction rates remained at basal levels
showing that the Miocene slowdown in the living ruminant tree is
rendered at the end of an expansion phase of the modern forms and
not by extinction increasing above speciation (Moen and Morlon
2014) Distinguishing between these alternatives is challenging
if just living species trees are used (Rabosky and Lovette 2008)
Ecological saturation occurs at the species level and only evolu-
tionary rates estimated from species-level fossil occurrence data
should be used to address such questions precisely (Harmon and
Harrison 2015) In this regard our fossil-based analyses provide
valuable support to previous conclusions built on neontological
information and simulations (Rabosky and Lovette 2008)
Ruminant faunas underwent critical macroevolutionary pro-
cesses in the last 10 million years (Fig 2) The fossil data sug-
gest an increase of extinction from that time onwards and a later
rebound of speciation rates Estimates from the ldquothree-timersrdquo
method and PyRate fit showing neutral-to-negative net diversi-
fication that translated into a late Miocene diversity loss Phylo-
genetic rates remained steady or slightly decreased Overall we
do not recognize a direct resemblance among curves in this tem-
poral point Nevertheless it may be the case that late Miocene
depletion also contributed to the low branching rates recovered
earlier in the trees (15ndash10 Ma see Rabosky and Lovette 2008) If
the Oligocene prolonged extinction erased most of the branches
before 30 Ma the late Miocene diversity loss may also have pre-
vented part of the evolutionary signal from the middle Miocene
to be recorded in the living species trees (Harvey et al 1994a)
We rule out the possibility that this extinction pulse is an artifact
derived from poor sampling Preservation rates of the ruminant
fossil record are relatively high for the late Miocene (around 075
Fig S1) Furthermore the two methods used to analyze the fossil
data account for heterogeneous sampling in very different ways
and yet yield very similar results with tight confidence intervals
(Fig 2) Our results show a recovery in speciation during the latest
Miocene and the Pliocene from around 7 to 25 Ma Late Pliocene
speciation rebound to levels comparable to the early Miocene As
argued above this recovery probably is reflected by the trees with
nodes slightly deeper in time due to the deeper molecular esti-
mates toward the Miocene-Pliocene Very likely mainly bovids
and deer lineages led that speciation pulse including the radiation
of American deer and that of African bovid tribes (Bibi et al
2009 Cantalapiedra et al 2014c)
The Plio-Pleistocene was one of the most dramatic episodes
in ruminant evolution A critical net diversification drop recov-
ered from the fossil record couples a slowdown in the phylogenetic
rates toward the end of our analysis interval (Fig 2) Fossil-based
rates for the last 2 myrmdashonly provided by PyRate see Methodsmdash
exhibited a severe extinction event Speciation rate still remained
close to early Miocene levels during this period but extinction
significantly surpassed it (Fig 2D) The resulting replacement
process would have reshaped ruminant faunas faster than ever
The idea of a major Plio-Pleistocene climatic shift (the estab-
lishment of continental northern-hemisphere glaciations Miller
et al 2005) and human activity reshaping mammalian faunas have
been proposed for several mammalian clades (Delson 1985 Kim-
bel 1995 Lyons et al 2004 Gomez Cano et al 2013) These
suggestions are supported by our results
To our knowledge this is the first direct evidence for neg-
ative net diversificationmdashextinction above speciationmdashas being
behind the slowdowns in living species trees toward the tips often
reported in the literature (Moen and Morlon 2014) This empir-
ical case opens the possibility that indeed progressive decrease
in phylogenetic rates toward recent times may in some cases
be the result of recent and drastic climatic fluctuations triggering
extinction
Concluding remarks
Since the first studies on tree shape (Nee et al 1992 Harvey
et al 1994b) an extensive body of research has been devoted to
understand how evolutionary processes leave their signal in phy-
logenetic trees of extant taxa Most researchers have focused on
estimate evolutionary ratesmdashthat is speciation and extinctionmdash
from phylogenies of living species (Rabosky and Lovette 2008
Alfaro et al 2009 Stadler 2011a) Other studies have pursued
EVOLUTION NOVEMBER 2015 2 9 4 9
JUAN L CANTALAPIEDRA ET AL
the identification of past episodes in evolutionary trees by com-
parison with simulations (Crisp and Cook 2009) Surprisingly
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data Quental and Marshall 2010 Morlon
et al 2011 Etienne et al 2012) Simpson et al (2011) compared
phylogenetic rates with fossil-based rates but the correlation be-
tween curves was not tested statistically Here we have shown
how the combination of speciation and extinction as recovered
from the fossil record left a signal in the living species phylogeny
of ruminants through 50 myr of evolution Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved Also the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90 of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig 1) We
acknowledge that this might not be the case scenario for many
study groups
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive rep-
resentation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12) Also
calibrating phylogenies using highly tight and conservative fossil-
informed priors may not yield rate profiles that fit rates through
time from the fossil record because the major pulses in lineage
speciation may have taken place in stem lineages
Our results also provide new views on ruminant evolution
that should be contrasted in the future The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small hornless and browser forms that were
not involved in any extraordinary diversification pulse (ldquothe lull
before the stormrdquo Janis 2008) This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1 These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007) In contrast our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig 2C)
Our analyses strongly suggest that the classic ldquoMiocene ru-
minant radiationrdquo begun in Oligocene times and prolonged until
22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-
ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition
of larger body sizes (Morales et al 1993) new dietary strate-
gies (Cantalapiedra et al 2014b) and behavior (Janis 1982 1989
Brashares et al 2000) However this event and the estimated
origin of ruminant groups with horned forms (275 Ma) largely
predates the first fossil evidence of horns in ruminants (19ndash17
Ma see DeMiguel et al 2014 Fig 2C) This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al 2014) or
those horned ruminants are to be found in the Oligocene
Finally since little can be recovered from living species trees
about the first 25 myr of ruminant evolution improving the poor
Eocene and Oligocene fossil record is crucial for future paleobio-
logical studies (Blondel 2001) This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
ldquophylogenetic coveragerdquo due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al
2012 Hipsley et al 2014 McGuire et al 2014) In summary
unveiling Paleogene environmental trends and mammal commu-
nitiesrsquo dynamics will largely benefit from fossil data And basal
ruminants probably have a lot to teach us about it
ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education
DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)
LITERATURE CITEDAlfaro M E F Santini C Brock H Alamillo A Dornburg D L Rabosky
G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414
Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542
mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge
mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397
mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014
2 9 5 0 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
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JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
JUAN L CANTALAPIEDRA ET AL
such as origination extinction dispersal and turnover (Alroy
2009 Ezard et al 2011 Domingo et al 2014) On the other hand
living species phylogenies also provide valuable information on
such evolutionary processes (Ricklefs 2007 Jetz et al 2012) Be-
sides depicting evolutionary relationships among extant species
dated extant-taxa trees contain valuable information on the pro-
cesses that have shaped the evolutionary history of a group and
have given rise to its extant species These evolutionary processes
are responsible for phylogenetic trees being far from balanced
and presenting odd distributions of splitting times (Nee et al
1992 Harvey et al 1994a Mooers and Heard 1997) Interest-
ingly these footprints on the topology of trees are quantifiable
(Mooers and Heard 2002 Stadler 2011a) and recent methods
allow for statistical analyses of such patterns by fitting and com-
paring different macroevolutionary models of diversification in
highly resolved phylogenies (Rabosky 2006 Rabosky and Lovette
2008 Alfaro et al 2009 Paradis 2011 Stadler 2011b)
In most cases scholars are limited to one of the two
approachesmdashfossils or extant-taxa trees For instance reason-
able phylogenetic information may be available for extant groups
lacking an adequate fossil record In those circumstances the
study of evolutionary patterns through phylogenetic approaches
might be especially helpful (Fordyce 2010) On the other hand
the study of evolutionary patterns of extinct or severely impov-
erished groupsmdashfor example rhinoceros with a 40 myr history
and only six surviving speciesmdashmust rely on the fossil record
(Lloyd et al 2008 Silvestro et al 2014b) In a few cases both
comprehensive fossil and phylogenetic information are available
for a group and the comparison of the two proxies is desirable
(Simpson et al 2011 Etienne et al 2012) Exploring and con-
trasting the outcome of both methods may help us to overcome
their particular limitations (Fritz et al 2013) Additionally such
comparison might shed some light on the particular processes be-
hind tree shape beyond the pure fitting of evolutionary models
For instance a given turnover pulsemdashfaunal replacementmdashwith
both elevated origination and extinction rates may have resulted in
high origination of lineages leading to extant species thus being
recovered as a diversification pulse if only phylogenetic informa-
tion is used However studies comparing evolutionary rates from
trees of living taxa with the fossil record are few Furthermore
these typically focus solely on fossil taxonomic diversity (Quen-
tal and Marshall 2010 Morlon et al 2011 Springer et al 2012)
rather than assessing fossil-based rates (but see Simpson et al
2011) Directly testing the similarity between evolutionary rates
estimated from fossil occurrences and living species trees is the
goal of this contribution
To this aim we focus on ruminants because they provide
an ideal study group for testing the congruence between these
two sources Their fossil record is extensivemdashover 1200 species
spanning the last 50 myrmdashand reasonably well known (see the
50 40 30 20 10 0
Time before present (Ma)
EOCENE OLIGOCENE MIOCENE PLI PL
Hypertragulidae
Leptomerycidae
Blastomerycidae
Dremotheriidae
Moschidae
Gelocidae
Climacoceratidae
Archaeomerycidae
Andegamerycidae
Lophiomerycidae
Hoplitomerycidae
Bachitheriidae
daggerdaggerdaggerdagger
dagger
daggerdaggerdaggerdaggerdagger
dagger
Sp
ecie
s D
ive
rsity
30
20
10
0
s
s
s
Sp
ecie
s D
ive
rsity
0
100
200
300
400 Bovidae
Cervidae
Giraffidae
Antilocapridae
Tragulidae
Palaeomerycidae
Dromomerycidaeothers (below)
daggerdagger
A
B
Figure 1 Ruminants diversity through time Raw species diver-
sity of the 19 ruminant families through time plotted in 1 myr
time bins Families are ordered by species richness (A) Small fami-
lies are plotted in detail in plate (B) dagger extinct clade ϒ clade with
horned forms s stem group according to Metais and Vislovokowa
(2007) Pli Pliocene Pl Pleistocene Ma million years ago Note the
change of scale between plates A and B
Methods section Figs 1 and S1) Also their most complete phy-
logeny to date comprises all known species and is relatively well
resolved (12 of the nodes are polytomies Hernandez Fernandez
and Vrba 2005 Cantalapiedra et al 2014b) and newer phyloge-
netic hypotheses for the group have been published recently (Bibi
2013 2014) In this study we estimated diversification from two
large distributions of ruminant treesmdashwhich cover a wide array
of node-age configurationsmdashas well as from fossil species oc-
currence data using two different approaches We then tested for
a common signal in the rate-through-time curves from paleonto-
logical and neontological data while assessing which node-age
arrangements improved the fit against the fossil-derived rates
2 9 4 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Molecular estimates suggest that crown ruminants probably ap-
peared in the Eocene 45ndash40 Ma (Meredith et al 2011 Bibi
2013) but the radiation of the living groups mainly took place
in the last 30ndash20 myr (DeMiguel et al 2014) Thus we expect
higher concordance between rates from the two sources during the
last half of the study interval Furthermore the characterization
of the speciation-extinction interplay across such radiation using
living-taxa trees and extensive fossil datamdashboth at the species
levelmdashmay sum to the debate on ecological limits and their im-
pact on postradiation evolutionary rates (Rabosky and Lovette
2008 Moen and Morlon 2014 Harmon and Harrison 2015)
Ruminants have played a paramount role in terrestrial ecosys-
tems and their evolutionary history is relatively well known (for
recent reviews see Cantalapiedra et al 2014a Clauss and Rossner
2014 DeMiguel et al 2014) Due to their sensitivity to habitat
change ruminants have being commonly used as paleoecologi-
cal proxies (Bobe and Eck 2001 Hernandez Fernandez and Vrba
2006 Kaiser and Rossner 2007) However their macroevolution-
ary patterns are only known from raw diversity curves that are
temporal and spatially fragmentary (Vrba 1995 Blondel 2001
Costeur and Legendre 2008 Maridet and Costeur 2010 Clauss
and Rossner 2014) We here present the first estimate of diver-
sification trends of this large clade of terrestrial mammals at the
global scale Because ruminants are a habitat-informative clade a
detailed study of their diversification patterns may also have im-
portant implications for unveiling past environmental shifts within
mammalian communities during the Cenozoic
MethodsTIME SERIES OF DIVERSIFICATION FROM THE TREE
OF LIVING RUMINANTS
For comparison we estimated phylogenetic speciation rates
through time from two different tree distributions First we drew
on a recently published distribution of resolved and recalibrated
trees (Cantalapiedra et al 2014b) based on the topology pre-
sented by Hernandez Fernandez and Vrba (2005) which includes
all living ruminant species This tree distribution was obtained
by randomly resolving polytomies and recalibrating the nodes
using the extensive fossil and molecular dates of the original
papermdashavailable for 80 of the nodesmdashin a Bayesian frame-
work (see supplementary methods in Cantalapiedra et al 2014b)
Interestingly by using this tree distribution we incorporate broad
topological and temporal uncertainties into our phylogenetic-rates
analyses Second we estimated speciation rates from the Bayesian
tree distribution in Bibirsquos recent study (2013) Twelve percent of
the nodes were calibrated using priors based on a conservative in-
terpretation of the fossil record Thus the node ages in Bibirsquos tree
are significantly younger than those obtained by Cantalapiedra
et al (2014b) We used two tree distributions with different node-
age arrangements to identify how disparate node-age configura-
tions may impact the fit with the fossil record For simplicity we
will refer to these two datasets as ldquoBibirdquo and ldquoCantalapiedrardquo
To estimate time series of phylogenetic diversification dy-
namics we carried out a time windows analysis (Simpson et al
2011) We estimated speciation every 1 myr window For each
window speciation rate was calculated using the yuleWindow
function in the LASER (Rabosky 2006) package in R (R Devel-
opment Core team 2015) in which yuleWindow fits a pure birth
Yule model based on the distribution of nodes and branch lengths
(Simpson et al 2011) This means it does not estimate an ex-
tinction parameter Nevertheless the waiting times contained in
evolutionary trees that yuleWindow measures should reflect net
diversification (speciation minus extinction λ minus μ Harvey et al
1994a) Other available maximum likelihood methods (Stadler
2011b) allow estimating extinction directly However to estimate
accurate rates such methods require at least 30 branching events
per time slice (Jetz et al 2012) In our dataset this would imply
limiting our analyses interval to the last 10 myrmdashwith two 5 myr
time slicesmdashor the last 6 myrmdashwith three 2 myr times slices A
speciation time series was calculated for 500 trees of each tree
distributions Each of the 1000 curves was retained for plotting
and for individual correlation test with fossil-derived rates
ANALYSIS OF THE RUMINANT FOSSIL RECORD
Information of ruminant species occurrences in the fossil record
was compiled from the New and Old Worlds (NOW) database
(Fortelius 2015) and the Paleobiology Database (Alroy 2015)
both accessed in July 2014 Taxa not identified at the species level
were excluded (1763 occurrences see Supporting Information for
their temporal distribution) Subsequently the combined database
was completed and refined with information from the literature
(see Supporting Information) and information on synonyms pro-
vided by the NOW collaborators Finally we gathered a database
containing 9234 occurrences of 1246 ruminant species whose
record spans the last 50 myr (Fig 1 see also Dataset S1 in Dryad
repository) Species belonging to the six extant families (8558
occurrences of 1100 species) represent around 88 of ruminant
fossil diversity being recorded continuously since around 24 Ma
and making most of the ruminant fossil record since around 20
Ma (Fig 1) Significant gaps in the fossil record were identified
for Tragulidae Leptomerycidae Gelocidae Blastomerycidae
and Moschidae (noncontinuous colors in Fig 1) We performed
an estimation of the quality of the ruminant fossil record by
exploring the temporal distribution of fossil occurrences their
assigned temporal range and the preservation rate through time
(Alroy 2008 Simpson et al 2011 Supporting Information
Fig S1)
EVOLUTION NOVEMBER 2015 2 9 4 3
JUAN L CANTALAPIEDRA ET AL
FOSSILS-BASED EVOLUTIONARY RATES
We assessed relevant evolutionary rates (speciation and extinc-
tion) from the ruminant fossil record using two methods First
we used the most recent version of Alroyrsquos ldquothree-timersrdquo-based
equations (Alroy 2014) This method uses a four-interval moving
window that has been proved to be robust toward noise produced
by high turnover andor poor sampling The method incorporates
the interval-to-interval variation of preservation rate (see Sup-
porting Information) Alroyrsquos rates were estimated after dividing
the analysis interval in 1 myr bins To test the significance of
the evolutionary rates our dataset was bootstrapped with replace-
ment 5000 times using species occurrences as sampling units
Because occurrence data are usually assigned to temporal ranges
broader than 1 myr for each bootstrap occurrences were randomly
assigned to one of the 1 myr bins falling within their temporal
ranges We did this to include all the temporal uncertainty in our
analyses For each time bin we estimated the mean rate (Finarelli
and Badgley 2010)
Additionally to the bin-based method (three-timers) we es-
timated speciation extinction and net diversification from the
fossil record using a birthndashdeath MCMC analyses in a Bayesian
framework (BDMCMC as implemented in PyRate Silvestro et al
2014ab) The BDMCMC algorithm uses fossil occurrences data
to simultaneously estimate speciation and extinction times for
each species while finding the birthndashdeath model that better fits
the fossil record (Silvestro et al 2014ab) The model also incorpo-
rates sampling and the BDMCMC algorithm explores alternative
diversification models with different number of rate shifts (Silve-
stro et al 2014b) Importantly the method is robust toward data
incompleteness and is capable to recover a wide array of rates-
shift scenarios We randomly resampled the age of fossil occur-
rences from the occurrence intervals (from uniform distributions)
10 times using the R function extractages included in the PyRate
files Each replicate was analyzed independently for 10000000
generations using Python 26 in the Computational Cluster Trueno
at the CSIC We set the extant number of species to 197 the num-
ber of species of our bigger tree and allowed the preservation
rates to change across lineages following a gamma distribution
Mean rates through time were estimated after discarding the 20
of the logged rate estimates as burn-in and combining the results
from the 10 independent runs
Both Alroyrsquos method and the BDMCMC algorithm were used
to analyze the complete fossil record of crown ruminants (9186
occurrences see Fig 1) and the fossil record of the six living
ruminant families (8558 occurrences) We followed Metais and
Vislovokowa (2007) and considered crown ruminants all families
except Hypertragulidae Lophiomerycidae and Archaeomeryci-
dae (Fig 1) Some authors have considered the Eocene forms
Archaeotragulus and Krabitherium to belong to the extant family
Tragulidae (but see Sanchez et al 2010) thus implying a 10 myr
gap in the fossil record (from around 33 to 24 Ma see Fig 1) that
would certainly yield misleading rate estimates from this time
interval Thus we exclude these two genera from the six living
families fossil occurrences subset
We used PyRate to estimate fossil-based origination times
of the crown ruminants the pecoransmdashthe ldquomodern ruminantsrdquo
which usually have horns and include five of the six living fam-
ilies (Bibi 2014)mdashand the groups with horned forms (Fig 1)
This was done by extracting the posterior samples of the ages
of origin of the fossil species of interest derived from all occur-
rences replicates after modeling the fossil sampling process and
accounting for the uncertainties around the estimated ages of first
occurrences (Silvestro et al 2015) Thus these estimates predate
the oldest fossil occurrence of each group Then we fitted normal
lognormal and gamma distributions to these dates and choose the
best fit based on the Akaike Information Criterion (Burnham and
Anderson 2002) In this way we obtain origin age estimates that
may ease the discussion on evolutionary patterns and distribution
parameters that may be used in future phylogenetic analyses as
node-age priors (Silvestro et al 2015)
Net diversification was estimated as speciation minus ex-
tinction When the term ldquonet diversificationrdquo is used we refer to
this balance The term ldquodiversificationrdquo may be sometimes used
regarding evolutionary rates in a broader sense
CORRELATION OF THE TREE-BASED AND
FOSSILS-BASED CURVES
So far comparisons between evolutionary rates from fossil oc-
currence data and living species phylogenies have mostly relied
on pure visual and descriptive inspections (Simpson et al 2011)
Here to test whether curves are in phase with one another we
used Kendallrsquos correlation tests (Hammer and Harper 2006) This
method has been extensively applied to temporal series (Hammer
and Harper 2006 Mannion et al 2010) and assesses whether
the peaks and troughs correspond between two curves That is
it will here measure the concordance in shifts in evolutionary
rates
Because we aim to explore the impact of different node-age
configurations on the fit with fossil-derived curves we estimated
Kendallrsquos correlations between each of the 1000 rate curves ob-
tained from living-species phylogenies (500 from the trees in
Cantalapiedra and 500 from Bibi) and the mean fossil-derived
speciation and net-diversification curves estimated for the crown
ruminants using Alroyrsquos method and PyRate The correlation tests
were repeated using the fossil-derived curves (speciation and net
diversification from Alroyrsquos method and the BDMCMC analysis)
obtained from the fossil record of the six surviving ruminant fam-
ilies This was done to empirically assess whether the congruence
between fossil-based and tree-based rates is independent of the
inclusion of clades without phylogenetic representation in cases
2 9 4 4 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
where the extant families hold much of the fossil record A total
of 8000 Kendallrsquos correlations were estimated
To visualize the results we plotted the density distributions of
the P-values (for significance) and Kendallrsquos taus (τ for the sense
of the correlation) To explore whether different node-age arrange-
ments influence the correlation with the fossil record we plotted
P-values and taus obtained from each correlation test against the
mean node age of the 25 older and 25 younger nodes of the tree
involved To help data interpretation we fitted loess curves with
smoothing parameters estimated by generalized cross-validation
to avoid over-fitting to the data (Kohn et al 2000)
ResultsPHYLOGENETIC RATES
The two tree distributions encompass a wide array of node-age
configurations (Fig 2A) Nevertheless both datasets show a very
similar profile The speciation curves obtained from the two tree
distributions show a first pulse related to pecoran and tragulid
basal splits and a second part corresponding with the large radi-
ation within the six living families The deepest trees place the
first pulse in the early Oligocene (32 Ma) and the beginning
of within-family radiations in the Oligocene-Miocene (24 Ma)
The trees with younger node agesmdashmainly Bibirsquos distributionmdash
place these events in the early Miocene (20 Ma) and middle
Miocene (15 Ma) respectively In both tree distributions a slow-
down follows the second big burst followed by a recoverymdashwith
a synchronic peak in both datasets around 7 Mamdashand a final
slowdown toward the present (Bibirsquos dataset shows a recovery in
the Plio-Pleistocene Fig 2A)
RATES FROM FOSSIL OCCURRENCES
Rates estimated from fossil occurrences (net diversification spe-
ciation and extinction) obtained from the ldquothree-timersrdquo method
and the BDMCMC are depicted in Fig 2B and C respectively
Patterns of net diversification are congruent between both ap-
proaches although the speciation and extinction processes differ
in some aspects
According to the ldquothree-timersrdquo method important speci-
ation pulses are recovered during the middle and late Eocene
(45 Ma Fig 2B) and the Eocene-Oligocene boundary (34 Ma)
featured high extinction and speciation The early Oligocene is
characterized by overall neutral net diversification and turnovermdash
low extinction and very slow speciationmdash(Fig 2B) At the
end of the Oligocene net-diversification rates peaked again re-
maining high across the Oligocene-Miocene boundary (around
24 Ma) Speciation decelerated afterwards From about 20 Ma
onwards several speciation and extinction peaks render a rela-
tively constant turnover A negative net-diversification peak is
recovered around 15 Ma followed by a recovery between 12 and
10 Ma The Miocene to Pliocene transition marks a peak of the
replacement rate stemming from an episode of elevated specia-
tion and extinction rates (Fig 2B) Afterwards net diversification
increased again in part due to low extinction at the beginning
of the Pliocene Due to the ldquothree-timersrdquo methodology net di-
versification cannot be recovered from the last three bins of the
analysis interval
The BDMCMC analyses reveal high and maintained specia-
tion rates of crown ruminant lineages throughout the Eocene the
Oligocene and the earliest Miocene (Fig 2D) This high specia-
tion was coupled with elevated extinction rates particularly severe
in the late Eocene and much of the Oligocene (between 47 and
