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Species Richness at Continental Scales Is Dominated by Ecological LimitsAuthor(s): Daniel L. Rabosky, Allen H. HurlbertSource: The American Naturalist, Vol. 185, No. 5 (May 2015), pp. 572-583Published by: The University of Chicago Press for The American Society of NaturalistsStable URL: http://www.jstor.org/stable/10.1086/680850 .

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American Society of Naturalists Debate

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Species Richness at Continental Scales

Is Dominated by Ecological Limits*

aniel L. Rabosky1,† and Allen H. Hurlbert2

Museum of Zoology and Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48103;Department of Biology and Curriculum for the Environment and Ecology, University of North Carolina, Chapel Hill, North Carolina599

sity in a rapidly changing world. In this perspective, we as-
stract: Explaining variation in species richness among prov-
sert that species richness at continental scales is largelyeqouprnoisen

afelaabtosclainm19vife

(Esceqtiodetacoonarloriut

ces and other large geographic regions remains one of the mostallenging problems at the intersection of ecology and evolution.ere we argue that empirical evidence supports a model wherebyological factors associated with resource availability regulate spe-s richness at continental scales. Any large-scale predictive modelr biological diversity must explain three robust patterns in the nat-al world. First, species richness for evolutionary biotas is highly cor-lated with resource-associated surrogate variables, including area,perature, and productivity. Second, species richness across ep-

hal timescales is largely stationary in time. Third, the dynamics ofversity exhibit clear and predictable responses to mass extinctions,y innovations, and other perturbations. Collectively, these patternse readily explained by a model in which species richness is regu-ed by diversity-dependent feedback mechanisms. We argue thatany purported tests of the ecological limits hypothesis, includinganching patterns in molecular phylogenies, are inherently weakd distract from these three core patterns. We have much to learnout the complex hierarchy of processes by which local ecologicalteractions lead to diversity dependence at the continental scale,t the empirical evidence overwhelmingly suggests that they do.

ywords: speciation, extinction, diversity dependence, macroecol-y, equilibrium.

Introduction: For Ecological Limits

r decades, biologists have debated the relative contri-tions of equilibrium and nonequilibrium processes torge-scale patterns of species richness. Addressing this is-e remains one of the most important challenges in ecol-y and evolutionary biology because it has broad im-ications for understanding the history of diversity, theocesses that generate diversity, and the future of diver-

An earlier version of this article was presented as part of the American So-

laofnofuse

ty of Naturalists debate, which was held at the ASN stand-alone meeting atilomar, California, in January 2014.Corresponding author; e-mail: [email protected].

. Nat. 2015. Vol. 185, pp. 572–583. q 2015 by The University of Chicago.03-0147/2015/18505-55789$15.00. All rights reserved.I: 10.1086/680850

This content downloaded from 23.235.32.0All use subject to JSTOR Te

uilibrial and dominated by ecological limits. In contrast,r opponents in this debate (Harmon and Harrison 2015)opose that species richness at the largest spatial scales isnequilibrial and that ecological limits are either nonex-tent or unimportant relative to other processes that influ-ce the dynamics of speciation and extinction.We argue that the empirical evidence is consistent withtheory of species richness whereby diversity-dependentedback mechanisms regulate the number of species withinrge landmasses. This idea is simultaneously a statementout a process, its generality, and the spatiotemporal scalewhich it applies. By “continental scales,” we restrict theope of our arguments to landmasses that are sufficientlyrge that the majority of standing diversity is derived fromsitu speciation and not immigration from other land-asses (“mainlands,” in the terminology of Rosenzweig95). One can replace the word “continental” with “pro-ncial” to apply to marine faunas to much the same ef-ct (Rosenzweig 1995).In its simplest form, the ecological limits hypothesisLH) asserts (1) that species richness at biogeographicales exists in a state of dynamic equilibrium, (2) that thisuilibrium results from diversity dependence of specia-n and/or extinction rates, and (3) that diversity depen-nce of evolutionary rates results from constraints on to-l resource availability. Thus, the “ecological limit” is thenstraint on total resource availability, not a fixed limitthe number of species that can occur in a system. By