26 Ma) The confidence intervals are broad until around 26 Ma
probably due to the large occurrence temporal ranges (Fig S1)
The diversification maximum at the Oligocene-Miocene bound-
ary is here a result of decelerating extinction and sustained
high speciation The end of the net-diversification pulse around
20 Ma was rendered by a slowdown in speciation rates Moderate
speciation and extinction characterized much of the Miocene Ex-
tinction and speciation recovered around 8 and 6 Ma respectively
Whereas speciation stayed constant until the present extinction
intensely peaked during the last two million years resulting in the
most severe negative net-diversification pulse of the analysis in-
terval Gamma distributions best fitted the time of origin of crown
ruminants (offset = 4263 shape = 176 rate = 046 mean =4647 95 highest posterior density (HPD) = 4285ndash5224) pec-
orans (offset = 2696 shape = 168 rate = 057 mean = 2990
95 HPD = 2704ndash3330) and groups with horned forms (offset
= 2649 shape = 202 rate = 196 mean = 2751 95 HPD =2656ndash2906 Fig 2C)
CURVE CORRELATIONS
The results of the 8000 Kendallrsquos correlations are shown in
Figure 3 When the ldquothree-timersrdquo were used to estimate fossil-
based evolutionary rates the speciation rates based on the deepest
treesmdashfrom Cantalapiedrarsquos tree distributionmdashshowed high con-
gruence with the speciation in fossil crown Ruminantia and with
speciation and net diversification in the fossil lineages of the liv-
ing groups These correlations seemed unaffected by the different
node ages of the tree set Only the rate curves obtained from
the oldest trees showed significant correlationmdashand high positive
tausmdashwith the net-diversification curve of the crown fossil ru-
minants Speciation rates estimated from Bibirsquos trees correlated
positively with speciation in the fossil lineages of the living ru-
minant families This correlation is weaker for the trees whose
deeper nodes are younger
Rates calculated from tree distribution in Cantalapiedra cor-
related positively with speciation and net diversification in the
fossil record of the six living families as estimated by the BDM-
CMC algorithm (Fig 3GndashL) Only rates in Bibirsquos deepest trees
EVOLUTION NOVEMBER 2015 2 9 4 5
JUAN L CANTALAPIEDRA ET AL
groups withhorned forms
crown pecoranscrown ruminantsfirst fossil horns
times of origin(density)
05
0
A
B
C
D
00
01
02
03
04
05
50 40 30 20 10 0
tree-
base
d sp
ecia
tion
EOCENE OLIGOCENE MIOCENE PLI PL
50 40 30 20 10 0
50 40 30 20 10 0
EOCENE OLIGOCENE MIOCENE PLI PL
BibiCantalapiedra et al
-025
000
025
050
075
lsquothre
e-tim
ersrsquo
rate
s net-diversificationnet-div living familiesspeciationextinction
-03
00
03
06
Time (Ma)
PyR
ate
rate
s
inception offirst C3 grasslands
inception offirst C4 grasslands
permanentEAIS
onset ofmodern glaciations
Bering Strait
ArabianConnection
net-diversificationnet-div living familiesspeciationextinction
Figure 2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants (A) Tree-based speciation
rates estimated from 1000 living species phylogenies from Bibi (2013) and Cantalapiedra et al (2014b) The shadowed area represents the
95 confidence intervals (B) Net diversification speciation and extinction in fossil crown ruminants estimated using the ldquothree-timersrdquo
method (Alroy 2014) (C) Estimated times of origins of crown ruminants pecorans (advanced ruminants) and groups with horned forms
according to PyRate (D) Net diversification speciation and extinction in fossil crown ruminants estimated using PyRate (Silvestro et al
2014a) In (B) and (D) net diversification in fossil lineages of the living groups is shown in light blue Shadowed areas in (B) and (D)
represent the 95 confidence interval for the net diversification The first record of horned ruminants (gray) is based on DeMiguel et al
(2014) Mayor tectonic climatic and ecological episodes (Cerling et al 1997 Zachos et al 2008 Stromberg 2011) are shown in colors
EAIS East Antarctic Ice Sheet Pli Pliocene Pl Pleistocene Ma million years ago
showed a significant positive correlation with PyRatersquos speciation
and net diversification in the fossil record of the living groups
Phylogenetic rates from this tree set correlated negatively with
speciation in fossil crown ruminants A negative correlation was
found also with the net diversification of the fossil crown rumi-
nants for the younger trees in Bibirsquos dataset
DiscussionPast evolutionary processes left a congruent signal in the fossil
record and the phylogeny of the living ruminants The concor-
dance was stronger when fossil-based rates were estimated from
paleontological data of the living groups only (Figs 2 and 3) We
2 9 4 6 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Figure 3 Congruence of tree-based and fossils-based rates from the ldquothree-timersrdquo method (AndashF) and PyRate (GndashL) Density plots of
P-values (A) P-values from Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (B) and younger nodes (C)
of each tree Density plots of ldquotausrdquo (τ) (D) ldquotausrdquo Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (E)
and younger nodes (F) of each tree Same plots for P-values and taus when phylogenetic rates were compared with PyRate results (GndashL)
In each plot continuous LOESS lines represent results for trees in Cantalapiedra et al (2014b) and dashed lines results for Bibirsquos trees
(Bibi 2013) Dark blue and light blue fits of phylogenetic rates with net diversification in fossil lineages of crown ruminants and living
groups respectively Dark green and light green fits of phylogenetic rates with speciation in fossil lineages of crown ruminants and
living groups respectively Circles and triangles in plates A D G and J represent the medians of the parameter values of correlations for
trees in Cantalapiedra et al (2014b) and Bibi (2013) respectively
found less agreement in comparisons that used the entire fossil
record of crown ruminants where correspondences among dif-
ferent phylogenetic datasets and fossil-based methodsmdashldquothree-
timersrdquo and PyRatemdashperformed disparately (Fig 3) This is not
surprising given the nature of the evolutionary processes them-
selves and the particularities and limitations of each of the meth-
ods used in this study to recover the past Despite the many com-
parisons among rate profiles conducted here (ie two different
tree distributions two fossil-based methods two different fossil
subsets) we obtained unambiguous results about their fit through
a large array of different phylogenetic trees (Fig 3)
The capacity of living ruminant phylogenies to reconstruct
the most basal events of ruminant evolution (the Eocene and
Oligocene from around 50 to 24 Ma) critically determines the
extent to which they match evolutionary rates estimated from
the fossil record Reconstructed branching events in living ru-
minant trees are scarce during this early stage of the analysis
interval yielding very low speciation rates (Fig 2A) On top
of this different interpretations of our large fossil data (ie a
discrete-bin-based approach and a birthndashdeath Bayesian algo-
rithm) portrait disparate evolutionary scenarios for this period
(especially regarding speciation rates green curves in Fig 2B and
D) The ldquothree-timersrdquo approach reconstructed overall low specia-
tion and moderate-to-negative net diversification in the 50ndash24 Ma
temporal span Only one relevant speciation event was estimated
around 40 Ma (Fig 2B) This is a more literal read of the fossil
EVOLUTION NOVEMBER 2015 2 9 4 7
JUAN L CANTALAPIEDRA ET AL
record than that offered by PyRate (see below) The interpretation
of an early evolutionary calm before the big Miocene radiation
fits better the classic paleontological view (based on fossil ranges
and raw diversity curves Janis et al 2000 Costeur and Legendre
2008 Maridet and Costeur 2010) and the phylogenetic inferences
(Fig 2A and B) The two tree distributions yielded confidence
intervals that overlap with zero in this temporal span Thus when
the ldquothree-timersrdquo method was used the correlation between tree-
based rates and fossil speciation of the crown ruminants was
strong for most of the trees in the Cantalapiedra dataset and some
of Bibirsquos trees
PyRatersquos BDMCMC algorithm estimates a different scenario
for the first 25 myr of ruminant evolution especially with respect
to speciation rates (compare green curves in Fig 2B and D)
Unsurprisingly this notably influenced the congruence with phy-
logenetic rates (Fig 3GndashL) The BDMCMC approach places the
highest speciation rates in the Eocene Oligocene and earliest
Miocene (45ndash22 Ma Fig 2D) As a result PyRate speciation and
diversification estimates for the fossil crown ruminants yielded
a poor fit with our phylogenetic rates which show their low-
est values in this temporal span (Fig 2A) This striking differ-
ence with respect to the ldquothree-timersrdquo rates could be explained
by a deficient sampling rate (especially low for the Oligocene
Fig S1) Surprisingly although the BDMCMC algorithm (after
modeling the sampling to estimate the corrected life span of each
lineage Silvestro et al 2014a) showed high speciation rates it
still estimated accelerated extinction rates between 37 and 26 Ma
(Fig 2C) In this regard both methods agree suggesting that we
are recovering a true macroevolutionary signal and that the esti-
mate of high extinction rates is probably robust toward sampling
Although Alroyrsquos method yielded negative Eocene and
Oligocene diversification rate and subsequent diversity lossmdash
also visible in the raw diversity plot (Fig 1)mdashPyRate revealed
a scenario where net diversification slowed down but remained
positive Nonetheless PyRate yielded broad confidence intervals
for this temporal span suggesting other scenarios should not be
discarded The high Eocene-Oligocene speciation and extinction
rates should have rendered a profound replacement in ruminant
faunas This result is consistent with the high turnover previously
reported in Eurasian faunas (the so-called ldquoGrand Coupurerdquo
Janis 2008 Springer et al 2012) which has been associated with
cooler and more arid conditions in early Oligocene terrestrial
habitats (Mosbrugger et al 2005 Zachos et al 2008) However
understanding the impact of the Oligocene new environmental
context in mammalian communities demands further exploration
A comprehensive characterization of dietary shifts in Oligocene
ruminant lineages will be very insightful in this regard (Blondel
2001) Interestingly the Oligocene extinction peak is clearly
reflected by the trees as a prolonged period of low branching
rate (Fig 2A) We suggest that this lineage depletion marked the
shape of the living ruminants tree to a great extent restricting
the number of lineages that it recovers from the Eocene and
Oligocene (Fig 2) This provides an empirical proof of the
footprint that prolonged and high extinction rates leave in living
species phylogenies (Harvey et al 1994b Morlon et al 2011)
A major net-diversification pulse is robustly recovered from
both the fossil record and the phylogenetic trees during the
late Oligocene and early Miocene (27ndash22 Ma Fig 2) Al-
though the two fossil-based approaches show an increase in net-
diversification rates paired with low extinction they differ in
the macroevolutionary context of such major net-diversification
peaks Alroyrsquos method depicts accelerating speciation rates as ru-
minant lineages approached the Oligocene-Miocene limit PyRate
suggests that the high speciation rates represent continuity with
regard to Eocene and Oligocene times and that extinction would
have dropped as modern groups evolved around 27 Ma (Fig 2C
and D) This moment marked the shift toward a second major
stage of ruminant evolution the dominion of the ldquoadvancedrdquomdash
mostly hornedmdashruminants the pecorans (see Fig 1 and further
discussion below) The major radiation encompassed the appear-
ance of several living and extinct groups and a rapid accumulation
of species diversity (Fig 1) Extant groups may have exhibited
early Miocene rates above those estimated for the crown group
as a whole (Fig 2D) As a result ruminant diversity was rapidly
dominated by living groups since the early Miocene until today
(Fig 1 Costeur and Legendre 2008 Maridet and Costeur 2010)
Indeed diversification rates in fossil lineages of the crown and the
living families are very similar for the rest of the analysis interval
(Figs 2 and S2) This preponderance is also congruent with the
high agreement found between fossil-derived rates and phylo-
genetic rates in the last 25 myr of the study interval Correla-
tions showed significant concordance among curves from differ-
ent fossil-based methods and tree distributions when the fossil
record of the living groups was used (Fig 3) Only the youngest
trees from Bibirsquos dataset show nonsignificant fits Overall as early
Miocene net diversification recovered after a prolonged period of
high extinction the concordance between the macroevolutionary
signal in the fossil record and our phylogenetic data significantly
increased
After the Oligocene-Miocene diversification burst specia-
tion and net diversification significantly declined However only
trees from the dataset in Cantalapiedra et al show a comparable
pattern (Fig 2) There are two potential explanations for this out-
come First the middle Miocene (17ndash12 Ma) was indeed a period
of relatively low macroevolutionary rates and the younger trees
within Bibirsquos dataset are simply too young to reflect the true trend
Second Bibirsquos trees correctly reflect the timing of speciation of
crown living lineages whereas the other sources are recovering
the speciation of stem and crown living families combinedmdash
our fossil data include stem forms If true this second scenario
2 9 4 8 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
implies that high branching rates in living species trees may not
fit the rates estimated from the fossil record where a distinction
of crown and stem forms is very problematic even in a group with
a well-known fossil record as the ruminants (Sanchez et al 2011
Bibi 2014) Thus in cases where there is a significant temporal
lag between the diversification of stem and crown lineagesmdashas it
may be the case heremdashthe selection of true crown fossil calibra-
tion points is crucial (Bibi 2013) In this regard new total-evidence
methods (ldquotip-datingrdquo Ronquist et al 2012 Grimm et al 2015)
are contributing to overcome this issue by placing fossils within
the phylogenetic trees based on morphology while using them
to estimate divergence times (Ronquist et al 2012) Future total-
evidence analyses based on molecular data and morphology of
living and fossil ruminants will clarify this disagreement
The great diversification pulse of the Oligocene-Miocene
and the following deceleration of speciation rates may contribute
a first-hand empirical proof of the impact of ecological limits on
postradiation evolutionary rates (Moen and Morlon 2014 Harmon
and Harrison 2015) According to paleontological and paleocli-
matic evidences the Paleogene-Neogene transition was a period
of profound change in terrestrial ecosystems New available adap-
tive space was probably created by important shifts in Oligocene
and early Miocene climate (Bruch et al 2007 Eronen et al 2010)
environments (Stromberg 2011) and tectonicsmdashfor example ru-
minants entered Africa for the first time (Maglio 1978) Under this
view speciation rates would have slowed down as the adaptive
space filled Importantly extinction rates remained at basal levels
showing that the Miocene slowdown in the living ruminant tree is
rendered at the end of an expansion phase of the modern forms and
not by extinction increasing above speciation (Moen and Morlon
2014) Distinguishing between these alternatives is challenging
if just living species trees are used (Rabosky and Lovette 2008)
Ecological saturation occurs at the species level and only evolu-
tionary rates estimated from species-level fossil occurrence data
should be used to address such questions precisely (Harmon and
Harrison 2015) In this regard our fossil-based analyses provide
valuable support to previous conclusions built on neontological
information and simulations (Rabosky and Lovette 2008)
Ruminant faunas underwent critical macroevolutionary pro-
cesses in the last 10 million years (Fig 2) The fossil data sug-
gest an increase of extinction from that time onwards and a later
rebound of speciation rates Estimates from the ldquothree-timersrdquo
method and PyRate fit showing neutral-to-negative net diversi-
fication that translated into a late Miocene diversity loss Phylo-
genetic rates remained steady or slightly decreased Overall we
do not recognize a direct resemblance among curves in this tem-
poral point Nevertheless it may be the case that late Miocene
depletion also contributed to the low branching rates recovered
earlier in the trees (15ndash10 Ma see Rabosky and Lovette 2008) If
the Oligocene prolonged extinction erased most of the branches
before 30 Ma the late Miocene diversity loss may also have pre-
vented part of the evolutionary signal from the middle Miocene
to be recorded in the living species trees (Harvey et al 1994a)
We rule out the possibility that this extinction pulse is an artifact
derived from poor sampling Preservation rates of the ruminant
fossil record are relatively high for the late Miocene (around 075
Fig S1) Furthermore the two methods used to analyze the fossil
data account for heterogeneous sampling in very different ways
and yet yield very similar results with tight confidence intervals
(Fig 2) Our results show a recovery in speciation during the latest
Miocene and the Pliocene from around 7 to 25 Ma Late Pliocene
speciation rebound to levels comparable to the early Miocene As
argued above this recovery probably is reflected by the trees with
nodes slightly deeper in time due to the deeper molecular esti-
mates toward the Miocene-Pliocene Very likely mainly bovids
and deer lineages led that speciation pulse including the radiation
of American deer and that of African bovid tribes (Bibi et al
2009 Cantalapiedra et al 2014c)
The Plio-Pleistocene was one of the most dramatic episodes
in ruminant evolution A critical net diversification drop recov-
ered from the fossil record couples a slowdown in the phylogenetic
rates toward the end of our analysis interval (Fig 2) Fossil-based
rates for the last 2 myrmdashonly provided by PyRate see Methodsmdash
exhibited a severe extinction event Speciation rate still remained
close to early Miocene levels during this period but extinction
significantly surpassed it (Fig 2D) The resulting replacement
process would have reshaped ruminant faunas faster than ever
The idea of a major Plio-Pleistocene climatic shift (the estab-
lishment of continental northern-hemisphere glaciations Miller
et al 2005) and human activity reshaping mammalian faunas have
been proposed for several mammalian clades (Delson 1985 Kim-
bel 1995 Lyons et al 2004 Gomez Cano et al 2013) These
suggestions are supported by our results
To our knowledge this is the first direct evidence for neg-
ative net diversificationmdashextinction above speciationmdashas being
behind the slowdowns in living species trees toward the tips often
reported in the literature (Moen and Morlon 2014) This empir-
ical case opens the possibility that indeed progressive decrease
in phylogenetic rates toward recent times may in some cases
be the result of recent and drastic climatic fluctuations triggering
extinction
Concluding remarks
Since the first studies on tree shape (Nee et al 1992 Harvey
et al 1994b) an extensive body of research has been devoted to
understand how evolutionary processes leave their signal in phy-
logenetic trees of extant taxa Most researchers have focused on
estimate evolutionary ratesmdashthat is speciation and extinctionmdash
from phylogenies of living species (Rabosky and Lovette 2008
Alfaro et al 2009 Stadler 2011a) Other studies have pursued
EVOLUTION NOVEMBER 2015 2 9 4 9
JUAN L CANTALAPIEDRA ET AL
the identification of past episodes in evolutionary trees by com-
parison with simulations (Crisp and Cook 2009) Surprisingly
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data Quental and Marshall 2010 Morlon
et al 2011 Etienne et al 2012) Simpson et al (2011) compared
phylogenetic rates with fossil-based rates but the correlation be-
tween curves was not tested statistically Here we have shown
how the combination of speciation and extinction as recovered
from the fossil record left a signal in the living species phylogeny
of ruminants through 50 myr of evolution Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved Also the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90 of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig 1) We
acknowledge that this might not be the case scenario for many
study groups
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive rep-
resentation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12) Also
calibrating phylogenies using highly tight and conservative fossil-
informed priors may not yield rate profiles that fit rates through
time from the fossil record because the major pulses in lineage
speciation may have taken place in stem lineages
Our results also provide new views on ruminant evolution
that should be contrasted in the future The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small hornless and browser forms that were
not involved in any extraordinary diversification pulse (ldquothe lull
before the stormrdquo Janis 2008) This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1 These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007) In contrast our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig 2C)
Our analyses strongly suggest that the classic ldquoMiocene ru-
minant radiationrdquo begun in Oligocene times and prolonged until
22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-
ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition
of larger body sizes (Morales et al 1993) new dietary strate-
gies (Cantalapiedra et al 2014b) and behavior (Janis 1982 1989
Brashares et al 2000) However this event and the estimated
origin of ruminant groups with horned forms (275 Ma) largely
predates the first fossil evidence of horns in ruminants (19ndash17
Ma see DeMiguel et al 2014 Fig 2C) This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al 2014) or
those horned ruminants are to be found in the Oligocene
Finally since little can be recovered from living species trees
about the first 25 myr of ruminant evolution improving the poor
Eocene and Oligocene fossil record is crucial for future paleobio-
logical studies (Blondel 2001) This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
ldquophylogenetic coveragerdquo due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al
2012 Hipsley et al 2014 McGuire et al 2014) In summary
unveiling Paleogene environmental trends and mammal commu-
nitiesrsquo dynamics will largely benefit from fossil data And basal
ruminants probably have a lot to teach us about it
ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education
DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)
LITERATURE CITEDAlfaro M E F Santini C Brock H Alamillo A Dornburg D L Rabosky
G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414
Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542
mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge
mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397
mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014
2 9 5 0 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
EVOLUTION NOVEMBER 2015 2 9 5 1
JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Molecular estimates suggest that crown ruminants probably ap-
peared in the Eocene 45ndash40 Ma (Meredith et al 2011 Bibi
2013) but the radiation of the living groups mainly took place
in the last 30ndash20 myr (DeMiguel et al 2014) Thus we expect
higher concordance between rates from the two sources during the
last half of the study interval Furthermore the characterization
of the speciation-extinction interplay across such radiation using
living-taxa trees and extensive fossil datamdashboth at the species
levelmdashmay sum to the debate on ecological limits and their im-
pact on postradiation evolutionary rates (Rabosky and Lovette
2008 Moen and Morlon 2014 Harmon and Harrison 2015)
Ruminants have played a paramount role in terrestrial ecosys-
tems and their evolutionary history is relatively well known (for
recent reviews see Cantalapiedra et al 2014a Clauss and Rossner
2014 DeMiguel et al 2014) Due to their sensitivity to habitat
change ruminants have being commonly used as paleoecologi-
cal proxies (Bobe and Eck 2001 Hernandez Fernandez and Vrba
2006 Kaiser and Rossner 2007) However their macroevolution-
ary patterns are only known from raw diversity curves that are
temporal and spatially fragmentary (Vrba 1995 Blondel 2001
Costeur and Legendre 2008 Maridet and Costeur 2010 Clauss
and Rossner 2014) We here present the first estimate of diver-
sification trends of this large clade of terrestrial mammals at the
global scale Because ruminants are a habitat-informative clade a
detailed study of their diversification patterns may also have im-
portant implications for unveiling past environmental shifts within
mammalian communities during the Cenozoic
MethodsTIME SERIES OF DIVERSIFICATION FROM THE TREE
OF LIVING RUMINANTS
For comparison we estimated phylogenetic speciation rates
through time from two different tree distributions First we drew
on a recently published distribution of resolved and recalibrated
trees (Cantalapiedra et al 2014b) based on the topology pre-
sented by Hernandez Fernandez and Vrba (2005) which includes
all living ruminant species This tree distribution was obtained
by randomly resolving polytomies and recalibrating the nodes
using the extensive fossil and molecular dates of the original
papermdashavailable for 80 of the nodesmdashin a Bayesian frame-
work (see supplementary methods in Cantalapiedra et al 2014b)
Interestingly by using this tree distribution we incorporate broad
topological and temporal uncertainties into our phylogenetic-rates
analyses Second we estimated speciation rates from the Bayesian
tree distribution in Bibirsquos recent study (2013) Twelve percent of
the nodes were calibrated using priors based on a conservative in-
terpretation of the fossil record Thus the node ages in Bibirsquos tree
are significantly younger than those obtained by Cantalapiedra
et al (2014b) We used two tree distributions with different node-
age arrangements to identify how disparate node-age configura-
tions may impact the fit with the fossil record For simplicity we
will refer to these two datasets as ldquoBibirdquo and ldquoCantalapiedrardquo
To estimate time series of phylogenetic diversification dy-
namics we carried out a time windows analysis (Simpson et al
2011) We estimated speciation every 1 myr window For each
window speciation rate was calculated using the yuleWindow
function in the LASER (Rabosky 2006) package in R (R Devel-
opment Core team 2015) in which yuleWindow fits a pure birth
Yule model based on the distribution of nodes and branch lengths
(Simpson et al 2011) This means it does not estimate an ex-
tinction parameter Nevertheless the waiting times contained in
evolutionary trees that yuleWindow measures should reflect net
diversification (speciation minus extinction λ minus μ Harvey et al
1994a) Other available maximum likelihood methods (Stadler
2011b) allow estimating extinction directly However to estimate
accurate rates such methods require at least 30 branching events
per time slice (Jetz et al 2012) In our dataset this would imply
limiting our analyses interval to the last 10 myrmdashwith two 5 myr
time slicesmdashor the last 6 myrmdashwith three 2 myr times slices A
speciation time series was calculated for 500 trees of each tree
distributions Each of the 1000 curves was retained for plotting
and for individual correlation test with fossil-derived rates
ANALYSIS OF THE RUMINANT FOSSIL RECORD
Information of ruminant species occurrences in the fossil record
was compiled from the New and Old Worlds (NOW) database
(Fortelius 2015) and the Paleobiology Database (Alroy 2015)
both accessed in July 2014 Taxa not identified at the species level
were excluded (1763 occurrences see Supporting Information for
their temporal distribution) Subsequently the combined database
was completed and refined with information from the literature
(see Supporting Information) and information on synonyms pro-
vided by the NOW collaborators Finally we gathered a database
containing 9234 occurrences of 1246 ruminant species whose
record spans the last 50 myr (Fig 1 see also Dataset S1 in Dryad
repository) Species belonging to the six extant families (8558
occurrences of 1100 species) represent around 88 of ruminant
fossil diversity being recorded continuously since around 24 Ma
and making most of the ruminant fossil record since around 20
Ma (Fig 1) Significant gaps in the fossil record were identified
for Tragulidae Leptomerycidae Gelocidae Blastomerycidae
and Moschidae (noncontinuous colors in Fig 1) We performed
an estimation of the quality of the ruminant fossil record by
exploring the temporal distribution of fossil occurrences their
assigned temporal range and the preservation rate through time
(Alroy 2008 Simpson et al 2011 Supporting Information
Fig S1)
EVOLUTION NOVEMBER 2015 2 9 4 3
JUAN L CANTALAPIEDRA ET AL
FOSSILS-BASED EVOLUTIONARY RATES
We assessed relevant evolutionary rates (speciation and extinc-
tion) from the ruminant fossil record using two methods First
we used the most recent version of Alroyrsquos ldquothree-timersrdquo-based
equations (Alroy 2014) This method uses a four-interval moving
window that has been proved to be robust toward noise produced
by high turnover andor poor sampling The method incorporates
the interval-to-interval variation of preservation rate (see Sup-
porting Information) Alroyrsquos rates were estimated after dividing
the analysis interval in 1 myr bins To test the significance of
the evolutionary rates our dataset was bootstrapped with replace-
ment 5000 times using species occurrences as sampling units
Because occurrence data are usually assigned to temporal ranges
broader than 1 myr for each bootstrap occurrences were randomly
assigned to one of the 1 myr bins falling within their temporal
ranges We did this to include all the temporal uncertainty in our
analyses For each time bin we estimated the mean rate (Finarelli
and Badgley 2010)
Additionally to the bin-based method (three-timers) we es-
timated speciation extinction and net diversification from the
fossil record using a birthndashdeath MCMC analyses in a Bayesian
framework (BDMCMC as implemented in PyRate Silvestro et al
2014ab) The BDMCMC algorithm uses fossil occurrences data
to simultaneously estimate speciation and extinction times for
each species while finding the birthndashdeath model that better fits
the fossil record (Silvestro et al 2014ab) The model also incorpo-
rates sampling and the BDMCMC algorithm explores alternative
diversification models with different number of rate shifts (Silve-
stro et al 2014b) Importantly the method is robust toward data
incompleteness and is capable to recover a wide array of rates-
shift scenarios We randomly resampled the age of fossil occur-
rences from the occurrence intervals (from uniform distributions)
10 times using the R function extractages included in the PyRate
files Each replicate was analyzed independently for 10000000
generations using Python 26 in the Computational Cluster Trueno
at the CSIC We set the extant number of species to 197 the num-
ber of species of our bigger tree and allowed the preservation
rates to change across lineages following a gamma distribution
Mean rates through time were estimated after discarding the 20
of the logged rate estimates as burn-in and combining the results
from the 10 independent runs
Both Alroyrsquos method and the BDMCMC algorithm were used
to analyze the complete fossil record of crown ruminants (9186
occurrences see Fig 1) and the fossil record of the six living
ruminant families (8558 occurrences) We followed Metais and
Vislovokowa (2007) and considered crown ruminants all families
except Hypertragulidae Lophiomerycidae and Archaeomeryci-
dae (Fig 1) Some authors have considered the Eocene forms
Archaeotragulus and Krabitherium to belong to the extant family
Tragulidae (but see Sanchez et al 2010) thus implying a 10 myr
gap in the fossil record (from around 33 to 24 Ma see Fig 1) that
would certainly yield misleading rate estimates from this time
interval Thus we exclude these two genera from the six living
families fossil occurrences subset
We used PyRate to estimate fossil-based origination times
of the crown ruminants the pecoransmdashthe ldquomodern ruminantsrdquo
which usually have horns and include five of the six living fam-
ilies (Bibi 2014)mdashand the groups with horned forms (Fig 1)
This was done by extracting the posterior samples of the ages
of origin of the fossil species of interest derived from all occur-
rences replicates after modeling the fossil sampling process and
accounting for the uncertainties around the estimated ages of first
occurrences (Silvestro et al 2015) Thus these estimates predate
the oldest fossil occurrence of each group Then we fitted normal
lognormal and gamma distributions to these dates and choose the
best fit based on the Akaike Information Criterion (Burnham and
Anderson 2002) In this way we obtain origin age estimates that
may ease the discussion on evolutionary patterns and distribution
parameters that may be used in future phylogenetic analyses as
node-age priors (Silvestro et al 2015)
Net diversification was estimated as speciation minus ex-
tinction When the term ldquonet diversificationrdquo is used we refer to
this balance The term ldquodiversificationrdquo may be sometimes used
regarding evolutionary rates in a broader sense
CORRELATION OF THE TREE-BASED AND
FOSSILS-BASED CURVES
So far comparisons between evolutionary rates from fossil oc-
currence data and living species phylogenies have mostly relied
on pure visual and descriptive inspections (Simpson et al 2011)
Here to test whether curves are in phase with one another we
used Kendallrsquos correlation tests (Hammer and Harper 2006) This
method has been extensively applied to temporal series (Hammer
and Harper 2006 Mannion et al 2010) and assesses whether
the peaks and troughs correspond between two curves That is
it will here measure the concordance in shifts in evolutionary
rates
Because we aim to explore the impact of different node-age
configurations on the fit with fossil-derived curves we estimated
Kendallrsquos correlations between each of the 1000 rate curves ob-
tained from living-species phylogenies (500 from the trees in
Cantalapiedra and 500 from Bibi) and the mean fossil-derived
speciation and net-diversification curves estimated for the crown
ruminants using Alroyrsquos method and PyRate The correlation tests
were repeated using the fossil-derived curves (speciation and net
diversification from Alroyrsquos method and the BDMCMC analysis)
obtained from the fossil record of the six surviving ruminant fam-
ilies This was done to empirically assess whether the congruence
between fossil-based and tree-based rates is independent of the
inclusion of clades without phylogenetic representation in cases
2 9 4 4 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
where the extant families hold much of the fossil record A total
of 8000 Kendallrsquos correlations were estimated
To visualize the results we plotted the density distributions of
the P-values (for significance) and Kendallrsquos taus (τ for the sense
of the correlation) To explore whether different node-age arrange-
ments influence the correlation with the fossil record we plotted
P-values and taus obtained from each correlation test against the
mean node age of the 25 older and 25 younger nodes of the tree
involved To help data interpretation we fitted loess curves with
smoothing parameters estimated by generalized cross-validation
to avoid over-fitting to the data (Kohn et al 2000)
ResultsPHYLOGENETIC RATES
The two tree distributions encompass a wide array of node-age
configurations (Fig 2A) Nevertheless both datasets show a very
similar profile The speciation curves obtained from the two tree
distributions show a first pulse related to pecoran and tragulid
basal splits and a second part corresponding with the large radi-
ation within the six living families The deepest trees place the
first pulse in the early Oligocene (32 Ma) and the beginning
of within-family radiations in the Oligocene-Miocene (24 Ma)
The trees with younger node agesmdashmainly Bibirsquos distributionmdash
place these events in the early Miocene (20 Ma) and middle
Miocene (15 Ma) respectively In both tree distributions a slow-
down follows the second big burst followed by a recoverymdashwith
a synchronic peak in both datasets around 7 Mamdashand a final
slowdown toward the present (Bibirsquos dataset shows a recovery in
the Plio-Pleistocene Fig 2A)
RATES FROM FOSSIL OCCURRENCES
Rates estimated from fossil occurrences (net diversification spe-
ciation and extinction) obtained from the ldquothree-timersrdquo method
and the BDMCMC are depicted in Fig 2B and C respectively
Patterns of net diversification are congruent between both ap-
proaches although the speciation and extinction processes differ
in some aspects
According to the ldquothree-timersrdquo method important speci-
ation pulses are recovered during the middle and late Eocene
(45 Ma Fig 2B) and the Eocene-Oligocene boundary (34 Ma)
featured high extinction and speciation The early Oligocene is
characterized by overall neutral net diversification and turnovermdash
low extinction and very slow speciationmdash(Fig 2B) At the
end of the Oligocene net-diversification rates peaked again re-
maining high across the Oligocene-Miocene boundary (around
24 Ma) Speciation decelerated afterwards From about 20 Ma
onwards several speciation and extinction peaks render a rela-
tively constant turnover A negative net-diversification peak is
recovered around 15 Ma followed by a recovery between 12 and
10 Ma The Miocene to Pliocene transition marks a peak of the
replacement rate stemming from an episode of elevated specia-
tion and extinction rates (Fig 2B) Afterwards net diversification
increased again in part due to low extinction at the beginning
of the Pliocene Due to the ldquothree-timersrdquo methodology net di-
versification cannot be recovered from the last three bins of the
analysis interval
The BDMCMC analyses reveal high and maintained specia-
tion rates of crown ruminant lineages throughout the Eocene the
Oligocene and the earliest Miocene (Fig 2D) This high specia-
tion was coupled with elevated extinction rates particularly severe
in the late Eocene and much of the Oligocene (between 47 and
26 Ma) The confidence intervals are broad until around 26 Ma
probably due to the large occurrence temporal ranges (Fig S1)
The diversification maximum at the Oligocene-Miocene bound-
ary is here a result of decelerating extinction and sustained
high speciation The end of the net-diversification pulse around
20 Ma was rendered by a slowdown in speciation rates Moderate
speciation and extinction characterized much of the Miocene Ex-
tinction and speciation recovered around 8 and 6 Ma respectively
Whereas speciation stayed constant until the present extinction
intensely peaked during the last two million years resulting in the
most severe negative net-diversification pulse of the analysis in-
terval Gamma distributions best fitted the time of origin of crown
ruminants (offset = 4263 shape = 176 rate = 046 mean =4647 95 highest posterior density (HPD) = 4285ndash5224) pec-
orans (offset = 2696 shape = 168 rate = 057 mean = 2990
95 HPD = 2704ndash3330) and groups with horned forms (offset
= 2649 shape = 202 rate = 196 mean = 2751 95 HPD =2656ndash2906 Fig 2C)
CURVE CORRELATIONS
The results of the 8000 Kendallrsquos correlations are shown in
Figure 3 When the ldquothree-timersrdquo were used to estimate fossil-
based evolutionary rates the speciation rates based on the deepest
treesmdashfrom Cantalapiedrarsquos tree distributionmdashshowed high con-
gruence with the speciation in fossil crown Ruminantia and with
speciation and net diversification in the fossil lineages of the liv-
ing groups These correlations seemed unaffected by the different
node ages of the tree set Only the rate curves obtained from
the oldest trees showed significant correlationmdashand high positive
tausmdashwith the net-diversification curve of the crown fossil ru-
minants Speciation rates estimated from Bibirsquos trees correlated
positively with speciation in the fossil lineages of the living ru-
minant families This correlation is weaker for the trees whose
deeper nodes are younger
Rates calculated from tree distribution in Cantalapiedra cor-
related positively with speciation and net diversification in the
fossil record of the six living families as estimated by the BDM-
CMC algorithm (Fig 3GndashL) Only rates in Bibirsquos deepest trees
EVOLUTION NOVEMBER 2015 2 9 4 5
JUAN L CANTALAPIEDRA ET AL
groups withhorned forms
crown pecoranscrown ruminantsfirst fossil horns
times of origin(density)
05
0
A
B
C
D
00
01
02
03
04
05
50 40 30 20 10 0
tree-
base
d sp
ecia
tion
EOCENE OLIGOCENE MIOCENE PLI PL
50 40 30 20 10 0
50 40 30 20 10 0
EOCENE OLIGOCENE MIOCENE PLI PL
BibiCantalapiedra et al
-025
000
025
050
075
lsquothre
e-tim
ersrsquo
rate
s net-diversificationnet-div living familiesspeciationextinction
-03
00
03
06
Time (Ma)
PyR
ate
rate
s
inception offirst C3 grasslands
inception offirst C4 grasslands
permanentEAIS
onset ofmodern glaciations
Bering Strait
ArabianConnection
net-diversificationnet-div living familiesspeciationextinction
Figure 2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants (A) Tree-based speciation
rates estimated from 1000 living species phylogenies from Bibi (2013) and Cantalapiedra et al (2014b) The shadowed area represents the
95 confidence intervals (B) Net diversification speciation and extinction in fossil crown ruminants estimated using the ldquothree-timersrdquo
method (Alroy 2014) (C) Estimated times of origins of crown ruminants pecorans (advanced ruminants) and groups with horned forms
according to PyRate (D) Net diversification speciation and extinction in fossil crown ruminants estimated using PyRate (Silvestro et al
2014a) In (B) and (D) net diversification in fossil lineages of the living groups is shown in light blue Shadowed areas in (B) and (D)
represent the 95 confidence interval for the net diversification The first record of horned ruminants (gray) is based on DeMiguel et al
(2014) Mayor tectonic climatic and ecological episodes (Cerling et al 1997 Zachos et al 2008 Stromberg 2011) are shown in colors
EAIS East Antarctic Ice Sheet Pli Pliocene Pl Pleistocene Ma million years ago
showed a significant positive correlation with PyRatersquos speciation
and net diversification in the fossil record of the living groups
Phylogenetic rates from this tree set correlated negatively with
speciation in fossil crown ruminants A negative correlation was
found also with the net diversification of the fossil crown rumi-
nants for the younger trees in Bibirsquos dataset
DiscussionPast evolutionary processes left a congruent signal in the fossil
record and the phylogeny of the living ruminants The concor-
dance was stronger when fossil-based rates were estimated from
paleontological data of the living groups only (Figs 2 and 3) We
2 9 4 6 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Figure 3 Congruence of tree-based and fossils-based rates from the ldquothree-timersrdquo method (AndashF) and PyRate (GndashL) Density plots of
P-values (A) P-values from Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (B) and younger nodes (C)
of each tree Density plots of ldquotausrdquo (τ) (D) ldquotausrdquo Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (E)
and younger nodes (F) of each tree Same plots for P-values and taus when phylogenetic rates were compared with PyRate results (GndashL)
In each plot continuous LOESS lines represent results for trees in Cantalapiedra et al (2014b) and dashed lines results for Bibirsquos trees
(Bibi 2013) Dark blue and light blue fits of phylogenetic rates with net diversification in fossil lineages of crown ruminants and living
groups respectively Dark green and light green fits of phylogenetic rates with speciation in fossil lineages of crown ruminants and
living groups respectively Circles and triangles in plates A D G and J represent the medians of the parameter values of correlations for
trees in Cantalapiedra et al (2014b) and Bibi (2013) respectively
found less agreement in comparisons that used the entire fossil
record of crown ruminants where correspondences among dif-
ferent phylogenetic datasets and fossil-based methodsmdashldquothree-
timersrdquo and PyRatemdashperformed disparately (Fig 3) This is not
surprising given the nature of the evolutionary processes them-
selves and the particularities and limitations of each of the meth-
ods used in this study to recover the past Despite the many com-
parisons among rate profiles conducted here (ie two different
tree distributions two fossil-based methods two different fossil
subsets) we obtained unambiguous results about their fit through
a large array of different phylogenetic trees (Fig 3)
The capacity of living ruminant phylogenies to reconstruct
the most basal events of ruminant evolution (the Eocene and
Oligocene from around 50 to 24 Ma) critically determines the
extent to which they match evolutionary rates estimated from
the fossil record Reconstructed branching events in living ru-
minant trees are scarce during this early stage of the analysis
interval yielding very low speciation rates (Fig 2A) On top
of this different interpretations of our large fossil data (ie a
discrete-bin-based approach and a birthndashdeath Bayesian algo-
rithm) portrait disparate evolutionary scenarios for this period
(especially regarding speciation rates green curves in Fig 2B and
D) The ldquothree-timersrdquo approach reconstructed overall low specia-
tion and moderate-to-negative net diversification in the 50ndash24 Ma
temporal span Only one relevant speciation event was estimated
around 40 Ma (Fig 2B) This is a more literal read of the fossil
EVOLUTION NOVEMBER 2015 2 9 4 7
JUAN L CANTALAPIEDRA ET AL
record than that offered by PyRate (see below) The interpretation
of an early evolutionary calm before the big Miocene radiation
fits better the classic paleontological view (based on fossil ranges
and raw diversity curves Janis et al 2000 Costeur and Legendre
2008 Maridet and Costeur 2010) and the phylogenetic inferences
(Fig 2A and B) The two tree distributions yielded confidence
intervals that overlap with zero in this temporal span Thus when
the ldquothree-timersrdquo method was used the correlation between tree-
based rates and fossil speciation of the crown ruminants was
strong for most of the trees in the Cantalapiedra dataset and some
of Bibirsquos trees
PyRatersquos BDMCMC algorithm estimates a different scenario
for the first 25 myr of ruminant evolution especially with respect
to speciation rates (compare green curves in Fig 2B and D)
Unsurprisingly this notably influenced the congruence with phy-
logenetic rates (Fig 3GndashL) The BDMCMC approach places the
highest speciation rates in the Eocene Oligocene and earliest
Miocene (45ndash22 Ma Fig 2D) As a result PyRate speciation and
diversification estimates for the fossil crown ruminants yielded
a poor fit with our phylogenetic rates which show their low-
est values in this temporal span (Fig 2A) This striking differ-
ence with respect to the ldquothree-timersrdquo rates could be explained
by a deficient sampling rate (especially low for the Oligocene
Fig S1) Surprisingly although the BDMCMC algorithm (after
modeling the sampling to estimate the corrected life span of each
lineage Silvestro et al 2014a) showed high speciation rates it
still estimated accelerated extinction rates between 37 and 26 Ma
(Fig 2C) In this regard both methods agree suggesting that we
are recovering a true macroevolutionary signal and that the esti-
mate of high extinction rates is probably robust toward sampling
Although Alroyrsquos method yielded negative Eocene and
Oligocene diversification rate and subsequent diversity lossmdash
also visible in the raw diversity plot (Fig 1)mdashPyRate revealed
a scenario where net diversification slowed down but remained
positive Nonetheless PyRate yielded broad confidence intervals
for this temporal span suggesting other scenarios should not be
discarded The high Eocene-Oligocene speciation and extinction
rates should have rendered a profound replacement in ruminant
faunas This result is consistent with the high turnover previously
reported in Eurasian faunas (the so-called ldquoGrand Coupurerdquo
Janis 2008 Springer et al 2012) which has been associated with
cooler and more arid conditions in early Oligocene terrestrial
habitats (Mosbrugger et al 2005 Zachos et al 2008) However
understanding the impact of the Oligocene new environmental
context in mammalian communities demands further exploration
A comprehensive characterization of dietary shifts in Oligocene
ruminant lineages will be very insightful in this regard (Blondel
2001) Interestingly the Oligocene extinction peak is clearly
reflected by the trees as a prolonged period of low branching
rate (Fig 2A) We suggest that this lineage depletion marked the
shape of the living ruminants tree to a great extent restricting
the number of lineages that it recovers from the Eocene and
Oligocene (Fig 2) This provides an empirical proof of the
footprint that prolonged and high extinction rates leave in living
species phylogenies (Harvey et al 1994b Morlon et al 2011)
A major net-diversification pulse is robustly recovered from
both the fossil record and the phylogenetic trees during the
late Oligocene and early Miocene (27ndash22 Ma Fig 2) Al-
though the two fossil-based approaches show an increase in net-
diversification rates paired with low extinction they differ in
the macroevolutionary context of such major net-diversification
peaks Alroyrsquos method depicts accelerating speciation rates as ru-
minant lineages approached the Oligocene-Miocene limit PyRate
suggests that the high speciation rates represent continuity with
regard to Eocene and Oligocene times and that extinction would
have dropped as modern groups evolved around 27 Ma (Fig 2C
and D) This moment marked the shift toward a second major
stage of ruminant evolution the dominion of the ldquoadvancedrdquomdash
mostly hornedmdashruminants the pecorans (see Fig 1 and further
discussion below) The major radiation encompassed the appear-
ance of several living and extinct groups and a rapid accumulation
of species diversity (Fig 1) Extant groups may have exhibited
early Miocene rates above those estimated for the crown group
as a whole (Fig 2D) As a result ruminant diversity was rapidly
dominated by living groups since the early Miocene until today
(Fig 1 Costeur and Legendre 2008 Maridet and Costeur 2010)
Indeed diversification rates in fossil lineages of the crown and the
living families are very similar for the rest of the analysis interval
(Figs 2 and S2) This preponderance is also congruent with the
high agreement found between fossil-derived rates and phylo-
genetic rates in the last 25 myr of the study interval Correla-
tions showed significant concordance among curves from differ-
ent fossil-based methods and tree distributions when the fossil
record of the living groups was used (Fig 3) Only the youngest
trees from Bibirsquos dataset show nonsignificant fits Overall as early
Miocene net diversification recovered after a prolonged period of
high extinction the concordance between the macroevolutionary
signal in the fossil record and our phylogenetic data significantly
increased
After the Oligocene-Miocene diversification burst specia-
tion and net diversification significantly declined However only
trees from the dataset in Cantalapiedra et al show a comparable
pattern (Fig 2) There are two potential explanations for this out-
come First the middle Miocene (17ndash12 Ma) was indeed a period
of relatively low macroevolutionary rates and the younger trees
within Bibirsquos dataset are simply too young to reflect the true trend
Second Bibirsquos trees correctly reflect the timing of speciation of
crown living lineages whereas the other sources are recovering
the speciation of stem and crown living families combinedmdash
our fossil data include stem forms If true this second scenario
2 9 4 8 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
implies that high branching rates in living species trees may not
fit the rates estimated from the fossil record where a distinction
of crown and stem forms is very problematic even in a group with
a well-known fossil record as the ruminants (Sanchez et al 2011
Bibi 2014) Thus in cases where there is a significant temporal
lag between the diversification of stem and crown lineagesmdashas it
may be the case heremdashthe selection of true crown fossil calibra-
tion points is crucial (Bibi 2013) In this regard new total-evidence
methods (ldquotip-datingrdquo Ronquist et al 2012 Grimm et al 2015)
are contributing to overcome this issue by placing fossils within
the phylogenetic trees based on morphology while using them
to estimate divergence times (Ronquist et al 2012) Future total-
evidence analyses based on molecular data and morphology of
living and fossil ruminants will clarify this disagreement
The great diversification pulse of the Oligocene-Miocene
and the following deceleration of speciation rates may contribute
a first-hand empirical proof of the impact of ecological limits on
postradiation evolutionary rates (Moen and Morlon 2014 Harmon
and Harrison 2015) According to paleontological and paleocli-
matic evidences the Paleogene-Neogene transition was a period
of profound change in terrestrial ecosystems New available adap-
tive space was probably created by important shifts in Oligocene
and early Miocene climate (Bruch et al 2007 Eronen et al 2010)
environments (Stromberg 2011) and tectonicsmdashfor example ru-
minants entered Africa for the first time (Maglio 1978) Under this
view speciation rates would have slowed down as the adaptive
space filled Importantly extinction rates remained at basal levels
showing that the Miocene slowdown in the living ruminant tree is
rendered at the end of an expansion phase of the modern forms and
not by extinction increasing above speciation (Moen and Morlon
2014) Distinguishing between these alternatives is challenging
if just living species trees are used (Rabosky and Lovette 2008)
Ecological saturation occurs at the species level and only evolu-
tionary rates estimated from species-level fossil occurrence data
should be used to address such questions precisely (Harmon and
Harrison 2015) In this regard our fossil-based analyses provide
valuable support to previous conclusions built on neontological
information and simulations (Rabosky and Lovette 2008)
Ruminant faunas underwent critical macroevolutionary pro-
cesses in the last 10 million years (Fig 2) The fossil data sug-
gest an increase of extinction from that time onwards and a later
rebound of speciation rates Estimates from the ldquothree-timersrdquo
method and PyRate fit showing neutral-to-negative net diversi-
fication that translated into a late Miocene diversity loss Phylo-
genetic rates remained steady or slightly decreased Overall we
do not recognize a direct resemblance among curves in this tem-
poral point Nevertheless it may be the case that late Miocene
depletion also contributed to the low branching rates recovered
earlier in the trees (15ndash10 Ma see Rabosky and Lovette 2008) If
the Oligocene prolonged extinction erased most of the branches
before 30 Ma the late Miocene diversity loss may also have pre-
vented part of the evolutionary signal from the middle Miocene
to be recorded in the living species trees (Harvey et al 1994a)
We rule out the possibility that this extinction pulse is an artifact
derived from poor sampling Preservation rates of the ruminant
fossil record are relatively high for the late Miocene (around 075
Fig S1) Furthermore the two methods used to analyze the fossil
data account for heterogeneous sampling in very different ways
and yet yield very similar results with tight confidence intervals
(Fig 2) Our results show a recovery in speciation during the latest