guing that continental systems are “dominated” by eco-gical limits, we claim that most of the variance in specieschness among all such geographic regions can be attrib-ed to ecological limits. As such, species richness shouldrgely be predictable from knowledge of general propertiesa system that reflect total resource availability. We dot believe that diversity equilibria can exist in a meaning-l sense without ecological limits on resources. In the ab-nce of such limits, there is little reason to postulate the

on Mon, 7 Dec 2015 16:15:32 PMrms and Conditions


diversity dependence of speciation and extinction that re-sults in equilibrial dynamics. Even MacArthur and Wilson’s(1limisl19

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on the total number of individuals that can occupy an is-land. Per-lineage extinction rates in the model rise as a func-tiopoHargrpulustmde

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Ecological Limits on Diversity 573

963) theory of island biogeography invokes ecologicalits in order to predict positive relationships betweenand size and species richness (see below; Rosenzweig95).The ELH has a long history, and it is not our intentionreview this literature here. Systems that are governed byological limits are sometimes described as “saturated” orssessing “carrying capacities.” These terms invite confu-n because they can be taken to imply that species diver-y is static or that there are a fixed number of ecologicalches. However, strong regulation by ecological limits im-ies neither fixed numbers of niches nor static diversity.nder ecological limits, the number of species in a systemould be the outcome of a stochastic process with a meanlue determined by total resource availability. The quan-y of resources can itself fluctuate through time, perhapsrough secular changes in geochemical processes (Vermeij95; Vermeij and Roopnarine 2013), changes in continen-l shelf area (Peters 2005), or through episodic key inno-tions that increase the capacity of organisms to use re-urces (Boyce et al. 2009). Such perturbations to resourceailability should facilitate periodic expansions in specieshness, potentially cascading through other trophic levelsoyce and Lee 2010; Bush and Bambach 2011; Allmond Martin 2014).We first describe a simple model illustrating the logicthe ELH. The model is agnostic with respect to specificpulation-level mechanisms but provides a heuristic toolr understanding how ecological limits can generate var-tion in species richness among clades and regions. Ween describe three major biodiversity patterns that arensistent with ecological limits yet difficult to explaintheir absence. We then discuss other forms of evidenceat are variously interpreted as for and against the eco-gical limits hypothesis.

A Phenomenological Model for Ecological Limits
ne
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n argument for ecological limits is effectively an argu-ent for the diversity dependence of mean per-lineage netversification rates. If per-lineage speciation rates decreased/or per-lineage extinction rates increase with increasinghness, then richness will ultimately approach and fluctu-e about the equilibrial value where those rates are equalg. 1). The dynamic balance between speciation and ex-ction is based on the colonization-extinction dynamicsesented in MacArthur and Wilson’s (1963, 1967) theoryisland biogeography as well as a subsequent modificationr mainland systems (MacArthur 1969; Rosenzweig 1975;own et al. 2001). Diversity equilibrium in the MacArthur-ilson model emerges, in part, because of ecological limits