Miocene and the Pliocene from around 7 to 25 Ma Late Pliocene
speciation rebound to levels comparable to the early Miocene As
argued above this recovery probably is reflected by the trees with
nodes slightly deeper in time due to the deeper molecular esti-
mates toward the Miocene-Pliocene Very likely mainly bovids
and deer lineages led that speciation pulse including the radiation
of American deer and that of African bovid tribes (Bibi et al
2009 Cantalapiedra et al 2014c)
The Plio-Pleistocene was one of the most dramatic episodes
in ruminant evolution A critical net diversification drop recov-
ered from the fossil record couples a slowdown in the phylogenetic
rates toward the end of our analysis interval (Fig 2) Fossil-based
rates for the last 2 myrmdashonly provided by PyRate see Methodsmdash
exhibited a severe extinction event Speciation rate still remained
close to early Miocene levels during this period but extinction
significantly surpassed it (Fig 2D) The resulting replacement
process would have reshaped ruminant faunas faster than ever
The idea of a major Plio-Pleistocene climatic shift (the estab-
lishment of continental northern-hemisphere glaciations Miller
et al 2005) and human activity reshaping mammalian faunas have
been proposed for several mammalian clades (Delson 1985 Kim-
bel 1995 Lyons et al 2004 Gomez Cano et al 2013) These
suggestions are supported by our results
To our knowledge this is the first direct evidence for neg-
ative net diversificationmdashextinction above speciationmdashas being
behind the slowdowns in living species trees toward the tips often
reported in the literature (Moen and Morlon 2014) This empir-
ical case opens the possibility that indeed progressive decrease
in phylogenetic rates toward recent times may in some cases
be the result of recent and drastic climatic fluctuations triggering
extinction
Concluding remarks
Since the first studies on tree shape (Nee et al 1992 Harvey
et al 1994b) an extensive body of research has been devoted to
understand how evolutionary processes leave their signal in phy-
logenetic trees of extant taxa Most researchers have focused on
estimate evolutionary ratesmdashthat is speciation and extinctionmdash
from phylogenies of living species (Rabosky and Lovette 2008
Alfaro et al 2009 Stadler 2011a) Other studies have pursued
EVOLUTION NOVEMBER 2015 2 9 4 9
JUAN L CANTALAPIEDRA ET AL
the identification of past episodes in evolutionary trees by com-
parison with simulations (Crisp and Cook 2009) Surprisingly
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data Quental and Marshall 2010 Morlon
et al 2011 Etienne et al 2012) Simpson et al (2011) compared
phylogenetic rates with fossil-based rates but the correlation be-
tween curves was not tested statistically Here we have shown
how the combination of speciation and extinction as recovered
from the fossil record left a signal in the living species phylogeny
of ruminants through 50 myr of evolution Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved Also the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90 of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig 1) We
acknowledge that this might not be the case scenario for many
study groups
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive rep-
resentation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12) Also
calibrating phylogenies using highly tight and conservative fossil-
informed priors may not yield rate profiles that fit rates through
time from the fossil record because the major pulses in lineage
speciation may have taken place in stem lineages
Our results also provide new views on ruminant evolution
that should be contrasted in the future The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small hornless and browser forms that were
not involved in any extraordinary diversification pulse (ldquothe lull
before the stormrdquo Janis 2008) This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1 These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007) In contrast our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig 2C)
Our analyses strongly suggest that the classic ldquoMiocene ru-
minant radiationrdquo begun in Oligocene times and prolonged until
22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-
ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition
of larger body sizes (Morales et al 1993) new dietary strate-
gies (Cantalapiedra et al 2014b) and behavior (Janis 1982 1989
Brashares et al 2000) However this event and the estimated
origin of ruminant groups with horned forms (275 Ma) largely
predates the first fossil evidence of horns in ruminants (19ndash17
Ma see DeMiguel et al 2014 Fig 2C) This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al 2014) or
those horned ruminants are to be found in the Oligocene
Finally since little can be recovered from living species trees
about the first 25 myr of ruminant evolution improving the poor
Eocene and Oligocene fossil record is crucial for future paleobio-
logical studies (Blondel 2001) This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
ldquophylogenetic coveragerdquo due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al
2012 Hipsley et al 2014 McGuire et al 2014) In summary
unveiling Paleogene environmental trends and mammal commu-
nitiesrsquo dynamics will largely benefit from fossil data And basal
ruminants probably have a lot to teach us about it
ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education
DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)
LITERATURE CITEDAlfaro M E F Santini C Brock H Alamillo A Dornburg D L Rabosky
G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414
Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542
mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge
mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397
mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014
2 9 5 0 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
EVOLUTION NOVEMBER 2015 2 9 5 1
JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
JUAN L CANTALAPIEDRA ET AL
FOSSILS-BASED EVOLUTIONARY RATES
We assessed relevant evolutionary rates (speciation and extinc-
tion) from the ruminant fossil record using two methods First
we used the most recent version of Alroyrsquos ldquothree-timersrdquo-based
equations (Alroy 2014) This method uses a four-interval moving
window that has been proved to be robust toward noise produced
by high turnover andor poor sampling The method incorporates
the interval-to-interval variation of preservation rate (see Sup-
porting Information) Alroyrsquos rates were estimated after dividing
the analysis interval in 1 myr bins To test the significance of
the evolutionary rates our dataset was bootstrapped with replace-
ment 5000 times using species occurrences as sampling units
Because occurrence data are usually assigned to temporal ranges
broader than 1 myr for each bootstrap occurrences were randomly
assigned to one of the 1 myr bins falling within their temporal
ranges We did this to include all the temporal uncertainty in our
analyses For each time bin we estimated the mean rate (Finarelli
and Badgley 2010)
Additionally to the bin-based method (three-timers) we es-
timated speciation extinction and net diversification from the
fossil record using a birthndashdeath MCMC analyses in a Bayesian
framework (BDMCMC as implemented in PyRate Silvestro et al
2014ab) The BDMCMC algorithm uses fossil occurrences data
to simultaneously estimate speciation and extinction times for
each species while finding the birthndashdeath model that better fits
the fossil record (Silvestro et al 2014ab) The model also incorpo-
rates sampling and the BDMCMC algorithm explores alternative
diversification models with different number of rate shifts (Silve-
stro et al 2014b) Importantly the method is robust toward data
incompleteness and is capable to recover a wide array of rates-
shift scenarios We randomly resampled the age of fossil occur-
rences from the occurrence intervals (from uniform distributions)
10 times using the R function extractages included in the PyRate
files Each replicate was analyzed independently for 10000000
generations using Python 26 in the Computational Cluster Trueno
at the CSIC We set the extant number of species to 197 the num-
ber of species of our bigger tree and allowed the preservation
rates to change across lineages following a gamma distribution
Mean rates through time were estimated after discarding the 20
of the logged rate estimates as burn-in and combining the results
from the 10 independent runs
Both Alroyrsquos method and the BDMCMC algorithm were used
to analyze the complete fossil record of crown ruminants (9186
occurrences see Fig 1) and the fossil record of the six living
ruminant families (8558 occurrences) We followed Metais and
Vislovokowa (2007) and considered crown ruminants all families
except Hypertragulidae Lophiomerycidae and Archaeomeryci-
dae (Fig 1) Some authors have considered the Eocene forms
Archaeotragulus and Krabitherium to belong to the extant family
Tragulidae (but see Sanchez et al 2010) thus implying a 10 myr
gap in the fossil record (from around 33 to 24 Ma see Fig 1) that
would certainly yield misleading rate estimates from this time
interval Thus we exclude these two genera from the six living
families fossil occurrences subset
We used PyRate to estimate fossil-based origination times
of the crown ruminants the pecoransmdashthe ldquomodern ruminantsrdquo
which usually have horns and include five of the six living fam-
ilies (Bibi 2014)mdashand the groups with horned forms (Fig 1)
This was done by extracting the posterior samples of the ages
of origin of the fossil species of interest derived from all occur-
rences replicates after modeling the fossil sampling process and
accounting for the uncertainties around the estimated ages of first
occurrences (Silvestro et al 2015) Thus these estimates predate
the oldest fossil occurrence of each group Then we fitted normal
lognormal and gamma distributions to these dates and choose the
best fit based on the Akaike Information Criterion (Burnham and
Anderson 2002) In this way we obtain origin age estimates that
may ease the discussion on evolutionary patterns and distribution
parameters that may be used in future phylogenetic analyses as
node-age priors (Silvestro et al 2015)
Net diversification was estimated as speciation minus ex-
tinction When the term ldquonet diversificationrdquo is used we refer to
this balance The term ldquodiversificationrdquo may be sometimes used
regarding evolutionary rates in a broader sense
CORRELATION OF THE TREE-BASED AND
FOSSILS-BASED CURVES
So far comparisons between evolutionary rates from fossil oc-
currence data and living species phylogenies have mostly relied
on pure visual and descriptive inspections (Simpson et al 2011)
Here to test whether curves are in phase with one another we
used Kendallrsquos correlation tests (Hammer and Harper 2006) This
method has been extensively applied to temporal series (Hammer
and Harper 2006 Mannion et al 2010) and assesses whether
the peaks and troughs correspond between two curves That is
it will here measure the concordance in shifts in evolutionary
rates
Because we aim to explore the impact of different node-age
configurations on the fit with fossil-derived curves we estimated
Kendallrsquos correlations between each of the 1000 rate curves ob-
tained from living-species phylogenies (500 from the trees in
Cantalapiedra and 500 from Bibi) and the mean fossil-derived
speciation and net-diversification curves estimated for the crown
ruminants using Alroyrsquos method and PyRate The correlation tests
were repeated using the fossil-derived curves (speciation and net
diversification from Alroyrsquos method and the BDMCMC analysis)
obtained from the fossil record of the six surviving ruminant fam-
ilies This was done to empirically assess whether the congruence
between fossil-based and tree-based rates is independent of the
inclusion of clades without phylogenetic representation in cases
2 9 4 4 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
where the extant families hold much of the fossil record A total
of 8000 Kendallrsquos correlations were estimated
To visualize the results we plotted the density distributions of
the P-values (for significance) and Kendallrsquos taus (τ for the sense
of the correlation) To explore whether different node-age arrange-
ments influence the correlation with the fossil record we plotted
P-values and taus obtained from each correlation test against the
mean node age of the 25 older and 25 younger nodes of the tree
involved To help data interpretation we fitted loess curves with
smoothing parameters estimated by generalized cross-validation
to avoid over-fitting to the data (Kohn et al 2000)
ResultsPHYLOGENETIC RATES
The two tree distributions encompass a wide array of node-age
configurations (Fig 2A) Nevertheless both datasets show a very
similar profile The speciation curves obtained from the two tree
distributions show a first pulse related to pecoran and tragulid
basal splits and a second part corresponding with the large radi-
ation within the six living families The deepest trees place the
first pulse in the early Oligocene (32 Ma) and the beginning
of within-family radiations in the Oligocene-Miocene (24 Ma)
The trees with younger node agesmdashmainly Bibirsquos distributionmdash
place these events in the early Miocene (20 Ma) and middle
Miocene (15 Ma) respectively In both tree distributions a slow-
down follows the second big burst followed by a recoverymdashwith
a synchronic peak in both datasets around 7 Mamdashand a final
slowdown toward the present (Bibirsquos dataset shows a recovery in
the Plio-Pleistocene Fig 2A)
RATES FROM FOSSIL OCCURRENCES
Rates estimated from fossil occurrences (net diversification spe-
ciation and extinction) obtained from the ldquothree-timersrdquo method
and the BDMCMC are depicted in Fig 2B and C respectively
Patterns of net diversification are congruent between both ap-
proaches although the speciation and extinction processes differ
in some aspects
According to the ldquothree-timersrdquo method important speci-
ation pulses are recovered during the middle and late Eocene
(45 Ma Fig 2B) and the Eocene-Oligocene boundary (34 Ma)
featured high extinction and speciation The early Oligocene is
characterized by overall neutral net diversification and turnovermdash
low extinction and very slow speciationmdash(Fig 2B) At the
end of the Oligocene net-diversification rates peaked again re-
maining high across the Oligocene-Miocene boundary (around
24 Ma) Speciation decelerated afterwards From about 20 Ma
onwards several speciation and extinction peaks render a rela-
tively constant turnover A negative net-diversification peak is
recovered around 15 Ma followed by a recovery between 12 and
10 Ma The Miocene to Pliocene transition marks a peak of the
replacement rate stemming from an episode of elevated specia-
tion and extinction rates (Fig 2B) Afterwards net diversification
increased again in part due to low extinction at the beginning
of the Pliocene Due to the ldquothree-timersrdquo methodology net di-
versification cannot be recovered from the last three bins of the
analysis interval
The BDMCMC analyses reveal high and maintained specia-
tion rates of crown ruminant lineages throughout the Eocene the
Oligocene and the earliest Miocene (Fig 2D) This high specia-
tion was coupled with elevated extinction rates particularly severe
in the late Eocene and much of the Oligocene (between 47 and
26 Ma) The confidence intervals are broad until around 26 Ma
probably due to the large occurrence temporal ranges (Fig S1)
The diversification maximum at the Oligocene-Miocene bound-
ary is here a result of decelerating extinction and sustained
high speciation The end of the net-diversification pulse around
20 Ma was rendered by a slowdown in speciation rates Moderate
speciation and extinction characterized much of the Miocene Ex-
tinction and speciation recovered around 8 and 6 Ma respectively
Whereas speciation stayed constant until the present extinction
intensely peaked during the last two million years resulting in the
most severe negative net-diversification pulse of the analysis in-
terval Gamma distributions best fitted the time of origin of crown
ruminants (offset = 4263 shape = 176 rate = 046 mean =4647 95 highest posterior density (HPD) = 4285ndash5224) pec-
orans (offset = 2696 shape = 168 rate = 057 mean = 2990
95 HPD = 2704ndash3330) and groups with horned forms (offset
= 2649 shape = 202 rate = 196 mean = 2751 95 HPD =2656ndash2906 Fig 2C)
CURVE CORRELATIONS
The results of the 8000 Kendallrsquos correlations are shown in
Figure 3 When the ldquothree-timersrdquo were used to estimate fossil-
based evolutionary rates the speciation rates based on the deepest
treesmdashfrom Cantalapiedrarsquos tree distributionmdashshowed high con-
gruence with the speciation in fossil crown Ruminantia and with
speciation and net diversification in the fossil lineages of the liv-
ing groups These correlations seemed unaffected by the different
node ages of the tree set Only the rate curves obtained from
the oldest trees showed significant correlationmdashand high positive
tausmdashwith the net-diversification curve of the crown fossil ru-
minants Speciation rates estimated from Bibirsquos trees correlated
positively with speciation in the fossil lineages of the living ru-
minant families This correlation is weaker for the trees whose
deeper nodes are younger
Rates calculated from tree distribution in Cantalapiedra cor-
related positively with speciation and net diversification in the
fossil record of the six living families as estimated by the BDM-
CMC algorithm (Fig 3GndashL) Only rates in Bibirsquos deepest trees
EVOLUTION NOVEMBER 2015 2 9 4 5
JUAN L CANTALAPIEDRA ET AL
groups withhorned forms
crown pecoranscrown ruminantsfirst fossil horns
times of origin(density)
05
0
A
B
C
D
00
01
02
03
04
05
50 40 30 20 10 0
tree-
base
d sp
ecia
tion
EOCENE OLIGOCENE MIOCENE PLI PL
50 40 30 20 10 0
50 40 30 20 10 0
EOCENE OLIGOCENE MIOCENE PLI PL
BibiCantalapiedra et al
-025
000
025
050
075
lsquothre
e-tim
ersrsquo
rate
s net-diversificationnet-div living familiesspeciationextinction
-03
00
03
06
Time (Ma)
PyR
ate
rate
s
inception offirst C3 grasslands
inception offirst C4 grasslands
permanentEAIS
onset ofmodern glaciations
Bering Strait
ArabianConnection
net-diversificationnet-div living familiesspeciationextinction
Figure 2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants (A) Tree-based speciation
rates estimated from 1000 living species phylogenies from Bibi (2013) and Cantalapiedra et al (2014b) The shadowed area represents the
95 confidence intervals (B) Net diversification speciation and extinction in fossil crown ruminants estimated using the ldquothree-timersrdquo
method (Alroy 2014) (C) Estimated times of origins of crown ruminants pecorans (advanced ruminants) and groups with horned forms
according to PyRate (D) Net diversification speciation and extinction in fossil crown ruminants estimated using PyRate (Silvestro et al
2014a) In (B) and (D) net diversification in fossil lineages of the living groups is shown in light blue Shadowed areas in (B) and (D)
represent the 95 confidence interval for the net diversification The first record of horned ruminants (gray) is based on DeMiguel et al
(2014) Mayor tectonic climatic and ecological episodes (Cerling et al 1997 Zachos et al 2008 Stromberg 2011) are shown in colors
EAIS East Antarctic Ice Sheet Pli Pliocene Pl Pleistocene Ma million years ago
showed a significant positive correlation with PyRatersquos speciation
and net diversification in the fossil record of the living groups
Phylogenetic rates from this tree set correlated negatively with
speciation in fossil crown ruminants A negative correlation was
found also with the net diversification of the fossil crown rumi-
nants for the younger trees in Bibirsquos dataset
DiscussionPast evolutionary processes left a congruent signal in the fossil
record and the phylogeny of the living ruminants The concor-
dance was stronger when fossil-based rates were estimated from
paleontological data of the living groups only (Figs 2 and 3) We
2 9 4 6 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Figure 3 Congruence of tree-based and fossils-based rates from the ldquothree-timersrdquo method (AndashF) and PyRate (GndashL) Density plots of
P-values (A) P-values from Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (B) and younger nodes (C)
of each tree Density plots of ldquotausrdquo (τ) (D) ldquotausrdquo Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (E)
and younger nodes (F) of each tree Same plots for P-values and taus when phylogenetic rates were compared with PyRate results (GndashL)
In each plot continuous LOESS lines represent results for trees in Cantalapiedra et al (2014b) and dashed lines results for Bibirsquos trees
(Bibi 2013) Dark blue and light blue fits of phylogenetic rates with net diversification in fossil lineages of crown ruminants and living
groups respectively Dark green and light green fits of phylogenetic rates with speciation in fossil lineages of crown ruminants and
living groups respectively Circles and triangles in plates A D G and J represent the medians of the parameter values of correlations for
trees in Cantalapiedra et al (2014b) and Bibi (2013) respectively
found less agreement in comparisons that used the entire fossil
record of crown ruminants where correspondences among dif-
ferent phylogenetic datasets and fossil-based methodsmdashldquothree-
timersrdquo and PyRatemdashperformed disparately (Fig 3) This is not
surprising given the nature of the evolutionary processes them-
selves and the particularities and limitations of each of the meth-
ods used in this study to recover the past Despite the many com-
parisons among rate profiles conducted here (ie two different
tree distributions two fossil-based methods two different fossil
subsets) we obtained unambiguous results about their fit through
a large array of different phylogenetic trees (Fig 3)
The capacity of living ruminant phylogenies to reconstruct
the most basal events of ruminant evolution (the Eocene and
Oligocene from around 50 to 24 Ma) critically determines the
extent to which they match evolutionary rates estimated from
the fossil record Reconstructed branching events in living ru-
minant trees are scarce during this early stage of the analysis
interval yielding very low speciation rates (Fig 2A) On top
of this different interpretations of our large fossil data (ie a
discrete-bin-based approach and a birthndashdeath Bayesian algo-
rithm) portrait disparate evolutionary scenarios for this period
(especially regarding speciation rates green curves in Fig 2B and
D) The ldquothree-timersrdquo approach reconstructed overall low specia-
tion and moderate-to-negative net diversification in the 50ndash24 Ma
temporal span Only one relevant speciation event was estimated
around 40 Ma (Fig 2B) This is a more literal read of the fossil
EVOLUTION NOVEMBER 2015 2 9 4 7
JUAN L CANTALAPIEDRA ET AL
record than that offered by PyRate (see below) The interpretation
of an early evolutionary calm before the big Miocene radiation
fits better the classic paleontological view (based on fossil ranges
and raw diversity curves Janis et al 2000 Costeur and Legendre
2008 Maridet and Costeur 2010) and the phylogenetic inferences
(Fig 2A and B) The two tree distributions yielded confidence
intervals that overlap with zero in this temporal span Thus when
the ldquothree-timersrdquo method was used the correlation between tree-
based rates and fossil speciation of the crown ruminants was
strong for most of the trees in the Cantalapiedra dataset and some
of Bibirsquos trees
PyRatersquos BDMCMC algorithm estimates a different scenario
for the first 25 myr of ruminant evolution especially with respect
to speciation rates (compare green curves in Fig 2B and D)
Unsurprisingly this notably influenced the congruence with phy-
logenetic rates (Fig 3GndashL) The BDMCMC approach places the
highest speciation rates in the Eocene Oligocene and earliest
Miocene (45ndash22 Ma Fig 2D) As a result PyRate speciation and
diversification estimates for the fossil crown ruminants yielded
a poor fit with our phylogenetic rates which show their low-
est values in this temporal span (Fig 2A) This striking differ-
ence with respect to the ldquothree-timersrdquo rates could be explained
by a deficient sampling rate (especially low for the Oligocene
Fig S1) Surprisingly although the BDMCMC algorithm (after
modeling the sampling to estimate the corrected life span of each
lineage Silvestro et al 2014a) showed high speciation rates it
still estimated accelerated extinction rates between 37 and 26 Ma
(Fig 2C) In this regard both methods agree suggesting that we
are recovering a true macroevolutionary signal and that the esti-
mate of high extinction rates is probably robust toward sampling
Although Alroyrsquos method yielded negative Eocene and
Oligocene diversification rate and subsequent diversity lossmdash
also visible in the raw diversity plot (Fig 1)mdashPyRate revealed
a scenario where net diversification slowed down but remained
positive Nonetheless PyRate yielded broad confidence intervals
for this temporal span suggesting other scenarios should not be
discarded The high Eocene-Oligocene speciation and extinction
rates should have rendered a profound replacement in ruminant
faunas This result is consistent with the high turnover previously
reported in Eurasian faunas (the so-called ldquoGrand Coupurerdquo
Janis 2008 Springer et al 2012) which has been associated with
cooler and more arid conditions in early Oligocene terrestrial
habitats (Mosbrugger et al 2005 Zachos et al 2008) However
understanding the impact of the Oligocene new environmental
context in mammalian communities demands further exploration
A comprehensive characterization of dietary shifts in Oligocene
ruminant lineages will be very insightful in this regard (Blondel
2001) Interestingly the Oligocene extinction peak is clearly
reflected by the trees as a prolonged period of low branching
rate (Fig 2A) We suggest that this lineage depletion marked the
shape of the living ruminants tree to a great extent restricting
the number of lineages that it recovers from the Eocene and
Oligocene (Fig 2) This provides an empirical proof of the
footprint that prolonged and high extinction rates leave in living
species phylogenies (Harvey et al 1994b Morlon et al 2011)
A major net-diversification pulse is robustly recovered from
both the fossil record and the phylogenetic trees during the
late Oligocene and early Miocene (27ndash22 Ma Fig 2) Al-
though the two fossil-based approaches show an increase in net-
diversification rates paired with low extinction they differ in
the macroevolutionary context of such major net-diversification
peaks Alroyrsquos method depicts accelerating speciation rates as ru-
minant lineages approached the Oligocene-Miocene limit PyRate
suggests that the high speciation rates represent continuity with
regard to Eocene and Oligocene times and that extinction would
have dropped as modern groups evolved around 27 Ma (Fig 2C
and D) This moment marked the shift toward a second major
stage of ruminant evolution the dominion of the ldquoadvancedrdquomdash
mostly hornedmdashruminants the pecorans (see Fig 1 and further
discussion below) The major radiation encompassed the appear-
ance of several living and extinct groups and a rapid accumulation
of species diversity (Fig 1) Extant groups may have exhibited
early Miocene rates above those estimated for the crown group
as a whole (Fig 2D) As a result ruminant diversity was rapidly
dominated by living groups since the early Miocene until today
(Fig 1 Costeur and Legendre 2008 Maridet and Costeur 2010)
Indeed diversification rates in fossil lineages of the crown and the
living families are very similar for the rest of the analysis interval
(Figs 2 and S2) This preponderance is also congruent with the
high agreement found between fossil-derived rates and phylo-
genetic rates in the last 25 myr of the study interval Correla-
tions showed significant concordance among curves from differ-
ent fossil-based methods and tree distributions when the fossil
record of the living groups was used (Fig 3) Only the youngest