n of the number of species on an island because meanpulation sizes per species decline as richness increases.ence, for a given level of species richness, extinction ratese lower on large islands than small islands, leading toeater equilibrium diversities on large islands. Althoughrely phenomenological, the simple model in figure 1 il-strates two points that are often overlooked or misunder-ood in the debate on ecological limits, and it can accom-odate a wide range of specific mechanisms for diversitypendence.First, the model clarifies the role resource availabilityays in determining the equilibrium richness of a regionlative to other factors. The finite nature of resources ise ecological limit for a region that results in a zero-summe and the ensuing dynamic equilibrium between speci-ion and extinction (Van Valen 1976; Hubbell 2001; Hurl-rt and Stegen 2014b). Variation in resource availability ispected to shift equilibrial richness in a manner analogousthe effects of area in the theory of island biogeography,influencing the functional relationship between the ex-ction rate and species richness (Wright 1983; fig. 1B).However, changes in the shape of the relationships be-een diversification and species richness can influence re-ized equilibrium richness, regardless of the underlyingol of resources. This observation implies immediatelyat regions with the same resource base can have differentuilibrium diversities (fig. 1C, S1 vs. S2), if they differ in pro-sses that affect rates of speciation and extinction. For ex-ple, if one region had increased “background” speciationtes due to increased topographical complexity (Cracraft85; Badgley 2010) or increased temperature-driven mu-tion rates (Allen et al. 2006; Gillooly and Allen 2007) rel-ive to another region, then it would be expected to sup-rt more species at equilibrium (fig. 1C). Similarly, cladesight differ in key traits that make them more or less pronespeciation (or extinction), suggesting that the phyloge-tic makeup of a biota will affect equilibrial species rich-ss (Seq) as well.Second, the model demonstrates how geographic re-ons can differ in their equilibrium diversity even if allgions have identical speciation and extinction rates ine present day (fig. 1D). This point is particularly impor-nt because it means that finding identical evolutionarytes for regions that vary in diversity is uninformativeout the role of equilibrium processes in generating thatversity. The causes of differential diversity must be soughtt only in the rates themselves but also in the derivativesthese rates with respect to species richness (Rosenzweig95).This phenomenological model is consistent with a broadnge of proposed mechanisms that result in diversity-



dependent dynamics of speciation and extinction. Sepkos-ki’s (1978) pioneering study on diversity dependence inthlefluwcagesiz20isPapo

ation (Mayr 1963; Price 2008; Kisel and Barraclough 2010).To the extent that resource-mediated interactions betweenspsc20en

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574 The American Naturalist

e fossil record provided a lucid discussion of population-vel mechanisms by which species interactions could in-ence speciation and extinction probabilities. More recentork has expanded on the consequences of local ecologi-l interactions for species diversification via their emer-nt effects on population dynamics and geographic rangee (Ricklefs and Bermingham 2007; Price 2010; Rabosky13; Hurlbert and Stegen 2014b). Geographic range sizenegatively related to extinction risk (Manne et al. 1999;yne and Finnegan 2007; Harnik et al. 2012) and may besitively correlated with opportunities for allopatric speci-


ecies limit geographic distributions across continental-ale landscapes (Price and Kirkpatrick 2009; Sexton et al.09; Pigot and Tobias 2013), such interactions can influ-ce the dynamics of speciation and extinction.Much like island biogeography theory, the ecologicalits hypothesis makes first-order predictions about pat-

rn that can be tested with minimal knowledge of the un-rlying mechanisms. Specifically, the model predicts thatecies richness at biogeographic scales should in generalrrelate with total resources (or appropriate surrogate vari-les), that species richness should typically exist in a state

Per

-line

age

rate

Richness (S)

Per

-line

age

rate

Richness (S)

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-line

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rate

Richness (S)

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S1 S2

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gure 1: A, Equilibrium model for the assembly of continental biotas. In this example, speciation rates decline and extinction rates increasea function of species richness; the intersection between these curves is the equilibrial species richness (Seq). As in MacArthur and Wilson967), extinction rates should be low when a geographic region is occupied by a few species with large population sizes and high when agion is occupied by many species with smaller population sizes. Here SMAX is the theoretical maximum species richness that would be ob-ined by speciation in the absence of any extinction. The form of the curves shown here is arbitrary, and equilibrium will emerge even in thesence of diversity-dependent speciation, provided that per capita population sizes decline with increasing species richness. B, Regional aread/or resource availability should influence the form of the relationship between extinction and species richness, with the expectation thatger areas with more resources will have greater equilibrial species richness. C, A factor that increases the baseline rate of speciation ormigration (arrow) will increase equilibrial species richness (from S1 to S2), even if the resource pool remains unchanged. Geographicgions with identical resources can thus vary in their equilibrium richness values as a function of regional or clade-specific factors that affecteciation or immigration rates. D, Geographic regions can vary in equilibrium species richness even if speciation and extinction rates areactly equal. Hence, a finding that speciation rates are similar between geographic regions that differ in richness provides no evidence for anequilibrium model of diversity accumulation.



of dynamic equilibrium, and that richness should respondpredictably to perturbation.