trees from Bibirsquos dataset show nonsignificant fits Overall as early
Miocene net diversification recovered after a prolonged period of
high extinction the concordance between the macroevolutionary
signal in the fossil record and our phylogenetic data significantly
increased
After the Oligocene-Miocene diversification burst specia-
tion and net diversification significantly declined However only
trees from the dataset in Cantalapiedra et al show a comparable
pattern (Fig 2) There are two potential explanations for this out-
come First the middle Miocene (17ndash12 Ma) was indeed a period
of relatively low macroevolutionary rates and the younger trees
within Bibirsquos dataset are simply too young to reflect the true trend
Second Bibirsquos trees correctly reflect the timing of speciation of
crown living lineages whereas the other sources are recovering
the speciation of stem and crown living families combinedmdash
our fossil data include stem forms If true this second scenario
2 9 4 8 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
implies that high branching rates in living species trees may not
fit the rates estimated from the fossil record where a distinction
of crown and stem forms is very problematic even in a group with
a well-known fossil record as the ruminants (Sanchez et al 2011
Bibi 2014) Thus in cases where there is a significant temporal
lag between the diversification of stem and crown lineagesmdashas it
may be the case heremdashthe selection of true crown fossil calibra-
tion points is crucial (Bibi 2013) In this regard new total-evidence
methods (ldquotip-datingrdquo Ronquist et al 2012 Grimm et al 2015)
are contributing to overcome this issue by placing fossils within
the phylogenetic trees based on morphology while using them
to estimate divergence times (Ronquist et al 2012) Future total-
evidence analyses based on molecular data and morphology of
living and fossil ruminants will clarify this disagreement
The great diversification pulse of the Oligocene-Miocene
and the following deceleration of speciation rates may contribute
a first-hand empirical proof of the impact of ecological limits on
postradiation evolutionary rates (Moen and Morlon 2014 Harmon
and Harrison 2015) According to paleontological and paleocli-
matic evidences the Paleogene-Neogene transition was a period
of profound change in terrestrial ecosystems New available adap-
tive space was probably created by important shifts in Oligocene
and early Miocene climate (Bruch et al 2007 Eronen et al 2010)
environments (Stromberg 2011) and tectonicsmdashfor example ru-
minants entered Africa for the first time (Maglio 1978) Under this
view speciation rates would have slowed down as the adaptive
space filled Importantly extinction rates remained at basal levels
showing that the Miocene slowdown in the living ruminant tree is
rendered at the end of an expansion phase of the modern forms and
not by extinction increasing above speciation (Moen and Morlon
2014) Distinguishing between these alternatives is challenging
if just living species trees are used (Rabosky and Lovette 2008)
Ecological saturation occurs at the species level and only evolu-
tionary rates estimated from species-level fossil occurrence data
should be used to address such questions precisely (Harmon and
Harrison 2015) In this regard our fossil-based analyses provide
valuable support to previous conclusions built on neontological
information and simulations (Rabosky and Lovette 2008)
Ruminant faunas underwent critical macroevolutionary pro-
cesses in the last 10 million years (Fig 2) The fossil data sug-
gest an increase of extinction from that time onwards and a later
rebound of speciation rates Estimates from the ldquothree-timersrdquo
method and PyRate fit showing neutral-to-negative net diversi-
fication that translated into a late Miocene diversity loss Phylo-
genetic rates remained steady or slightly decreased Overall we
do not recognize a direct resemblance among curves in this tem-
poral point Nevertheless it may be the case that late Miocene
depletion also contributed to the low branching rates recovered
earlier in the trees (15ndash10 Ma see Rabosky and Lovette 2008) If
the Oligocene prolonged extinction erased most of the branches
before 30 Ma the late Miocene diversity loss may also have pre-
vented part of the evolutionary signal from the middle Miocene
to be recorded in the living species trees (Harvey et al 1994a)
We rule out the possibility that this extinction pulse is an artifact
derived from poor sampling Preservation rates of the ruminant
fossil record are relatively high for the late Miocene (around 075
Fig S1) Furthermore the two methods used to analyze the fossil
data account for heterogeneous sampling in very different ways
and yet yield very similar results with tight confidence intervals
(Fig 2) Our results show a recovery in speciation during the latest
Miocene and the Pliocene from around 7 to 25 Ma Late Pliocene
speciation rebound to levels comparable to the early Miocene As
argued above this recovery probably is reflected by the trees with
nodes slightly deeper in time due to the deeper molecular esti-
mates toward the Miocene-Pliocene Very likely mainly bovids
and deer lineages led that speciation pulse including the radiation
of American deer and that of African bovid tribes (Bibi et al
2009 Cantalapiedra et al 2014c)
The Plio-Pleistocene was one of the most dramatic episodes
in ruminant evolution A critical net diversification drop recov-
ered from the fossil record couples a slowdown in the phylogenetic
rates toward the end of our analysis interval (Fig 2) Fossil-based
rates for the last 2 myrmdashonly provided by PyRate see Methodsmdash
exhibited a severe extinction event Speciation rate still remained
close to early Miocene levels during this period but extinction
significantly surpassed it (Fig 2D) The resulting replacement
process would have reshaped ruminant faunas faster than ever
The idea of a major Plio-Pleistocene climatic shift (the estab-
lishment of continental northern-hemisphere glaciations Miller
et al 2005) and human activity reshaping mammalian faunas have
been proposed for several mammalian clades (Delson 1985 Kim-
bel 1995 Lyons et al 2004 Gomez Cano et al 2013) These
suggestions are supported by our results
To our knowledge this is the first direct evidence for neg-
ative net diversificationmdashextinction above speciationmdashas being
behind the slowdowns in living species trees toward the tips often
reported in the literature (Moen and Morlon 2014) This empir-
ical case opens the possibility that indeed progressive decrease
in phylogenetic rates toward recent times may in some cases
be the result of recent and drastic climatic fluctuations triggering
extinction
Concluding remarks
Since the first studies on tree shape (Nee et al 1992 Harvey
et al 1994b) an extensive body of research has been devoted to
understand how evolutionary processes leave their signal in phy-
logenetic trees of extant taxa Most researchers have focused on
estimate evolutionary ratesmdashthat is speciation and extinctionmdash
from phylogenies of living species (Rabosky and Lovette 2008
Alfaro et al 2009 Stadler 2011a) Other studies have pursued
EVOLUTION NOVEMBER 2015 2 9 4 9
JUAN L CANTALAPIEDRA ET AL
the identification of past episodes in evolutionary trees by com-
parison with simulations (Crisp and Cook 2009) Surprisingly
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data Quental and Marshall 2010 Morlon
et al 2011 Etienne et al 2012) Simpson et al (2011) compared
phylogenetic rates with fossil-based rates but the correlation be-
tween curves was not tested statistically Here we have shown
how the combination of speciation and extinction as recovered
from the fossil record left a signal in the living species phylogeny
of ruminants through 50 myr of evolution Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved Also the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90 of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig 1) We
acknowledge that this might not be the case scenario for many
study groups
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive rep-
resentation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12) Also
calibrating phylogenies using highly tight and conservative fossil-
informed priors may not yield rate profiles that fit rates through
time from the fossil record because the major pulses in lineage
speciation may have taken place in stem lineages
Our results also provide new views on ruminant evolution
that should be contrasted in the future The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small hornless and browser forms that were
not involved in any extraordinary diversification pulse (ldquothe lull
before the stormrdquo Janis 2008) This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1 These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007) In contrast our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig 2C)
Our analyses strongly suggest that the classic ldquoMiocene ru-
minant radiationrdquo begun in Oligocene times and prolonged until
22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-
ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition
of larger body sizes (Morales et al 1993) new dietary strate-
gies (Cantalapiedra et al 2014b) and behavior (Janis 1982 1989
Brashares et al 2000) However this event and the estimated
origin of ruminant groups with horned forms (275 Ma) largely
predates the first fossil evidence of horns in ruminants (19ndash17
Ma see DeMiguel et al 2014 Fig 2C) This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al 2014) or
those horned ruminants are to be found in the Oligocene
Finally since little can be recovered from living species trees
about the first 25 myr of ruminant evolution improving the poor
Eocene and Oligocene fossil record is crucial for future paleobio-
logical studies (Blondel 2001) This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
ldquophylogenetic coveragerdquo due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al
2012 Hipsley et al 2014 McGuire et al 2014) In summary
unveiling Paleogene environmental trends and mammal commu-
nitiesrsquo dynamics will largely benefit from fossil data And basal
ruminants probably have a lot to teach us about it
ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education
DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)
LITERATURE CITEDAlfaro M E F Santini C Brock H Alamillo A Dornburg D L Rabosky
G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414
Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542
mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge
mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397
mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014
2 9 5 0 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
EVOLUTION NOVEMBER 2015 2 9 5 1
JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
where the extant families hold much of the fossil record A total
of 8000 Kendallrsquos correlations were estimated
To visualize the results we plotted the density distributions of
the P-values (for significance) and Kendallrsquos taus (τ for the sense
of the correlation) To explore whether different node-age arrange-
ments influence the correlation with the fossil record we plotted
P-values and taus obtained from each correlation test against the
mean node age of the 25 older and 25 younger nodes of the tree
involved To help data interpretation we fitted loess curves with
smoothing parameters estimated by generalized cross-validation
to avoid over-fitting to the data (Kohn et al 2000)
ResultsPHYLOGENETIC RATES
The two tree distributions encompass a wide array of node-age
configurations (Fig 2A) Nevertheless both datasets show a very
similar profile The speciation curves obtained from the two tree
distributions show a first pulse related to pecoran and tragulid
basal splits and a second part corresponding with the large radi-
ation within the six living families The deepest trees place the
first pulse in the early Oligocene (32 Ma) and the beginning
of within-family radiations in the Oligocene-Miocene (24 Ma)
The trees with younger node agesmdashmainly Bibirsquos distributionmdash
place these events in the early Miocene (20 Ma) and middle
Miocene (15 Ma) respectively In both tree distributions a slow-
down follows the second big burst followed by a recoverymdashwith
a synchronic peak in both datasets around 7 Mamdashand a final
slowdown toward the present (Bibirsquos dataset shows a recovery in
the Plio-Pleistocene Fig 2A)
RATES FROM FOSSIL OCCURRENCES
Rates estimated from fossil occurrences (net diversification spe-
ciation and extinction) obtained from the ldquothree-timersrdquo method
and the BDMCMC are depicted in Fig 2B and C respectively
Patterns of net diversification are congruent between both ap-
proaches although the speciation and extinction processes differ
in some aspects
According to the ldquothree-timersrdquo method important speci-
ation pulses are recovered during the middle and late Eocene
(45 Ma Fig 2B) and the Eocene-Oligocene boundary (34 Ma)
featured high extinction and speciation The early Oligocene is
characterized by overall neutral net diversification and turnovermdash
low extinction and very slow speciationmdash(Fig 2B) At the
end of the Oligocene net-diversification rates peaked again re-
maining high across the Oligocene-Miocene boundary (around
24 Ma) Speciation decelerated afterwards From about 20 Ma
onwards several speciation and extinction peaks render a rela-
tively constant turnover A negative net-diversification peak is
recovered around 15 Ma followed by a recovery between 12 and
10 Ma The Miocene to Pliocene transition marks a peak of the
replacement rate stemming from an episode of elevated specia-
tion and extinction rates (Fig 2B) Afterwards net diversification
increased again in part due to low extinction at the beginning
of the Pliocene Due to the ldquothree-timersrdquo methodology net di-
versification cannot be recovered from the last three bins of the
analysis interval
The BDMCMC analyses reveal high and maintained specia-
tion rates of crown ruminant lineages throughout the Eocene the
Oligocene and the earliest Miocene (Fig 2D) This high specia-
tion was coupled with elevated extinction rates particularly severe
in the late Eocene and much of the Oligocene (between 47 and
26 Ma) The confidence intervals are broad until around 26 Ma
probably due to the large occurrence temporal ranges (Fig S1)
The diversification maximum at the Oligocene-Miocene bound-
ary is here a result of decelerating extinction and sustained
high speciation The end of the net-diversification pulse around
20 Ma was rendered by a slowdown in speciation rates Moderate
speciation and extinction characterized much of the Miocene Ex-
tinction and speciation recovered around 8 and 6 Ma respectively
Whereas speciation stayed constant until the present extinction
intensely peaked during the last two million years resulting in the
most severe negative net-diversification pulse of the analysis in-
terval Gamma distributions best fitted the time of origin of crown
ruminants (offset = 4263 shape = 176 rate = 046 mean =4647 95 highest posterior density (HPD) = 4285ndash5224) pec-
orans (offset = 2696 shape = 168 rate = 057 mean = 2990
95 HPD = 2704ndash3330) and groups with horned forms (offset
= 2649 shape = 202 rate = 196 mean = 2751 95 HPD =2656ndash2906 Fig 2C)
CURVE CORRELATIONS
The results of the 8000 Kendallrsquos correlations are shown in
Figure 3 When the ldquothree-timersrdquo were used to estimate fossil-
based evolutionary rates the speciation rates based on the deepest
treesmdashfrom Cantalapiedrarsquos tree distributionmdashshowed high con-
gruence with the speciation in fossil crown Ruminantia and with
speciation and net diversification in the fossil lineages of the liv-
ing groups These correlations seemed unaffected by the different
node ages of the tree set Only the rate curves obtained from
the oldest trees showed significant correlationmdashand high positive
tausmdashwith the net-diversification curve of the crown fossil ru-
minants Speciation rates estimated from Bibirsquos trees correlated
positively with speciation in the fossil lineages of the living ru-
minant families This correlation is weaker for the trees whose
deeper nodes are younger
Rates calculated from tree distribution in Cantalapiedra cor-
related positively with speciation and net diversification in the
fossil record of the six living families as estimated by the BDM-
CMC algorithm (Fig 3GndashL) Only rates in Bibirsquos deepest trees
EVOLUTION NOVEMBER 2015 2 9 4 5
JUAN L CANTALAPIEDRA ET AL
groups withhorned forms
crown pecoranscrown ruminantsfirst fossil horns
times of origin(density)
05
0
A
B
C
D
00
01
02
03
04
05
50 40 30 20 10 0
tree-
base
d sp
ecia
tion
EOCENE OLIGOCENE MIOCENE PLI PL
50 40 30 20 10 0
50 40 30 20 10 0
EOCENE OLIGOCENE MIOCENE PLI PL
BibiCantalapiedra et al
-025
000
025
050
075
lsquothre
e-tim
ersrsquo
rate
s net-diversificationnet-div living familiesspeciationextinction
-03
00
03
06
Time (Ma)
PyR
ate
rate
s
inception offirst C3 grasslands
inception offirst C4 grasslands
permanentEAIS
onset ofmodern glaciations
Bering Strait
ArabianConnection
net-diversificationnet-div living familiesspeciationextinction
Figure 2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants (A) Tree-based speciation
rates estimated from 1000 living species phylogenies from Bibi (2013) and Cantalapiedra et al (2014b) The shadowed area represents the
95 confidence intervals (B) Net diversification speciation and extinction in fossil crown ruminants estimated using the ldquothree-timersrdquo
method (Alroy 2014) (C) Estimated times of origins of crown ruminants pecorans (advanced ruminants) and groups with horned forms
according to PyRate (D) Net diversification speciation and extinction in fossil crown ruminants estimated using PyRate (Silvestro et al
2014a) In (B) and (D) net diversification in fossil lineages of the living groups is shown in light blue Shadowed areas in (B) and (D)
represent the 95 confidence interval for the net diversification The first record of horned ruminants (gray) is based on DeMiguel et al
(2014) Mayor tectonic climatic and ecological episodes (Cerling et al 1997 Zachos et al 2008 Stromberg 2011) are shown in colors
EAIS East Antarctic Ice Sheet Pli Pliocene Pl Pleistocene Ma million years ago
showed a significant positive correlation with PyRatersquos speciation
and net diversification in the fossil record of the living groups
Phylogenetic rates from this tree set correlated negatively with
speciation in fossil crown ruminants A negative correlation was
found also with the net diversification of the fossil crown rumi-
nants for the younger trees in Bibirsquos dataset
DiscussionPast evolutionary processes left a congruent signal in the fossil
record and the phylogeny of the living ruminants The concor-
dance was stronger when fossil-based rates were estimated from
paleontological data of the living groups only (Figs 2 and 3) We
2 9 4 6 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Figure 3 Congruence of tree-based and fossils-based rates from the ldquothree-timersrdquo method (AndashF) and PyRate (GndashL) Density plots of
P-values (A) P-values from Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (B) and younger nodes (C)
of each tree Density plots of ldquotausrdquo (τ) (D) ldquotausrdquo Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (E)
and younger nodes (F) of each tree Same plots for P-values and taus when phylogenetic rates were compared with PyRate results (GndashL)
In each plot continuous LOESS lines represent results for trees in Cantalapiedra et al (2014b) and dashed lines results for Bibirsquos trees
(Bibi 2013) Dark blue and light blue fits of phylogenetic rates with net diversification in fossil lineages of crown ruminants and living
groups respectively Dark green and light green fits of phylogenetic rates with speciation in fossil lineages of crown ruminants and
living groups respectively Circles and triangles in plates A D G and J represent the medians of the parameter values of correlations for
trees in Cantalapiedra et al (2014b) and Bibi (2013) respectively
found less agreement in comparisons that used the entire fossil
record of crown ruminants where correspondences among dif-
ferent phylogenetic datasets and fossil-based methodsmdashldquothree-
timersrdquo and PyRatemdashperformed disparately (Fig 3) This is not
surprising given the nature of the evolutionary processes them-
selves and the particularities and limitations of each of the meth-
ods used in this study to recover the past Despite the many com-
parisons among rate profiles conducted here (ie two different
tree distributions two fossil-based methods two different fossil
subsets) we obtained unambiguous results about their fit through
a large array of different phylogenetic trees (Fig 3)
The capacity of living ruminant phylogenies to reconstruct
the most basal events of ruminant evolution (the Eocene and
Oligocene from around 50 to 24 Ma) critically determines the
extent to which they match evolutionary rates estimated from
the fossil record Reconstructed branching events in living ru-
minant trees are scarce during this early stage of the analysis
interval yielding very low speciation rates (Fig 2A) On top
of this different interpretations of our large fossil data (ie a
discrete-bin-based approach and a birthndashdeath Bayesian algo-
rithm) portrait disparate evolutionary scenarios for this period
(especially regarding speciation rates green curves in Fig 2B and
D) The ldquothree-timersrdquo approach reconstructed overall low specia-
tion and moderate-to-negative net diversification in the 50ndash24 Ma
temporal span Only one relevant speciation event was estimated
around 40 Ma (Fig 2B) This is a more literal read of the fossil
EVOLUTION NOVEMBER 2015 2 9 4 7
JUAN L CANTALAPIEDRA ET AL
record than that offered by PyRate (see below) The interpretation
of an early evolutionary calm before the big Miocene radiation
fits better the classic paleontological view (based on fossil ranges
and raw diversity curves Janis et al 2000 Costeur and Legendre
2008 Maridet and Costeur 2010) and the phylogenetic inferences
(Fig 2A and B) The two tree distributions yielded confidence
intervals that overlap with zero in this temporal span Thus when
the ldquothree-timersrdquo method was used the correlation between tree-
based rates and fossil speciation of the crown ruminants was
strong for most of the trees in the Cantalapiedra dataset and some
of Bibirsquos trees
PyRatersquos BDMCMC algorithm estimates a different scenario
for the first 25 myr of ruminant evolution especially with respect
to speciation rates (compare green curves in Fig 2B and D)
Unsurprisingly this notably influenced the congruence with phy-
logenetic rates (Fig 3GndashL) The BDMCMC approach places the
highest speciation rates in the Eocene Oligocene and earliest
Miocene (45ndash22 Ma Fig 2D) As a result PyRate speciation and
diversification estimates for the fossil crown ruminants yielded
a poor fit with our phylogenetic rates which show their low-
est values in this temporal span (Fig 2A) This striking differ-
ence with respect to the ldquothree-timersrdquo rates could be explained
by a deficient sampling rate (especially low for the Oligocene
Fig S1) Surprisingly although the BDMCMC algorithm (after
modeling the sampling to estimate the corrected life span of each
lineage Silvestro et al 2014a) showed high speciation rates it
still estimated accelerated extinction rates between 37 and 26 Ma
(Fig 2C) In this regard both methods agree suggesting that we
are recovering a true macroevolutionary signal and that the esti-
mate of high extinction rates is probably robust toward sampling
Although Alroyrsquos method yielded negative Eocene and
Oligocene diversification rate and subsequent diversity lossmdash
also visible in the raw diversity plot (Fig 1)mdashPyRate revealed
a scenario where net diversification slowed down but remained
positive Nonetheless PyRate yielded broad confidence intervals
for this temporal span suggesting other scenarios should not be
discarded The high Eocene-Oligocene speciation and extinction
rates should have rendered a profound replacement in ruminant
faunas This result is consistent with the high turnover previously
reported in Eurasian faunas (the so-called ldquoGrand Coupurerdquo
Janis 2008 Springer et al 2012) which has been associated with
cooler and more arid conditions in early Oligocene terrestrial
habitats (Mosbrugger et al 2005 Zachos et al 2008) However
understanding the impact of the Oligocene new environmental
context in mammalian communities demands further exploration
A comprehensive characterization of dietary shifts in Oligocene
ruminant lineages will be very insightful in this regard (Blondel
2001) Interestingly the Oligocene extinction peak is clearly
reflected by the trees as a prolonged period of low branching
rate (Fig 2A) We suggest that this lineage depletion marked the
shape of the living ruminants tree to a great extent restricting
the number of lineages that it recovers from the Eocene and
Oligocene (Fig 2) This provides an empirical proof of the
footprint that prolonged and high extinction rates leave in living
species phylogenies (Harvey et al 1994b Morlon et al 2011)
A major net-diversification pulse is robustly recovered from
both the fossil record and the phylogenetic trees during the
late Oligocene and early Miocene (27ndash22 Ma Fig 2) Al-
though the two fossil-based approaches show an increase in net-
diversification rates paired with low extinction they differ in
the macroevolutionary context of such major net-diversification
peaks Alroyrsquos method depicts accelerating speciation rates as ru-
minant lineages approached the Oligocene-Miocene limit PyRate
suggests that the high speciation rates represent continuity with
regard to Eocene and Oligocene times and that extinction would
have dropped as modern groups evolved around 27 Ma (Fig 2C
and D) This moment marked the shift toward a second major
stage of ruminant evolution the dominion of the ldquoadvancedrdquomdash
mostly hornedmdashruminants the pecorans (see Fig 1 and further
discussion below) The major radiation encompassed the appear-
ance of several living and extinct groups and a rapid accumulation
of species diversity (Fig 1) Extant groups may have exhibited
early Miocene rates above those estimated for the crown group
as a whole (Fig 2D) As a result ruminant diversity was rapidly
dominated by living groups since the early Miocene until today
(Fig 1 Costeur and Legendre 2008 Maridet and Costeur 2010)
Indeed diversification rates in fossil lineages of the crown and the
living families are very similar for the rest of the analysis interval
(Figs 2 and S2) This preponderance is also congruent with the
high agreement found between fossil-derived rates and phylo-
genetic rates in the last 25 myr of the study interval Correla-
tions showed significant concordance among curves from differ-
ent fossil-based methods and tree distributions when the fossil
record of the living groups was used (Fig 3) Only the youngest
trees from Bibirsquos dataset show nonsignificant fits Overall as early
Miocene net diversification recovered after a prolonged period of
high extinction the concordance between the macroevolutionary
signal in the fossil record and our phylogenetic data significantly
increased
After the Oligocene-Miocene diversification burst specia-
tion and net diversification significantly declined However only
trees from the dataset in Cantalapiedra et al show a comparable
pattern (Fig 2) There are two potential explanations for this out-
come First the middle Miocene (17ndash12 Ma) was indeed a period
of relatively low macroevolutionary rates and the younger trees
within Bibirsquos dataset are simply too young to reflect the true trend
Second Bibirsquos trees correctly reflect the timing of speciation of
crown living lineages whereas the other sources are recovering
the speciation of stem and crown living families combinedmdash
our fossil data include stem forms If true this second scenario
2 9 4 8 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
implies that high branching rates in living species trees may not
fit the rates estimated from the fossil record where a distinction