Thscsttuthgrthgecota!5exboicvatomsitecnoth

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strongest predictors of total richness (fig. 2). For plants,energy- and productivity-associated variables consistentlyemri


Ecological Limits Can Explain the “Big Three”
Patterns of Diversity
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e predictions of the ecological limits hypothesis de-ribed above are strongly supported by three of the mostriking large-scale spatiotemporal patterns in the struc-re and dynamics of biological diversity. First, most ofe variation in species richness among major biogeo-aphic regions can be explained by surrogate variablesat reflect the total pool of resources available in a givenographic region. Second, species richness is generallynstant in time, at least over timescales relevant to the es-blishment of diversity equilibria (e.g., epochal timescales;0 million years). Third, the dynamics of species richnesshibit clear and predictable responses to perturbations,th positive and negative. Thus, mass extinctions are typ-ally followed by recoveries, and major evolutionary inno-tions that increase the resource economy of the biota leadincreases in diversity. In isolation, each of these patternsay be consistent with nonequilibrial mechanisms of diver-y regulation. Yet all three emerge immediately from theological limits hypothesis, while predictions of any singlenequilibrial model typically contradict one or more ofese patterns.

Species Richness Is Correlated with Area and Energy
eqgeattioasdiby
by Exponential Increase

DinnezeTtimofarpragforesi

ne of the most striking patterns in the global distributionspecies richness is the correlation between the area ofregion and its species richness (MacArthur and Wilson63). Area is, of course, a surrogate variable that scalesith various measures of total resources (Wright 1983;senzweig 1995). By virtue of an expanded resource base,rger areas can generally support more individuals thanaller areas; a consequence of this relationship is an in-ease in realized equilibrium diversities relative to smallereas. At the scale of biotic provinces, area emerges consis-ntly as the strongest single predictor of species diversityosenzweig 1995), explaining up to 84% of the variation inrrestrial vertebrate richness among major zoogeographicgions (97% for area plus a single climate parameter; Ro-nzweig et al. 2012). At this spatial scale, the species-arealationship cannot reflect sampling effects, as we are con-ering entire biotas that were assembled largely by in situversification processes. Recent analyses at the level of bio-ographic provinces have found strong effects of area,oductivity, and temperature on vertebrate species rich-ss. Although time-associated variables are highly corre-ted with the number of endemic species within regionsetz and Fine 2012), area and productivity remain the


erge as the strongest predictors of species richness (Cur-e 1991; Kreft and Jetz 2007). At continental to global scales,e relationship is unambiguous: every large-scale studyviewed by Gilman andWright (2006) found a positive re-tionship between productivity and species richness. Whileological limits are not mutually exclusive with other hy-theses that might affect the shape of speciation and im-igration curves, the strength of these correlations is con-stent with the idea that ecological limits are the mostportant of these drivers.Other hypotheses have been proposed to account forese patterns, including the kinetic effects of temperaturegenetic divergence (Rohde 1992; Allen et al. 2002). Whileis true that rates of speciation (or extinction) might varystematically across geographic regions, this hypothesisedicts at best a weak relationship with area and othervironmental factors, because any variation in the agesclades among regions will decrease the relationship be-een diversification rate and richness. There has yet beendemonstration of a nonequilibrium process that can

motely approach the explanatory power of equilibriumodels in accounting for evolutionary species-environmentrrelations. In the equilibrium framework described above,e noted that geographic variation in speciation or extinc-n rates can lead to differences in equilibrium diversitiesr regions with identical levels of resources (fig. 1C). Thisads to a “weak” version of the ELH, whereby diversity isuilibrial but much of the variation in richness amongographic regions is nonetheless driven by regional vari-ion in evolutionary rates. However, the general observa-n that species richness is highly correlated with resource-sociated variables suggests that, in general, equilibriumversities are influenced more by resource availability thanthese regional factors.

Species Richness Is Not Characterized

iversity-independent models also predict high volatilityspecies richness: at any given point in time, species rich-ss should be increasing exponentially or decreasing toro. This volatility is rarely observed in the fossil record.his is not to say that diversity has not increased throughe (clearly it has; see next section) but that the dynamicsdiversity throughout most of the history of life on Earthgue in favor of a strongly regulated diversity-dependentocess. The evidence for this pattern—and, in particular,ainst the idea that diversity ever shows exponential risesr any substantial durations of time—is too extensive toview adequately here. At global scales, marine biodiver-ty appears largely equilibrial across the entirety of the



Phin response to the availability of shallow water and reefharetioeqhomreclflude

po(Wbyrenobueqcoci

and transformative key innovations, local diversity is largelystroplrigathnethstzoleansi19itascDriofba

R2 = 0.40 R2 = 0.37A B

Fi(Bar


bitats (Alroy 2010a, 2010b). Similar patterns emerge forgional faunas using standardized methods of data collec-n. North American mammals collectively show largelyuilibrial diversity dynamics (Alroy 2009), a pattern thatlds for at least some individual subclades within mam-als (Van Valkenburgh and Janis 1993; Liow and Fina-lli 2014). Large-scale diversity trends are often coupled toimate-associated variables (Jaramillo et al. 2006), but thesectuations in diversity are fully consistent with diversity-pendent controls (Ezard et al. 2011).Trends in local diversity through geological time cantentially provide strong tests of the equilibrial modeliens 2011), as local paleocommunities are less influencedmany confounding factors that compromise global or

gional diversity curves (Bambach 1977). This test doest require independence of local and regional diversityt is simply based on the assumption that—under non-uilibrium, expansionist models—local diversity shouldntinue to rise as new species are added to the regional spe-es pool through speciation. The evidence from local com-


atic through time, at least in the absence of severe envi-nmental perturbations (e.g., Barry et al. 2002). For exam-e, the evolution of angiosperms resulted in a pronouncedse in diversity within local assemblages (Knoll 1986; Lid-rd and Crane 1990). However, it is incorrect to suggestat this shift in diversity is consistent with an overall expo-ntial and unbounded rise in land plant diversity. Beforee origin of angiosperms, local floras are characterized byable diversity levels over much of the Paleozoic and Meso-ic (Knoll 1986). The pulse of angiosperm diversity did notad to sustained exponential rise within local communitiesd was accompanied by concomitant declines in the diver-ty of gymnosperms and free-sporing plants (Lupia et al.99). Taphonomically matched samples from specific hab-ts have shown no change in floral richness over time-ales that span several hundred million years (Wing andiMichele 1995). Similar patterns are observed for the ma-ne benthos, where episodic increases in species richnessmarine invertebrates have undoubtedly occurred (Bam-ch 1977; Bush and Bambach 2011). However, these in-

anerozoic, despite increases and decreases of diversity munities is unambiguous: with the exception of episodic

2.0 2.5 3.0 3.5 4.0

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3.5

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log 1

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3.0 4.0 5.0 6.0

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gure 2: Relationship between total vertebrate species richness of 32 bioregions and bioregion area (A), time-integrated bioregion area), total contemporary bioregion productivity (C), and total time-integrated bioregion productivity (D). Contemporary productivity per unitea is a stronger predictor of total vertebrate richness than either area or time-integrated area. Data from Jetz and Fine (2012).



creases appear to have involved major expansions in eco-logical space associated with colonization of new habitats(eorgi

Thabtutocrinriadi(rofstDexangucufuthetlamtiofrthgeof

exbihatiodievsoeqandrthfeBofothciwof

sperm leaf hydraulics potentially facilitated themassive risein flowering plant diversity that occurred in the late Creta-cepaha


.g., the muddy benthos; Rosenzweig and Taylor 1980)the evolution of fundamentally novel ecological strate-es (Bambach et al. 2007; Bush and Bambach 2011).