of crown and stem forms is very problematic even in a group with
a well-known fossil record as the ruminants (Sanchez et al 2011
Bibi 2014) Thus in cases where there is a significant temporal
lag between the diversification of stem and crown lineagesmdashas it
may be the case heremdashthe selection of true crown fossil calibra-
tion points is crucial (Bibi 2013) In this regard new total-evidence
methods (ldquotip-datingrdquo Ronquist et al 2012 Grimm et al 2015)
are contributing to overcome this issue by placing fossils within
the phylogenetic trees based on morphology while using them
to estimate divergence times (Ronquist et al 2012) Future total-
evidence analyses based on molecular data and morphology of
living and fossil ruminants will clarify this disagreement
The great diversification pulse of the Oligocene-Miocene
and the following deceleration of speciation rates may contribute
a first-hand empirical proof of the impact of ecological limits on
postradiation evolutionary rates (Moen and Morlon 2014 Harmon
and Harrison 2015) According to paleontological and paleocli-
matic evidences the Paleogene-Neogene transition was a period
of profound change in terrestrial ecosystems New available adap-
tive space was probably created by important shifts in Oligocene
and early Miocene climate (Bruch et al 2007 Eronen et al 2010)
environments (Stromberg 2011) and tectonicsmdashfor example ru-
minants entered Africa for the first time (Maglio 1978) Under this
view speciation rates would have slowed down as the adaptive
space filled Importantly extinction rates remained at basal levels
showing that the Miocene slowdown in the living ruminant tree is
rendered at the end of an expansion phase of the modern forms and
not by extinction increasing above speciation (Moen and Morlon
2014) Distinguishing between these alternatives is challenging
if just living species trees are used (Rabosky and Lovette 2008)
Ecological saturation occurs at the species level and only evolu-
tionary rates estimated from species-level fossil occurrence data
should be used to address such questions precisely (Harmon and
Harrison 2015) In this regard our fossil-based analyses provide
valuable support to previous conclusions built on neontological
information and simulations (Rabosky and Lovette 2008)
Ruminant faunas underwent critical macroevolutionary pro-
cesses in the last 10 million years (Fig 2) The fossil data sug-
gest an increase of extinction from that time onwards and a later
rebound of speciation rates Estimates from the ldquothree-timersrdquo
method and PyRate fit showing neutral-to-negative net diversi-
fication that translated into a late Miocene diversity loss Phylo-
genetic rates remained steady or slightly decreased Overall we
do not recognize a direct resemblance among curves in this tem-
poral point Nevertheless it may be the case that late Miocene
depletion also contributed to the low branching rates recovered
earlier in the trees (15ndash10 Ma see Rabosky and Lovette 2008) If
the Oligocene prolonged extinction erased most of the branches
before 30 Ma the late Miocene diversity loss may also have pre-
vented part of the evolutionary signal from the middle Miocene
to be recorded in the living species trees (Harvey et al 1994a)
We rule out the possibility that this extinction pulse is an artifact
derived from poor sampling Preservation rates of the ruminant
fossil record are relatively high for the late Miocene (around 075
Fig S1) Furthermore the two methods used to analyze the fossil
data account for heterogeneous sampling in very different ways
and yet yield very similar results with tight confidence intervals
(Fig 2) Our results show a recovery in speciation during the latest
Miocene and the Pliocene from around 7 to 25 Ma Late Pliocene
speciation rebound to levels comparable to the early Miocene As
argued above this recovery probably is reflected by the trees with
nodes slightly deeper in time due to the deeper molecular esti-
mates toward the Miocene-Pliocene Very likely mainly bovids
and deer lineages led that speciation pulse including the radiation
of American deer and that of African bovid tribes (Bibi et al
2009 Cantalapiedra et al 2014c)
The Plio-Pleistocene was one of the most dramatic episodes
in ruminant evolution A critical net diversification drop recov-
ered from the fossil record couples a slowdown in the phylogenetic
rates toward the end of our analysis interval (Fig 2) Fossil-based
rates for the last 2 myrmdashonly provided by PyRate see Methodsmdash
exhibited a severe extinction event Speciation rate still remained
close to early Miocene levels during this period but extinction
significantly surpassed it (Fig 2D) The resulting replacement
process would have reshaped ruminant faunas faster than ever
The idea of a major Plio-Pleistocene climatic shift (the estab-
lishment of continental northern-hemisphere glaciations Miller
et al 2005) and human activity reshaping mammalian faunas have
been proposed for several mammalian clades (Delson 1985 Kim-
bel 1995 Lyons et al 2004 Gomez Cano et al 2013) These
suggestions are supported by our results
To our knowledge this is the first direct evidence for neg-
ative net diversificationmdashextinction above speciationmdashas being
behind the slowdowns in living species trees toward the tips often
reported in the literature (Moen and Morlon 2014) This empir-
ical case opens the possibility that indeed progressive decrease
in phylogenetic rates toward recent times may in some cases
be the result of recent and drastic climatic fluctuations triggering
extinction
Concluding remarks
Since the first studies on tree shape (Nee et al 1992 Harvey
et al 1994b) an extensive body of research has been devoted to
understand how evolutionary processes leave their signal in phy-
logenetic trees of extant taxa Most researchers have focused on
estimate evolutionary ratesmdashthat is speciation and extinctionmdash
from phylogenies of living species (Rabosky and Lovette 2008
Alfaro et al 2009 Stadler 2011a) Other studies have pursued
EVOLUTION NOVEMBER 2015 2 9 4 9
JUAN L CANTALAPIEDRA ET AL
the identification of past episodes in evolutionary trees by com-
parison with simulations (Crisp and Cook 2009) Surprisingly
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data Quental and Marshall 2010 Morlon
et al 2011 Etienne et al 2012) Simpson et al (2011) compared
phylogenetic rates with fossil-based rates but the correlation be-
tween curves was not tested statistically Here we have shown
how the combination of speciation and extinction as recovered
from the fossil record left a signal in the living species phylogeny
of ruminants through 50 myr of evolution Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved Also the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90 of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig 1) We
acknowledge that this might not be the case scenario for many
study groups
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive rep-
resentation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12) Also
calibrating phylogenies using highly tight and conservative fossil-
informed priors may not yield rate profiles that fit rates through
time from the fossil record because the major pulses in lineage
speciation may have taken place in stem lineages
Our results also provide new views on ruminant evolution
that should be contrasted in the future The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small hornless and browser forms that were
not involved in any extraordinary diversification pulse (ldquothe lull
before the stormrdquo Janis 2008) This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1 These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007) In contrast our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig 2C)
Our analyses strongly suggest that the classic ldquoMiocene ru-
minant radiationrdquo begun in Oligocene times and prolonged until
22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-
ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition
of larger body sizes (Morales et al 1993) new dietary strate-
gies (Cantalapiedra et al 2014b) and behavior (Janis 1982 1989
Brashares et al 2000) However this event and the estimated
origin of ruminant groups with horned forms (275 Ma) largely
predates the first fossil evidence of horns in ruminants (19ndash17
Ma see DeMiguel et al 2014 Fig 2C) This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al 2014) or
those horned ruminants are to be found in the Oligocene
Finally since little can be recovered from living species trees
about the first 25 myr of ruminant evolution improving the poor
Eocene and Oligocene fossil record is crucial for future paleobio-
logical studies (Blondel 2001) This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
ldquophylogenetic coveragerdquo due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al
2012 Hipsley et al 2014 McGuire et al 2014) In summary
unveiling Paleogene environmental trends and mammal commu-
nitiesrsquo dynamics will largely benefit from fossil data And basal
ruminants probably have a lot to teach us about it
ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education
DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)
LITERATURE CITEDAlfaro M E F Santini C Brock H Alamillo A Dornburg D L Rabosky
G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414
Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542
mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge
mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397
mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014
2 9 5 0 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
EVOLUTION NOVEMBER 2015 2 9 5 1
JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
JUAN L CANTALAPIEDRA ET AL
groups withhorned forms
crown pecoranscrown ruminantsfirst fossil horns
times of origin(density)
05
0
A
B
C
D
00
01
02
03
04
05
50 40 30 20 10 0
tree-
base
d sp
ecia
tion
EOCENE OLIGOCENE MIOCENE PLI PL
50 40 30 20 10 0
50 40 30 20 10 0
EOCENE OLIGOCENE MIOCENE PLI PL
BibiCantalapiedra et al
-025
000
025
050
075
lsquothre
e-tim
ersrsquo
rate
s net-diversificationnet-div living familiesspeciationextinction
-03
00
03
06
Time (Ma)
PyR
ate
rate
s
inception offirst C3 grasslands
inception offirst C4 grasslands
permanentEAIS
onset ofmodern glaciations
Bering Strait
ArabianConnection
net-diversificationnet-div living familiesspeciationextinction
Figure 2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants (A) Tree-based speciation
rates estimated from 1000 living species phylogenies from Bibi (2013) and Cantalapiedra et al (2014b) The shadowed area represents the
95 confidence intervals (B) Net diversification speciation and extinction in fossil crown ruminants estimated using the ldquothree-timersrdquo
method (Alroy 2014) (C) Estimated times of origins of crown ruminants pecorans (advanced ruminants) and groups with horned forms
according to PyRate (D) Net diversification speciation and extinction in fossil crown ruminants estimated using PyRate (Silvestro et al
2014a) In (B) and (D) net diversification in fossil lineages of the living groups is shown in light blue Shadowed areas in (B) and (D)
represent the 95 confidence interval for the net diversification The first record of horned ruminants (gray) is based on DeMiguel et al
(2014) Mayor tectonic climatic and ecological episodes (Cerling et al 1997 Zachos et al 2008 Stromberg 2011) are shown in colors
EAIS East Antarctic Ice Sheet Pli Pliocene Pl Pleistocene Ma million years ago
showed a significant positive correlation with PyRatersquos speciation
and net diversification in the fossil record of the living groups
Phylogenetic rates from this tree set correlated negatively with
speciation in fossil crown ruminants A negative correlation was
found also with the net diversification of the fossil crown rumi-
nants for the younger trees in Bibirsquos dataset
DiscussionPast evolutionary processes left a congruent signal in the fossil
record and the phylogeny of the living ruminants The concor-
dance was stronger when fossil-based rates were estimated from
paleontological data of the living groups only (Figs 2 and 3) We
2 9 4 6 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Figure 3 Congruence of tree-based and fossils-based rates from the ldquothree-timersrdquo method (AndashF) and PyRate (GndashL) Density plots of
P-values (A) P-values from Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (B) and younger nodes (C)
of each tree Density plots of ldquotausrdquo (τ) (D) ldquotausrdquo Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (E)
and younger nodes (F) of each tree Same plots for P-values and taus when phylogenetic rates were compared with PyRate results (GndashL)
In each plot continuous LOESS lines represent results for trees in Cantalapiedra et al (2014b) and dashed lines results for Bibirsquos trees
(Bibi 2013) Dark blue and light blue fits of phylogenetic rates with net diversification in fossil lineages of crown ruminants and living
groups respectively Dark green and light green fits of phylogenetic rates with speciation in fossil lineages of crown ruminants and
living groups respectively Circles and triangles in plates A D G and J represent the medians of the parameter values of correlations for
trees in Cantalapiedra et al (2014b) and Bibi (2013) respectively
found less agreement in comparisons that used the entire fossil
record of crown ruminants where correspondences among dif-
ferent phylogenetic datasets and fossil-based methodsmdashldquothree-
timersrdquo and PyRatemdashperformed disparately (Fig 3) This is not
surprising given the nature of the evolutionary processes them-
selves and the particularities and limitations of each of the meth-
ods used in this study to recover the past Despite the many com-
parisons among rate profiles conducted here (ie two different
tree distributions two fossil-based methods two different fossil
subsets) we obtained unambiguous results about their fit through
a large array of different phylogenetic trees (Fig 3)
The capacity of living ruminant phylogenies to reconstruct
the most basal events of ruminant evolution (the Eocene and
Oligocene from around 50 to 24 Ma) critically determines the
extent to which they match evolutionary rates estimated from
the fossil record Reconstructed branching events in living ru-
minant trees are scarce during this early stage of the analysis
interval yielding very low speciation rates (Fig 2A) On top
of this different interpretations of our large fossil data (ie a
discrete-bin-based approach and a birthndashdeath Bayesian algo-
rithm) portrait disparate evolutionary scenarios for this period
(especially regarding speciation rates green curves in Fig 2B and
D) The ldquothree-timersrdquo approach reconstructed overall low specia-
tion and moderate-to-negative net diversification in the 50ndash24 Ma
temporal span Only one relevant speciation event was estimated
around 40 Ma (Fig 2B) This is a more literal read of the fossil
EVOLUTION NOVEMBER 2015 2 9 4 7
JUAN L CANTALAPIEDRA ET AL
record than that offered by PyRate (see below) The interpretation
of an early evolutionary calm before the big Miocene radiation
fits better the classic paleontological view (based on fossil ranges
and raw diversity curves Janis et al 2000 Costeur and Legendre
2008 Maridet and Costeur 2010) and the phylogenetic inferences
(Fig 2A and B) The two tree distributions yielded confidence
intervals that overlap with zero in this temporal span Thus when
the ldquothree-timersrdquo method was used the correlation between tree-
based rates and fossil speciation of the crown ruminants was
strong for most of the trees in the Cantalapiedra dataset and some
of Bibirsquos trees
PyRatersquos BDMCMC algorithm estimates a different scenario
for the first 25 myr of ruminant evolution especially with respect
to speciation rates (compare green curves in Fig 2B and D)
Unsurprisingly this notably influenced the congruence with phy-
logenetic rates (Fig 3GndashL) The BDMCMC approach places the
highest speciation rates in the Eocene Oligocene and earliest
Miocene (45ndash22 Ma Fig 2D) As a result PyRate speciation and
diversification estimates for the fossil crown ruminants yielded
a poor fit with our phylogenetic rates which show their low-
est values in this temporal span (Fig 2A) This striking differ-
ence with respect to the ldquothree-timersrdquo rates could be explained
by a deficient sampling rate (especially low for the Oligocene
Fig S1) Surprisingly although the BDMCMC algorithm (after
modeling the sampling to estimate the corrected life span of each
lineage Silvestro et al 2014a) showed high speciation rates it
still estimated accelerated extinction rates between 37 and 26 Ma
(Fig 2C) In this regard both methods agree suggesting that we
are recovering a true macroevolutionary signal and that the esti-
mate of high extinction rates is probably robust toward sampling
Although Alroyrsquos method yielded negative Eocene and
Oligocene diversification rate and subsequent diversity lossmdash
also visible in the raw diversity plot (Fig 1)mdashPyRate revealed
a scenario where net diversification slowed down but remained
positive Nonetheless PyRate yielded broad confidence intervals
for this temporal span suggesting other scenarios should not be
discarded The high Eocene-Oligocene speciation and extinction
rates should have rendered a profound replacement in ruminant
faunas This result is consistent with the high turnover previously
reported in Eurasian faunas (the so-called ldquoGrand Coupurerdquo
Janis 2008 Springer et al 2012) which has been associated with
cooler and more arid conditions in early Oligocene terrestrial
habitats (Mosbrugger et al 2005 Zachos et al 2008) However
understanding the impact of the Oligocene new environmental
context in mammalian communities demands further exploration
A comprehensive characterization of dietary shifts in Oligocene
ruminant lineages will be very insightful in this regard (Blondel
2001) Interestingly the Oligocene extinction peak is clearly
reflected by the trees as a prolonged period of low branching
rate (Fig 2A) We suggest that this lineage depletion marked the
shape of the living ruminants tree to a great extent restricting
the number of lineages that it recovers from the Eocene and
Oligocene (Fig 2) This provides an empirical proof of the
footprint that prolonged and high extinction rates leave in living
species phylogenies (Harvey et al 1994b Morlon et al 2011)
A major net-diversification pulse is robustly recovered from
both the fossil record and the phylogenetic trees during the
late Oligocene and early Miocene (27ndash22 Ma Fig 2) Al-
though the two fossil-based approaches show an increase in net-
diversification rates paired with low extinction they differ in
the macroevolutionary context of such major net-diversification
peaks Alroyrsquos method depicts accelerating speciation rates as ru-
minant lineages approached the Oligocene-Miocene limit PyRate
suggests that the high speciation rates represent continuity with
regard to Eocene and Oligocene times and that extinction would
have dropped as modern groups evolved around 27 Ma (Fig 2C
and D) This moment marked the shift toward a second major
stage of ruminant evolution the dominion of the ldquoadvancedrdquomdash
mostly hornedmdashruminants the pecorans (see Fig 1 and further
discussion below) The major radiation encompassed the appear-
ance of several living and extinct groups and a rapid accumulation
of species diversity (Fig 1) Extant groups may have exhibited
early Miocene rates above those estimated for the crown group
as a whole (Fig 2D) As a result ruminant diversity was rapidly
dominated by living groups since the early Miocene until today
(Fig 1 Costeur and Legendre 2008 Maridet and Costeur 2010)
Indeed diversification rates in fossil lineages of the crown and the
living families are very similar for the rest of the analysis interval
(Figs 2 and S2) This preponderance is also congruent with the
high agreement found between fossil-derived rates and phylo-
genetic rates in the last 25 myr of the study interval Correla-
tions showed significant concordance among curves from differ-
ent fossil-based methods and tree distributions when the fossil
record of the living groups was used (Fig 3) Only the youngest
trees from Bibirsquos dataset show nonsignificant fits Overall as early
Miocene net diversification recovered after a prolonged period of
high extinction the concordance between the macroevolutionary
signal in the fossil record and our phylogenetic data significantly
increased
After the Oligocene-Miocene diversification burst specia-
tion and net diversification significantly declined However only
trees from the dataset in Cantalapiedra et al show a comparable
pattern (Fig 2) There are two potential explanations for this out-
come First the middle Miocene (17ndash12 Ma) was indeed a period
of relatively low macroevolutionary rates and the younger trees
within Bibirsquos dataset are simply too young to reflect the true trend
Second Bibirsquos trees correctly reflect the timing of speciation of
crown living lineages whereas the other sources are recovering
the speciation of stem and crown living families combinedmdash
our fossil data include stem forms If true this second scenario
2 9 4 8 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
implies that high branching rates in living species trees may not
fit the rates estimated from the fossil record where a distinction
of crown and stem forms is very problematic even in a group with
a well-known fossil record as the ruminants (Sanchez et al 2011
Bibi 2014) Thus in cases where there is a significant temporal
lag between the diversification of stem and crown lineagesmdashas it
may be the case heremdashthe selection of true crown fossil calibra-
tion points is crucial (Bibi 2013) In this regard new total-evidence
methods (ldquotip-datingrdquo Ronquist et al 2012 Grimm et al 2015)
are contributing to overcome this issue by placing fossils within
the phylogenetic trees based on morphology while using them
to estimate divergence times (Ronquist et al 2012) Future total-
evidence analyses based on molecular data and morphology of
living and fossil ruminants will clarify this disagreement
The great diversification pulse of the Oligocene-Miocene
and the following deceleration of speciation rates may contribute
a first-hand empirical proof of the impact of ecological limits on
postradiation evolutionary rates (Moen and Morlon 2014 Harmon
and Harrison 2015) According to paleontological and paleocli-
matic evidences the Paleogene-Neogene transition was a period
of profound change in terrestrial ecosystems New available adap-
tive space was probably created by important shifts in Oligocene
and early Miocene climate (Bruch et al 2007 Eronen et al 2010)
environments (Stromberg 2011) and tectonicsmdashfor example ru-
minants entered Africa for the first time (Maglio 1978) Under this
view speciation rates would have slowed down as the adaptive
space filled Importantly extinction rates remained at basal levels
showing that the Miocene slowdown in the living ruminant tree is
rendered at the end of an expansion phase of the modern forms and
not by extinction increasing above speciation (Moen and Morlon
2014) Distinguishing between these alternatives is challenging
if just living species trees are used (Rabosky and Lovette 2008)
Ecological saturation occurs at the species level and only evolu-
tionary rates estimated from species-level fossil occurrence data
should be used to address such questions precisely (Harmon and
Harrison 2015) In this regard our fossil-based analyses provide
valuable support to previous conclusions built on neontological
information and simulations (Rabosky and Lovette 2008)
Ruminant faunas underwent critical macroevolutionary pro-
cesses in the last 10 million years (Fig 2) The fossil data sug-
gest an increase of extinction from that time onwards and a later
rebound of speciation rates Estimates from the ldquothree-timersrdquo
method and PyRate fit showing neutral-to-negative net diversi-
fication that translated into a late Miocene diversity loss Phylo-
genetic rates remained steady or slightly decreased Overall we
do not recognize a direct resemblance among curves in this tem-
poral point Nevertheless it may be the case that late Miocene
depletion also contributed to the low branching rates recovered
earlier in the trees (15ndash10 Ma see Rabosky and Lovette 2008) If
the Oligocene prolonged extinction erased most of the branches
before 30 Ma the late Miocene diversity loss may also have pre-
vented part of the evolutionary signal from the middle Miocene
to be recorded in the living species trees (Harvey et al 1994a)
We rule out the possibility that this extinction pulse is an artifact
derived from poor sampling Preservation rates of the ruminant
fossil record are relatively high for the late Miocene (around 075
Fig S1) Furthermore the two methods used to analyze the fossil
data account for heterogeneous sampling in very different ways
and yet yield very similar results with tight confidence intervals
(Fig 2) Our results show a recovery in speciation during the latest
Miocene and the Pliocene from around 7 to 25 Ma Late Pliocene
speciation rebound to levels comparable to the early Miocene As
argued above this recovery probably is reflected by the trees with
nodes slightly deeper in time due to the deeper molecular esti-
mates toward the Miocene-Pliocene Very likely mainly bovids
and deer lineages led that speciation pulse including the radiation
of American deer and that of African bovid tribes (Bibi et al
2009 Cantalapiedra et al 2014c)
The Plio-Pleistocene was one of the most dramatic episodes
in ruminant evolution A critical net diversification drop recov-
ered from the fossil record couples a slowdown in the phylogenetic
rates toward the end of our analysis interval (Fig 2) Fossil-based
rates for the last 2 myrmdashonly provided by PyRate see Methodsmdash
exhibited a severe extinction event Speciation rate still remained
close to early Miocene levels during this period but extinction
significantly surpassed it (Fig 2D) The resulting replacement
process would have reshaped ruminant faunas faster than ever
The idea of a major Plio-Pleistocene climatic shift (the estab-
lishment of continental northern-hemisphere glaciations Miller
et al 2005) and human activity reshaping mammalian faunas have
been proposed for several mammalian clades (Delson 1985 Kim-
bel 1995 Lyons et al 2004 Gomez Cano et al 2013) These
suggestions are supported by our results
To our knowledge this is the first direct evidence for neg-
ative net diversificationmdashextinction above speciationmdashas being
behind the slowdowns in living species trees toward the tips often
reported in the literature (Moen and Morlon 2014) This empir-
ical case opens the possibility that indeed progressive decrease
in phylogenetic rates toward recent times may in some cases
be the result of recent and drastic climatic fluctuations triggering
extinction
Concluding remarks
Since the first studies on tree shape (Nee et al 1992 Harvey
et al 1994b) an extensive body of research has been devoted to
understand how evolutionary processes leave their signal in phy-
logenetic trees of extant taxa Most researchers have focused on
estimate evolutionary ratesmdashthat is speciation and extinctionmdash
from phylogenies of living species (Rabosky and Lovette 2008
Alfaro et al 2009 Stadler 2011a) Other studies have pursued
EVOLUTION NOVEMBER 2015 2 9 4 9
JUAN L CANTALAPIEDRA ET AL
the identification of past episodes in evolutionary trees by com-
parison with simulations (Crisp and Cook 2009) Surprisingly
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data Quental and Marshall 2010 Morlon
et al 2011 Etienne et al 2012) Simpson et al (2011) compared
phylogenetic rates with fossil-based rates but the correlation be-
tween curves was not tested statistically Here we have shown
how the combination of speciation and extinction as recovered
from the fossil record left a signal in the living species phylogeny
of ruminants through 50 myr of evolution Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved Also the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90 of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig 1) We
acknowledge that this might not be the case scenario for many