Species Richness Responds Predictably to Perturbations
Limits Hypothesis
InungrcaforawinfeOlimfrpobrthpathcalinof

Molecular Phylogenies

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e ecological limits hypothesis makes two predictionsout biotic responses to perturbations. First, negative per-rbations—mass extinctions, in particular—should leaddiversity recoveries. Second, positive perturbations—in-eases in the resource base available to a biota—predictcreases in species richness to stable but greater equilib-l levels. The diversity-independent model does not pre-ct either of these patterns. Diversity recoveries entail aelatively) rapid rise in species diversity in the aftermathmajor extinction events, followed by the resumption ofationary dynamics showing little net change in richness.iversity recoveries are documented for nearly all majortinction events and across a wide range of taxa (e.g., Krugd Patzkowsky 2004; Brayard et al. 2009). We are not ar-ing that recovery dynamics are simple, that rebounds oc-r instantaneously, or that postextinction ecosystems arenctionally identical to pre-extinction ecosystems. Clearly,ere is great complexity to the recovery process (Erwinal. 1987; Erwin 2001): recovery may be associated withg times (Chen and Benton 2012), ecological interactionsay be restructured (Wagner et al. 2006), and postextinc-n replacement diversity may be phylogenetically distinctom the pre-extinction biota (Sallan and Coates 2010). Butere is no question that recoveries typically occur, and thisneral phenomenon is difficult to explain in the absencestrong diversity-dependent controls.A second type of perturbation occurs when intrinsic ortrinsic factors increase the resource base available to aota. Clearly, the evolutionary invasion of new habitatss facilitated increases in species richness: the coloniza-n of land, for example, led to a dramatic rise in globalversity across the Phanerozoic. However, other types ofolutionary innovations can permanently alter the re-urce constraints on biotas and lead to expansions of theuilibrial levels at which diversity is regulated (Vermeijd Roopnarine 2013). For example, the evolution of hy-aulic features in angiosperm leaves more than doubledeir photosynthetic capacity relative to gymnosperms andrns (Boyce et al. 2009; Brodribb and Feild 2010; Jan deer et al. 2012). This event was a physiologically trans-rmative key innovation that increased total energy fluxrough the biota and that, under the ELH, should have fa-litated a global expansion of species richness. Althoughe are in the early stages of addressing the implicationsthese findings (Feild et al. 2011), the evolution of angio-


ous (Knoll 1986; Lupia et al. 1999). This and similar ex-nsions in the energy economy of biotas appear to haved effects that are fully predicted by the ELH.

Phylogenetic Data and the Ecological

many ways, phylogenetic data have transformed ourderstanding of the diversification process. For the manyoups of organisms that lack adequate fossil records, time-librated phylogenies of living species provide the only in-rmation we will ever have about variation in speciationtes through time and among lineages. Phylogenetic dataill continue to be of fundamental importance in explain-g why species richness varies so dramatically among dif-rent groups of organisms (Mitter et al. 1988; Coyne andrr 2004). However, it is increasingly clear that there areits to what can be inferred about diversity dynamics

om phylogenetic data alone, and we agree with manyints raised by Harmon and Harrison (2015). Below, weiefly highlight several reasons why phylogenetic tests ofe ecological limits model are inherently weak, and—inrticular—why they typically cannot be used to rejecte ELH. A focus on phylogenetic diversification patternsn be a distraction from the three robust patterns out-ed above, which are difficult to explain in the absenceecological limits.

Diversification Patterns in Time-Calibrated

olecular phylogenies frequently reveal evidence for de-lerations in the rate of speciation through time duringe course of evolutionary radiations, consistent with neg-ive feedback between species richness and diversificationabosky and Lovette 2008; Etienne and Haegeman 2012).owever, there are numerous caveats that apply to the in-rpretation of phylogenetic diversification patterns. Weill not review these issues here, other than to note thatylogenetic estimates of diversification rates can be biasedtaxon sampling, phylogeny reconstruction, and other

ctors (Revell et al. 2005; Cusimano and Renner 2010;ienne and Rosindell 2012; Harmon and Harrison 2015).number of confounding factors can create the impres-on that diversification has slowed through time (Rabosky09; Moen and Morlon 2014). In our view, the assump-n that “early burst” patterns in molecular phylogeniese the only lineage accumulation patterns consistent withversity dependence is conceptually flawed, because strictlyuilibrial processes of diversity regulation are consistentith many patterns in phylogenetic trees that do not involve



apparent slowdowns in speciation (Rabosky 2009). For ex-ample, the early burst signal is primarily relevant to earlystwat