study groups
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive rep-
resentation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12) Also
calibrating phylogenies using highly tight and conservative fossil-
informed priors may not yield rate profiles that fit rates through
time from the fossil record because the major pulses in lineage
speciation may have taken place in stem lineages
Our results also provide new views on ruminant evolution
that should be contrasted in the future The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small hornless and browser forms that were
not involved in any extraordinary diversification pulse (ldquothe lull
before the stormrdquo Janis 2008) This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1 These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007) In contrast our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig 2C)
Our analyses strongly suggest that the classic ldquoMiocene ru-
minant radiationrdquo begun in Oligocene times and prolonged until
22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-
ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition
of larger body sizes (Morales et al 1993) new dietary strate-
gies (Cantalapiedra et al 2014b) and behavior (Janis 1982 1989
Brashares et al 2000) However this event and the estimated
origin of ruminant groups with horned forms (275 Ma) largely
predates the first fossil evidence of horns in ruminants (19ndash17
Ma see DeMiguel et al 2014 Fig 2C) This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al 2014) or
those horned ruminants are to be found in the Oligocene
Finally since little can be recovered from living species trees
about the first 25 myr of ruminant evolution improving the poor
Eocene and Oligocene fossil record is crucial for future paleobio-
logical studies (Blondel 2001) This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
ldquophylogenetic coveragerdquo due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al
2012 Hipsley et al 2014 McGuire et al 2014) In summary
unveiling Paleogene environmental trends and mammal commu-
nitiesrsquo dynamics will largely benefit from fossil data And basal
ruminants probably have a lot to teach us about it
ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education
DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)
LITERATURE CITEDAlfaro M E F Santini C Brock H Alamillo A Dornburg D L Rabosky
G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414
Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542
mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge
mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397
mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014
2 9 5 0 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
EVOLUTION NOVEMBER 2015 2 9 5 1
JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Figure 3 Congruence of tree-based and fossils-based rates from the ldquothree-timersrdquo method (AndashF) and PyRate (GndashL) Density plots of
P-values (A) P-values from Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (B) and younger nodes (C)
of each tree Density plots of ldquotausrdquo (τ) (D) ldquotausrdquo Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (E)
and younger nodes (F) of each tree Same plots for P-values and taus when phylogenetic rates were compared with PyRate results (GndashL)
In each plot continuous LOESS lines represent results for trees in Cantalapiedra et al (2014b) and dashed lines results for Bibirsquos trees
(Bibi 2013) Dark blue and light blue fits of phylogenetic rates with net diversification in fossil lineages of crown ruminants and living
groups respectively Dark green and light green fits of phylogenetic rates with speciation in fossil lineages of crown ruminants and
living groups respectively Circles and triangles in plates A D G and J represent the medians of the parameter values of correlations for
trees in Cantalapiedra et al (2014b) and Bibi (2013) respectively
found less agreement in comparisons that used the entire fossil
record of crown ruminants where correspondences among dif-
ferent phylogenetic datasets and fossil-based methodsmdashldquothree-
timersrdquo and PyRatemdashperformed disparately (Fig 3) This is not
surprising given the nature of the evolutionary processes them-
selves and the particularities and limitations of each of the meth-
ods used in this study to recover the past Despite the many com-
parisons among rate profiles conducted here (ie two different
tree distributions two fossil-based methods two different fossil
subsets) we obtained unambiguous results about their fit through
a large array of different phylogenetic trees (Fig 3)
The capacity of living ruminant phylogenies to reconstruct
the most basal events of ruminant evolution (the Eocene and
Oligocene from around 50 to 24 Ma) critically determines the
extent to which they match evolutionary rates estimated from
the fossil record Reconstructed branching events in living ru-
minant trees are scarce during this early stage of the analysis
interval yielding very low speciation rates (Fig 2A) On top
of this different interpretations of our large fossil data (ie a
discrete-bin-based approach and a birthndashdeath Bayesian algo-
rithm) portrait disparate evolutionary scenarios for this period
(especially regarding speciation rates green curves in Fig 2B and
D) The ldquothree-timersrdquo approach reconstructed overall low specia-
tion and moderate-to-negative net diversification in the 50ndash24 Ma
temporal span Only one relevant speciation event was estimated
around 40 Ma (Fig 2B) This is a more literal read of the fossil
EVOLUTION NOVEMBER 2015 2 9 4 7
JUAN L CANTALAPIEDRA ET AL
record than that offered by PyRate (see below) The interpretation
of an early evolutionary calm before the big Miocene radiation
fits better the classic paleontological view (based on fossil ranges
and raw diversity curves Janis et al 2000 Costeur and Legendre
2008 Maridet and Costeur 2010) and the phylogenetic inferences
(Fig 2A and B) The two tree distributions yielded confidence
intervals that overlap with zero in this temporal span Thus when
the ldquothree-timersrdquo method was used the correlation between tree-
based rates and fossil speciation of the crown ruminants was
strong for most of the trees in the Cantalapiedra dataset and some
of Bibirsquos trees
PyRatersquos BDMCMC algorithm estimates a different scenario
for the first 25 myr of ruminant evolution especially with respect
to speciation rates (compare green curves in Fig 2B and D)
Unsurprisingly this notably influenced the congruence with phy-
logenetic rates (Fig 3GndashL) The BDMCMC approach places the
highest speciation rates in the Eocene Oligocene and earliest
Miocene (45ndash22 Ma Fig 2D) As a result PyRate speciation and
diversification estimates for the fossil crown ruminants yielded
a poor fit with our phylogenetic rates which show their low-
est values in this temporal span (Fig 2A) This striking differ-
ence with respect to the ldquothree-timersrdquo rates could be explained
by a deficient sampling rate (especially low for the Oligocene
Fig S1) Surprisingly although the BDMCMC algorithm (after
modeling the sampling to estimate the corrected life span of each
lineage Silvestro et al 2014a) showed high speciation rates it
still estimated accelerated extinction rates between 37 and 26 Ma
(Fig 2C) In this regard both methods agree suggesting that we
are recovering a true macroevolutionary signal and that the esti-
mate of high extinction rates is probably robust toward sampling
Although Alroyrsquos method yielded negative Eocene and
Oligocene diversification rate and subsequent diversity lossmdash
also visible in the raw diversity plot (Fig 1)mdashPyRate revealed
a scenario where net diversification slowed down but remained
positive Nonetheless PyRate yielded broad confidence intervals
for this temporal span suggesting other scenarios should not be
discarded The high Eocene-Oligocene speciation and extinction
rates should have rendered a profound replacement in ruminant
faunas This result is consistent with the high turnover previously
reported in Eurasian faunas (the so-called ldquoGrand Coupurerdquo
Janis 2008 Springer et al 2012) which has been associated with
cooler and more arid conditions in early Oligocene terrestrial
habitats (Mosbrugger et al 2005 Zachos et al 2008) However
understanding the impact of the Oligocene new environmental
context in mammalian communities demands further exploration
A comprehensive characterization of dietary shifts in Oligocene
ruminant lineages will be very insightful in this regard (Blondel
2001) Interestingly the Oligocene extinction peak is clearly
reflected by the trees as a prolonged period of low branching
rate (Fig 2A) We suggest that this lineage depletion marked the
shape of the living ruminants tree to a great extent restricting
the number of lineages that it recovers from the Eocene and
Oligocene (Fig 2) This provides an empirical proof of the
footprint that prolonged and high extinction rates leave in living
species phylogenies (Harvey et al 1994b Morlon et al 2011)
A major net-diversification pulse is robustly recovered from
both the fossil record and the phylogenetic trees during the
late Oligocene and early Miocene (27ndash22 Ma Fig 2) Al-
though the two fossil-based approaches show an increase in net-
diversification rates paired with low extinction they differ in
the macroevolutionary context of such major net-diversification
peaks Alroyrsquos method depicts accelerating speciation rates as ru-
minant lineages approached the Oligocene-Miocene limit PyRate
suggests that the high speciation rates represent continuity with
regard to Eocene and Oligocene times and that extinction would
have dropped as modern groups evolved around 27 Ma (Fig 2C
and D) This moment marked the shift toward a second major
stage of ruminant evolution the dominion of the ldquoadvancedrdquomdash
mostly hornedmdashruminants the pecorans (see Fig 1 and further
discussion below) The major radiation encompassed the appear-
ance of several living and extinct groups and a rapid accumulation
of species diversity (Fig 1) Extant groups may have exhibited
early Miocene rates above those estimated for the crown group
as a whole (Fig 2D) As a result ruminant diversity was rapidly
dominated by living groups since the early Miocene until today
(Fig 1 Costeur and Legendre 2008 Maridet and Costeur 2010)
Indeed diversification rates in fossil lineages of the crown and the
living families are very similar for the rest of the analysis interval
(Figs 2 and S2) This preponderance is also congruent with the
high agreement found between fossil-derived rates and phylo-
genetic rates in the last 25 myr of the study interval Correla-
tions showed significant concordance among curves from differ-
ent fossil-based methods and tree distributions when the fossil
record of the living groups was used (Fig 3) Only the youngest
trees from Bibirsquos dataset show nonsignificant fits Overall as early
Miocene net diversification recovered after a prolonged period of
high extinction the concordance between the macroevolutionary
signal in the fossil record and our phylogenetic data significantly
increased
After the Oligocene-Miocene diversification burst specia-
tion and net diversification significantly declined However only
trees from the dataset in Cantalapiedra et al show a comparable
pattern (Fig 2) There are two potential explanations for this out-
come First the middle Miocene (17ndash12 Ma) was indeed a period
of relatively low macroevolutionary rates and the younger trees
within Bibirsquos dataset are simply too young to reflect the true trend
Second Bibirsquos trees correctly reflect the timing of speciation of
crown living lineages whereas the other sources are recovering
the speciation of stem and crown living families combinedmdash
our fossil data include stem forms If true this second scenario
2 9 4 8 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
implies that high branching rates in living species trees may not
fit the rates estimated from the fossil record where a distinction
of crown and stem forms is very problematic even in a group with
a well-known fossil record as the ruminants (Sanchez et al 2011
Bibi 2014) Thus in cases where there is a significant temporal
lag between the diversification of stem and crown lineagesmdashas it
may be the case heremdashthe selection of true crown fossil calibra-
tion points is crucial (Bibi 2013) In this regard new total-evidence
methods (ldquotip-datingrdquo Ronquist et al 2012 Grimm et al 2015)
are contributing to overcome this issue by placing fossils within
the phylogenetic trees based on morphology while using them
to estimate divergence times (Ronquist et al 2012) Future total-
evidence analyses based on molecular data and morphology of
living and fossil ruminants will clarify this disagreement
The great diversification pulse of the Oligocene-Miocene
and the following deceleration of speciation rates may contribute
a first-hand empirical proof of the impact of ecological limits on
postradiation evolutionary rates (Moen and Morlon 2014 Harmon
and Harrison 2015) According to paleontological and paleocli-
matic evidences the Paleogene-Neogene transition was a period
of profound change in terrestrial ecosystems New available adap-
tive space was probably created by important shifts in Oligocene
and early Miocene climate (Bruch et al 2007 Eronen et al 2010)
environments (Stromberg 2011) and tectonicsmdashfor example ru-
minants entered Africa for the first time (Maglio 1978) Under this
view speciation rates would have slowed down as the adaptive
space filled Importantly extinction rates remained at basal levels
showing that the Miocene slowdown in the living ruminant tree is
rendered at the end of an expansion phase of the modern forms and
not by extinction increasing above speciation (Moen and Morlon
2014) Distinguishing between these alternatives is challenging
if just living species trees are used (Rabosky and Lovette 2008)
Ecological saturation occurs at the species level and only evolu-
tionary rates estimated from species-level fossil occurrence data
should be used to address such questions precisely (Harmon and
Harrison 2015) In this regard our fossil-based analyses provide
valuable support to previous conclusions built on neontological
information and simulations (Rabosky and Lovette 2008)
Ruminant faunas underwent critical macroevolutionary pro-
cesses in the last 10 million years (Fig 2) The fossil data sug-
gest an increase of extinction from that time onwards and a later
rebound of speciation rates Estimates from the ldquothree-timersrdquo
method and PyRate fit showing neutral-to-negative net diversi-
fication that translated into a late Miocene diversity loss Phylo-
genetic rates remained steady or slightly decreased Overall we
do not recognize a direct resemblance among curves in this tem-
poral point Nevertheless it may be the case that late Miocene
depletion also contributed to the low branching rates recovered
earlier in the trees (15ndash10 Ma see Rabosky and Lovette 2008) If
the Oligocene prolonged extinction erased most of the branches
before 30 Ma the late Miocene diversity loss may also have pre-
vented part of the evolutionary signal from the middle Miocene
to be recorded in the living species trees (Harvey et al 1994a)
We rule out the possibility that this extinction pulse is an artifact
derived from poor sampling Preservation rates of the ruminant
fossil record are relatively high for the late Miocene (around 075
Fig S1) Furthermore the two methods used to analyze the fossil
data account for heterogeneous sampling in very different ways
and yet yield very similar results with tight confidence intervals
(Fig 2) Our results show a recovery in speciation during the latest
Miocene and the Pliocene from around 7 to 25 Ma Late Pliocene
speciation rebound to levels comparable to the early Miocene As
argued above this recovery probably is reflected by the trees with
nodes slightly deeper in time due to the deeper molecular esti-
mates toward the Miocene-Pliocene Very likely mainly bovids
and deer lineages led that speciation pulse including the radiation
of American deer and that of African bovid tribes (Bibi et al
2009 Cantalapiedra et al 2014c)
The Plio-Pleistocene was one of the most dramatic episodes
in ruminant evolution A critical net diversification drop recov-
ered from the fossil record couples a slowdown in the phylogenetic
rates toward the end of our analysis interval (Fig 2) Fossil-based
rates for the last 2 myrmdashonly provided by PyRate see Methodsmdash
exhibited a severe extinction event Speciation rate still remained
close to early Miocene levels during this period but extinction
significantly surpassed it (Fig 2D) The resulting replacement
process would have reshaped ruminant faunas faster than ever
The idea of a major Plio-Pleistocene climatic shift (the estab-
lishment of continental northern-hemisphere glaciations Miller
et al 2005) and human activity reshaping mammalian faunas have
been proposed for several mammalian clades (Delson 1985 Kim-
bel 1995 Lyons et al 2004 Gomez Cano et al 2013) These
suggestions are supported by our results
To our knowledge this is the first direct evidence for neg-
ative net diversificationmdashextinction above speciationmdashas being
behind the slowdowns in living species trees toward the tips often
reported in the literature (Moen and Morlon 2014) This empir-
ical case opens the possibility that indeed progressive decrease
in phylogenetic rates toward recent times may in some cases
be the result of recent and drastic climatic fluctuations triggering
extinction
Concluding remarks
Since the first studies on tree shape (Nee et al 1992 Harvey
et al 1994b) an extensive body of research has been devoted to
understand how evolutionary processes leave their signal in phy-
logenetic trees of extant taxa Most researchers have focused on
estimate evolutionary ratesmdashthat is speciation and extinctionmdash
from phylogenies of living species (Rabosky and Lovette 2008
Alfaro et al 2009 Stadler 2011a) Other studies have pursued
EVOLUTION NOVEMBER 2015 2 9 4 9
JUAN L CANTALAPIEDRA ET AL
the identification of past episodes in evolutionary trees by com-
parison with simulations (Crisp and Cook 2009) Surprisingly
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data Quental and Marshall 2010 Morlon
et al 2011 Etienne et al 2012) Simpson et al (2011) compared
phylogenetic rates with fossil-based rates but the correlation be-
tween curves was not tested statistically Here we have shown
how the combination of speciation and extinction as recovered
from the fossil record left a signal in the living species phylogeny
of ruminants through 50 myr of evolution Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved Also the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90 of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig 1) We
acknowledge that this might not be the case scenario for many
study groups
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive rep-
resentation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12) Also
calibrating phylogenies using highly tight and conservative fossil-
informed priors may not yield rate profiles that fit rates through
time from the fossil record because the major pulses in lineage
speciation may have taken place in stem lineages
Our results also provide new views on ruminant evolution
that should be contrasted in the future The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small hornless and browser forms that were
not involved in any extraordinary diversification pulse (ldquothe lull
before the stormrdquo Janis 2008) This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1 These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007) In contrast our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig 2C)
Our analyses strongly suggest that the classic ldquoMiocene ru-
minant radiationrdquo begun in Oligocene times and prolonged until
22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-
ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition
of larger body sizes (Morales et al 1993) new dietary strate-
gies (Cantalapiedra et al 2014b) and behavior (Janis 1982 1989
Brashares et al 2000) However this event and the estimated
origin of ruminant groups with horned forms (275 Ma) largely
predates the first fossil evidence of horns in ruminants (19ndash17
Ma see DeMiguel et al 2014 Fig 2C) This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al 2014) or
those horned ruminants are to be found in the Oligocene
Finally since little can be recovered from living species trees
about the first 25 myr of ruminant evolution improving the poor
Eocene and Oligocene fossil record is crucial for future paleobio-
logical studies (Blondel 2001) This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
ldquophylogenetic coveragerdquo due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al
2012 Hipsley et al 2014 McGuire et al 2014) In summary
unveiling Paleogene environmental trends and mammal commu-
nitiesrsquo dynamics will largely benefit from fossil data And basal
ruminants probably have a lot to teach us about it
ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education
DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)
LITERATURE CITEDAlfaro M E F Santini C Brock H Alamillo A Dornburg D L Rabosky
G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414
Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542
mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge
mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397
mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014
2 9 5 0 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
EVOLUTION NOVEMBER 2015 2 9 5 1
JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
JUAN L CANTALAPIEDRA ET AL
record than that offered by PyRate (see below) The interpretation
of an early evolutionary calm before the big Miocene radiation
fits better the classic paleontological view (based on fossil ranges
and raw diversity curves Janis et al 2000 Costeur and Legendre
2008 Maridet and Costeur 2010) and the phylogenetic inferences
(Fig 2A and B) The two tree distributions yielded confidence
intervals that overlap with zero in this temporal span Thus when
the ldquothree-timersrdquo method was used the correlation between tree-
based rates and fossil speciation of the crown ruminants was
strong for most of the trees in the Cantalapiedra dataset and some
of Bibirsquos trees
PyRatersquos BDMCMC algorithm estimates a different scenario
for the first 25 myr of ruminant evolution especially with respect
to speciation rates (compare green curves in Fig 2B and D)
Unsurprisingly this notably influenced the congruence with phy-
logenetic rates (Fig 3GndashL) The BDMCMC approach places the
highest speciation rates in the Eocene Oligocene and earliest
Miocene (45ndash22 Ma Fig 2D) As a result PyRate speciation and
diversification estimates for the fossil crown ruminants yielded
a poor fit with our phylogenetic rates which show their low-
est values in this temporal span (Fig 2A) This striking differ-
ence with respect to the ldquothree-timersrdquo rates could be explained
by a deficient sampling rate (especially low for the Oligocene
Fig S1) Surprisingly although the BDMCMC algorithm (after
modeling the sampling to estimate the corrected life span of each
lineage Silvestro et al 2014a) showed high speciation rates it
still estimated accelerated extinction rates between 37 and 26 Ma
(Fig 2C) In this regard both methods agree suggesting that we
are recovering a true macroevolutionary signal and that the esti-
mate of high extinction rates is probably robust toward sampling
Although Alroyrsquos method yielded negative Eocene and
Oligocene diversification rate and subsequent diversity lossmdash
also visible in the raw diversity plot (Fig 1)mdashPyRate revealed
a scenario where net diversification slowed down but remained
positive Nonetheless PyRate yielded broad confidence intervals
for this temporal span suggesting other scenarios should not be
discarded The high Eocene-Oligocene speciation and extinction
rates should have rendered a profound replacement in ruminant
faunas This result is consistent with the high turnover previously
reported in Eurasian faunas (the so-called ldquoGrand Coupurerdquo
Janis 2008 Springer et al 2012) which has been associated with
cooler and more arid conditions in early Oligocene terrestrial
habitats (Mosbrugger et al 2005 Zachos et al 2008) However
understanding the impact of the Oligocene new environmental
context in mammalian communities demands further exploration
A comprehensive characterization of dietary shifts in Oligocene
ruminant lineages will be very insightful in this regard (Blondel
2001) Interestingly the Oligocene extinction peak is clearly
reflected by the trees as a prolonged period of low branching
rate (Fig 2A) We suggest that this lineage depletion marked the
shape of the living ruminants tree to a great extent restricting
the number of lineages that it recovers from the Eocene and
Oligocene (Fig 2) This provides an empirical proof of the
footprint that prolonged and high extinction rates leave in living
species phylogenies (Harvey et al 1994b Morlon et al 2011)
A major net-diversification pulse is robustly recovered from
both the fossil record and the phylogenetic trees during the
late Oligocene and early Miocene (27ndash22 Ma Fig 2) Al-
though the two fossil-based approaches show an increase in net-
diversification rates paired with low extinction they differ in
the macroevolutionary context of such major net-diversification
peaks Alroyrsquos method depicts accelerating speciation rates as ru-
minant lineages approached the Oligocene-Miocene limit PyRate
suggests that the high speciation rates represent continuity with
regard to Eocene and Oligocene times and that extinction would
have dropped as modern groups evolved around 27 Ma (Fig 2C
and D) This moment marked the shift toward a second major
stage of ruminant evolution the dominion of the ldquoadvancedrdquomdash
mostly hornedmdashruminants the pecorans (see Fig 1 and further
discussion below) The major radiation encompassed the appear-
ance of several living and extinct groups and a rapid accumulation
of species diversity (Fig 1) Extant groups may have exhibited
early Miocene rates above those estimated for the crown group
as a whole (Fig 2D) As a result ruminant diversity was rapidly
dominated by living groups since the early Miocene until today
(Fig 1 Costeur and Legendre 2008 Maridet and Costeur 2010)
Indeed diversification rates in fossil lineages of the crown and the
living families are very similar for the rest of the analysis interval
(Figs 2 and S2) This preponderance is also congruent with the
high agreement found between fossil-derived rates and phylo-
genetic rates in the last 25 myr of the study interval Correla-
tions showed significant concordance among curves from differ-
ent fossil-based methods and tree distributions when the fossil
record of the living groups was used (Fig 3) Only the youngest
trees from Bibirsquos dataset show nonsignificant fits Overall as early
Miocene net diversification recovered after a prolonged period of
high extinction the concordance between the macroevolutionary
signal in the fossil record and our phylogenetic data significantly
increased
After the Oligocene-Miocene diversification burst specia-
tion and net diversification significantly declined However only
trees from the dataset in Cantalapiedra et al show a comparable
pattern (Fig 2) There are two potential explanations for this out-
come First the middle Miocene (17ndash12 Ma) was indeed a period
of relatively low macroevolutionary rates and the younger trees
within Bibirsquos dataset are simply too young to reflect the true trend
Second Bibirsquos trees correctly reflect the timing of speciation of
crown living lineages whereas the other sources are recovering
the speciation of stem and crown living families combinedmdash
our fossil data include stem forms If true this second scenario
2 9 4 8 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
implies that high branching rates in living species trees may not
fit the rates estimated from the fossil record where a distinction
of crown and stem forms is very problematic even in a group with
a well-known fossil record as the ruminants (Sanchez et al 2011
Bibi 2014) Thus in cases where there is a significant temporal
lag between the diversification of stem and crown lineagesmdashas it
may be the case heremdashthe selection of true crown fossil calibra-
tion points is crucial (Bibi 2013) In this regard new total-evidence
methods (ldquotip-datingrdquo Ronquist et al 2012 Grimm et al 2015)
are contributing to overcome this issue by placing fossils within
the phylogenetic trees based on morphology while using them
to estimate divergence times (Ronquist et al 2012) Future total-
evidence analyses based on molecular data and morphology of
living and fossil ruminants will clarify this disagreement
The great diversification pulse of the Oligocene-Miocene
and the following deceleration of speciation rates may contribute
a first-hand empirical proof of the impact of ecological limits on
postradiation evolutionary rates (Moen and Morlon 2014 Harmon
and Harrison 2015) According to paleontological and paleocli-
matic evidences the Paleogene-Neogene transition was a period
of profound change in terrestrial ecosystems New available adap-
tive space was probably created by important shifts in Oligocene
and early Miocene climate (Bruch et al 2007 Eronen et al 2010)
environments (Stromberg 2011) and tectonicsmdashfor example ru-
minants entered Africa for the first time (Maglio 1978) Under this
view speciation rates would have slowed down as the adaptive
space filled Importantly extinction rates remained at basal levels
showing that the Miocene slowdown in the living ruminant tree is
rendered at the end of an expansion phase of the modern forms and
not by extinction increasing above speciation (Moen and Morlon
2014) Distinguishing between these alternatives is challenging
if just living species trees are used (Rabosky and Lovette 2008)
Ecological saturation occurs at the species level and only evolu-
tionary rates estimated from species-level fossil occurrence data
should be used to address such questions precisely (Harmon and
Harrison 2015) In this regard our fossil-based analyses provide
valuable support to previous conclusions built on neontological
information and simulations (Rabosky and Lovette 2008)
Ruminant faunas underwent critical macroevolutionary pro-
cesses in the last 10 million years (Fig 2) The fossil data sug-
gest an increase of extinction from that time onwards and a later
rebound of speciation rates Estimates from the ldquothree-timersrdquo
method and PyRate fit showing neutral-to-negative net diversi-
fication that translated into a late Miocene diversity loss Phylo-
genetic rates remained steady or slightly decreased Overall we
do not recognize a direct resemblance among curves in this tem-
poral point Nevertheless it may be the case that late Miocene
depletion also contributed to the low branching rates recovered
earlier in the trees (15ndash10 Ma see Rabosky and Lovette 2008) If
the Oligocene prolonged extinction erased most of the branches
before 30 Ma the late Miocene diversity loss may also have pre-
vented part of the evolutionary signal from the middle Miocene
to be recorded in the living species trees (Harvey et al 1994a)
We rule out the possibility that this extinction pulse is an artifact
derived from poor sampling Preservation rates of the ruminant
fossil record are relatively high for the late Miocene (around 075
Fig S1) Furthermore the two methods used to analyze the fossil
data account for heterogeneous sampling in very different ways
and yet yield very similar results with tight confidence intervals
(Fig 2) Our results show a recovery in speciation during the latest
Miocene and the Pliocene from around 7 to 25 Ma Late Pliocene
speciation rebound to levels comparable to the early Miocene As
argued above this recovery probably is reflected by the trees with
nodes slightly deeper in time due to the deeper molecular esti-
mates toward the Miocene-Pliocene Very likely mainly bovids
and deer lineages led that speciation pulse including the radiation
of American deer and that of African bovid tribes (Bibi et al
2009 Cantalapiedra et al 2014c)
The Plio-Pleistocene was one of the most dramatic episodes
in ruminant evolution A critical net diversification drop recov-
ered from the fossil record couples a slowdown in the phylogenetic
rates toward the end of our analysis interval (Fig 2) Fossil-based
rates for the last 2 myrmdashonly provided by PyRate see Methodsmdash
exhibited a severe extinction event Speciation rate still remained
close to early Miocene levels during this period but extinction
significantly surpassed it (Fig 2D) The resulting replacement
process would have reshaped ruminant faunas faster than ever
The idea of a major Plio-Pleistocene climatic shift (the estab-
lishment of continental northern-hemisphere glaciations Miller
et al 2005) and human activity reshaping mammalian faunas have
been proposed for several mammalian clades (Delson 1985 Kim-
bel 1995 Lyons et al 2004 Gomez Cano et al 2013) These
suggestions are supported by our results
To our knowledge this is the first direct evidence for neg-
ative net diversificationmdashextinction above speciationmdashas being
behind the slowdowns in living species trees toward the tips often
reported in the literature (Moen and Morlon 2014) This empir-
ical case opens the possibility that indeed progressive decrease
in phylogenetic rates toward recent times may in some cases
be the result of recent and drastic climatic fluctuations triggering
extinction
Concluding remarks
Since the first studies on tree shape (Nee et al 1992 Harvey
et al 1994b) an extensive body of research has been devoted to
understand how evolutionary processes leave their signal in phy-
logenetic trees of extant taxa Most researchers have focused on
estimate evolutionary ratesmdashthat is speciation and extinctionmdash
from phylogenies of living species (Rabosky and Lovette 2008
Alfaro et al 2009 Stadler 2011a) Other studies have pursued
EVOLUTION NOVEMBER 2015 2 9 4 9
JUAN L CANTALAPIEDRA ET AL
the identification of past episodes in evolutionary trees by com-
parison with simulations (Crisp and Cook 2009) Surprisingly
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data Quental and Marshall 2010 Morlon
et al 2011 Etienne et al 2012) Simpson et al (2011) compared
phylogenetic rates with fossil-based rates but the correlation be-
tween curves was not tested statistically Here we have shown
how the combination of speciation and extinction as recovered
from the fossil record left a signal in the living species phylogeny
of ruminants through 50 myr of evolution Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved Also the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90 of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig 1) We
acknowledge that this might not be the case scenario for many
study groups
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive rep-
resentation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12) Also
calibrating phylogenies using highly tight and conservative fossil-
informed priors may not yield rate profiles that fit rates through
time from the fossil record because the major pulses in lineage
speciation may have taken place in stem lineages
Our results also provide new views on ruminant evolution
that should be contrasted in the future The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small hornless and browser forms that were
not involved in any extraordinary diversification pulse (ldquothe lull
before the stormrdquo Janis 2008) This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1 These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007) In contrast our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig 2C)
Our analyses strongly suggest that the classic ldquoMiocene ru-
minant radiationrdquo begun in Oligocene times and prolonged until
22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-
ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition
of larger body sizes (Morales et al 1993) new dietary strate-
gies (Cantalapiedra et al 2014b) and behavior (Janis 1982 1989
Brashares et al 2000) However this event and the estimated
origin of ruminant groups with horned forms (275 Ma) largely
predates the first fossil evidence of horns in ruminants (19ndash17
Ma see DeMiguel et al 2014 Fig 2C) This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al 2014) or
those horned ruminants are to be found in the Oligocene
Finally since little can be recovered from living species trees
about the first 25 myr of ruminant evolution improving the poor
Eocene and Oligocene fossil record is crucial for future paleobio-
logical studies (Blondel 2001) This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
ldquophylogenetic coveragerdquo due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al
2012 Hipsley et al 2014 McGuire et al 2014) In summary
unveiling Paleogene environmental trends and mammal commu-
nitiesrsquo dynamics will largely benefit from fossil data And basal
ruminants probably have a lot to teach us about it
ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education
DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)
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G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414
Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542
mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge
mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397
mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014
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CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
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JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
implies that high branching rates in living species trees may not
fit the rates estimated from the fossil record where a distinction
of crown and stem forms is very problematic even in a group with
a well-known fossil record as the ruminants (Sanchez et al 2011
Bibi 2014) Thus in cases where there is a significant temporal
lag between the diversification of stem and crown lineagesmdashas it
may be the case heremdashthe selection of true crown fossil calibra-
tion points is crucial (Bibi 2013) In this regard new total-evidence
methods (ldquotip-datingrdquo Ronquist et al 2012 Grimm et al 2015)
are contributing to overcome this issue by placing fossils within
the phylogenetic trees based on morphology while using them
to estimate divergence times (Ronquist et al 2012) Future total-
evidence analyses based on molecular data and morphology of
living and fossil ruminants will clarify this disagreement
The great diversification pulse of the Oligocene-Miocene
and the following deceleration of speciation rates may contribute
a first-hand empirical proof of the impact of ecological limits on
postradiation evolutionary rates (Moen and Morlon 2014 Harmon
and Harrison 2015) According to paleontological and paleocli-
matic evidences the Paleogene-Neogene transition was a period
of profound change in terrestrial ecosystems New available adap-
tive space was probably created by important shifts in Oligocene
and early Miocene climate (Bruch et al 2007 Eronen et al 2010)
environments (Stromberg 2011) and tectonicsmdashfor example ru-
minants entered Africa for the first time (Maglio 1978) Under this
view speciation rates would have slowed down as the adaptive
space filled Importantly extinction rates remained at basal levels
showing that the Miocene slowdown in the living ruminant tree is
rendered at the end of an expansion phase of the modern forms and
not by extinction increasing above speciation (Moen and Morlon
2014) Distinguishing between these alternatives is challenging
if just living species trees are used (Rabosky and Lovette 2008)
Ecological saturation occurs at the species level and only evolu-
tionary rates estimated from species-level fossil occurrence data
should be used to address such questions precisely (Harmon and
Harrison 2015) In this regard our fossil-based analyses provide
valuable support to previous conclusions built on neontological
information and simulations (Rabosky and Lovette 2008)
Ruminant faunas underwent critical macroevolutionary pro-
cesses in the last 10 million years (Fig 2) The fossil data sug-
gest an increase of extinction from that time onwards and a later
rebound of speciation rates Estimates from the ldquothree-timersrdquo
method and PyRate fit showing neutral-to-negative net diversi-
fication that translated into a late Miocene diversity loss Phylo-
genetic rates remained steady or slightly decreased Overall we
do not recognize a direct resemblance among curves in this tem-
poral point Nevertheless it may be the case that late Miocene
depletion also contributed to the low branching rates recovered
earlier in the trees (15ndash10 Ma see Rabosky and Lovette 2008) If
the Oligocene prolonged extinction erased most of the branches
before 30 Ma the late Miocene diversity loss may also have pre-
vented part of the evolutionary signal from the middle Miocene
to be recorded in the living species trees (Harvey et al 1994a)
We rule out the possibility that this extinction pulse is an artifact
derived from poor sampling Preservation rates of the ruminant
fossil record are relatively high for the late Miocene (around 075
Fig S1) Furthermore the two methods used to analyze the fossil
data account for heterogeneous sampling in very different ways
and yet yield very similar results with tight confidence intervals
(Fig 2) Our results show a recovery in speciation during the latest
Miocene and the Pliocene from around 7 to 25 Ma Late Pliocene
speciation rebound to levels comparable to the early Miocene As
argued above this recovery probably is reflected by the trees with
nodes slightly deeper in time due to the deeper molecular esti-
mates toward the Miocene-Pliocene Very likely mainly bovids
and deer lineages led that speciation pulse including the radiation
of American deer and that of African bovid tribes (Bibi et al
2009 Cantalapiedra et al 2014c)
The Plio-Pleistocene was one of the most dramatic episodes
in ruminant evolution A critical net diversification drop recov-
ered from the fossil record couples a slowdown in the phylogenetic
rates toward the end of our analysis interval (Fig 2) Fossil-based
rates for the last 2 myrmdashonly provided by PyRate see Methodsmdash
exhibited a severe extinction event Speciation rate still remained
close to early Miocene levels during this period but extinction
significantly surpassed it (Fig 2D) The resulting replacement
process would have reshaped ruminant faunas faster than ever
The idea of a major Plio-Pleistocene climatic shift (the estab-
lishment of continental northern-hemisphere glaciations Miller
et al 2005) and human activity reshaping mammalian faunas have
been proposed for several mammalian clades (Delson 1985 Kim-
bel 1995 Lyons et al 2004 Gomez Cano et al 2013) These
suggestions are supported by our results
To our knowledge this is the first direct evidence for neg-
ative net diversificationmdashextinction above speciationmdashas being
behind the slowdowns in living species trees toward the tips often
reported in the literature (Moen and Morlon 2014) This empir-
ical case opens the possibility that indeed progressive decrease
in phylogenetic rates toward recent times may in some cases
be the result of recent and drastic climatic fluctuations triggering
extinction
Concluding remarks
Since the first studies on tree shape (Nee et al 1992 Harvey
et al 1994b) an extensive body of research has been devoted to
understand how evolutionary processes leave their signal in phy-
logenetic trees of extant taxa Most researchers have focused on
estimate evolutionary ratesmdashthat is speciation and extinctionmdash
from phylogenies of living species (Rabosky and Lovette 2008
Alfaro et al 2009 Stadler 2011a) Other studies have pursued
EVOLUTION NOVEMBER 2015 2 9 4 9
JUAN L CANTALAPIEDRA ET AL
the identification of past episodes in evolutionary trees by com-
parison with simulations (Crisp and Cook 2009) Surprisingly
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data Quental and Marshall 2010 Morlon
et al 2011 Etienne et al 2012) Simpson et al (2011) compared
phylogenetic rates with fossil-based rates but the correlation be-
tween curves was not tested statistically Here we have shown
how the combination of speciation and extinction as recovered
from the fossil record left a signal in the living species phylogeny
of ruminants through 50 myr of evolution Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved Also the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90 of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig 1) We
acknowledge that this might not be the case scenario for many
study groups
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive rep-
resentation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12) Also
calibrating phylogenies using highly tight and conservative fossil-
informed priors may not yield rate profiles that fit rates through
time from the fossil record because the major pulses in lineage
speciation may have taken place in stem lineages
Our results also provide new views on ruminant evolution
that should be contrasted in the future The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small hornless and browser forms that were
not involved in any extraordinary diversification pulse (ldquothe lull
before the stormrdquo Janis 2008) This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1 These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007) In contrast our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig 2C)
Our analyses strongly suggest that the classic ldquoMiocene ru-
minant radiationrdquo begun in Oligocene times and prolonged until
22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-
ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition
of larger body sizes (Morales et al 1993) new dietary strate-
gies (Cantalapiedra et al 2014b) and behavior (Janis 1982 1989
Brashares et al 2000) However this event and the estimated
origin of ruminant groups with horned forms (275 Ma) largely
predates the first fossil evidence of horns in ruminants (19ndash17
Ma see DeMiguel et al 2014 Fig 2C) This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al 2014) or
those horned ruminants are to be found in the Oligocene
Finally since little can be recovered from living species trees
about the first 25 myr of ruminant evolution improving the poor
Eocene and Oligocene fossil record is crucial for future paleobio-
logical studies (Blondel 2001) This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
ldquophylogenetic coveragerdquo due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al
2012 Hipsley et al 2014 McGuire et al 2014) In summary
unveiling Paleogene environmental trends and mammal commu-
nitiesrsquo dynamics will largely benefit from fossil data And basal
ruminants probably have a lot to teach us about it
ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education
DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)
LITERATURE CITEDAlfaro M E F Santini C Brock H Alamillo A Dornburg D L Rabosky
G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414
Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542
mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge
mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397
mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014
2 9 5 0 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
EVOLUTION NOVEMBER 2015 2 9 5 1
JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
JUAN L CANTALAPIEDRA ET AL
the identification of past episodes in evolutionary trees by com-
parison with simulations (Crisp and Cook 2009) Surprisingly
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data Quental and Marshall 2010 Morlon
et al 2011 Etienne et al 2012) Simpson et al (2011) compared
phylogenetic rates with fossil-based rates but the correlation be-
tween curves was not tested statistically Here we have shown
how the combination of speciation and extinction as recovered
from the fossil record left a signal in the living species phylogeny
of ruminants through 50 myr of evolution Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved Also the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90 of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig 1) We
acknowledge that this might not be the case scenario for many
study groups
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive rep-
resentation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12) Also
calibrating phylogenies using highly tight and conservative fossil-
informed priors may not yield rate profiles that fit rates through
time from the fossil record because the major pulses in lineage
speciation may have taken place in stem lineages
Our results also provide new views on ruminant evolution
that should be contrasted in the future The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small hornless and browser forms that were
not involved in any extraordinary diversification pulse (ldquothe lull
before the stormrdquo Janis 2008) This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1 These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007) In contrast our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig 2C)
Our analyses strongly suggest that the classic ldquoMiocene ru-
minant radiationrdquo begun in Oligocene times and prolonged until
22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-
ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition
of larger body sizes (Morales et al 1993) new dietary strate-
gies (Cantalapiedra et al 2014b) and behavior (Janis 1982 1989
Brashares et al 2000) However this event and the estimated
origin of ruminant groups with horned forms (275 Ma) largely
predates the first fossil evidence of horns in ruminants (19ndash17
Ma see DeMiguel et al 2014 Fig 2C) This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al 2014) or
those horned ruminants are to be found in the Oligocene
Finally since little can be recovered from living species trees
about the first 25 myr of ruminant evolution improving the poor
Eocene and Oligocene fossil record is crucial for future paleobio-
logical studies (Blondel 2001) This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
ldquophylogenetic coveragerdquo due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al
2012 Hipsley et al 2014 McGuire et al 2014) In summary
unveiling Paleogene environmental trends and mammal commu-
nitiesrsquo dynamics will largely benefit from fossil data And basal
ruminants probably have a lot to teach us about it
ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education
DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)
LITERATURE CITEDAlfaro M E F Santini C Brock H Alamillo A Dornburg D L Rabosky
G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414
Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542
mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge
mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397
mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014
2 9 5 0 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
EVOLUTION NOVEMBER 2015 2 9 5 1
JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40
Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15
mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15
Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11
Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139
Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48
Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463
Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7
Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York
Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6
Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281
Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9
Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158
Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94
Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144
Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265
Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274
DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433
Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220
Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248
Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309
Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351
Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726
Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102
Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743
Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland
Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516
Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9
Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405
Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK
Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593
Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in
R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK
Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529
Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302
mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626
Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5
Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317
mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481
mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin
Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904
Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448
Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439
Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven
EVOLUTION NOVEMBER 2015 2 9 5 1
JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
JUAN L CANTALAPIEDRA ET AL
Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York
Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490
Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358
Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA
Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181
Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172
McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7
Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524
Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore
Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298
Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197
Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54
mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene
giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230
Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525
Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332
Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969
Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326
Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672
Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441
R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria
ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014
Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260
Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875
Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610
Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999
Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187
Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403
Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131
Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367
Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436
Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284
Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828
Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521
Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146
mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192
Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544
Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven
Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439
Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283
Associate Editor M FriedmanHandling Editor J Conner
2 9 5 2 EVOLUTION NOVEMBER 2015
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3
CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website
Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants
EVOLUTION NOVEMBER 2015 2 9 5 3