Threricmexthspamreric

Thus, an observation that regions with greater species rich-ness have had a longer history of occupancy, as inferredfrlimanexto

Fiofniinpo95uninrecoricpr


ages of an evolutionary radiation, and this signal willeaken and ultimately disappear for clades that have beenequilibrium for long periods of time (fig. 3).

Positive “Time-for-Speciation” RelationshipIs Consistent with Ecological Limits

loba

agcaliboftoifictimbecl

e effect of time on the species richness of geographicgions has long been recognized (Fischer 1960). If specieshness is not regulated by diversity-dependent feedbackechanisms, and if speciation rates consistently exceedtinction rates, then diversity should generally increaserough time. This logicism has led to the argument that ifecies richness of clades within a geographic region (orong regions: Stephens and Wiens 2003) is positively cor-lated with their age (or time within regions), then specieshness cannot be equilibrial (Wiens 2011; Cornell 2013).

8A


om phylogenetic data, would argue against the ecologicalits hypothesis. There are several reasons for caution inalyzing the relationship between time and diversity. Forample, it can be difficult to distinguish between asymp-tic, bounded diversity trajectories (consistent with eco-gical limits) and exponential clade growth with highckground extinction (Rabosky 2012).Most importantly, a positive relationship between thees of clades within regions and their species richnessnnot reject the possibility that diversity is strictly equi-rial. In a spatial context, if a clade originates in a regionhigh resource availability and diversifies and dispersesadjacent regions with progressively fewer resources, evendiversification is governed by strictly equilibrial dynam-s, a positive relationship is expected between the estimatede-within-region and species richness of the region (Hurl-rt and Stegen 2014a). As such, the relationship betweenade age (or time in a region) and species richness is not use-

B C

2x 4x 6x 8x 10x

-8

-6

-4

-2

0

2

4

6

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gure 3: A, Results of simulation illustrating that equilibrium diversification dynamics need not be associated with the “early burst” modeldiversification. Five hundred phylogenies were simulated under a diversity-dependent speciation process with constant extinction, begin-ng with a single lineage and parameterized exactly as in figure 2 from Liow et al. (2010). Polygons give the medians and 90% confidencetervals on the distribution of the gamma statistic (g) for reconstructed phylogenetic trees (e.g., with extinct species removed) at each timeint. Values of g less than zero are suggestive of declining speciation rates through time. An asterisk indicates the point in simulation where% of simulated trees had reached their equilibrium diversity, mediated by equal speciation and extinction rates (90 lineages). Time is inits of expected taxon durations, which is simply the inverse of the extinction rate. The distribution of g is maximally negative at the pointtime where equilibrium is first reached but rapidly becomes positive as lineage turnover erodes the signal of rapid speciation. B, A rep-sentative phylogenetic tree, pruned of extinct lineages, from the time when equilibrium was first reached (1# taxon durations); note thencentration of early speciation events and negative g. C, Representative phylogenetic tree 9# taxon durations after achieving equilibriumhness; g is positive, and most speciation events are clustered at the tips of the tree. Some residual signal of the initial speciation pulse is stillesent in C, but sufficient time (and/or fluctuations in population size) will ultimately eliminate this effect.



ful for making inferences about the presence or absence ofecological limits.

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stronger signature of history, time, and the idiosyncrasyof specific resource-use strategies or climatic tolerances.Tno


Counterarguments
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Invasions and the Dynamics of Species Richness

many regions, species richness appears to have in-eased in recent decades as invasive species have colo-zed with few subsequent extinctions (Sax et al. 2002;ohlgren et al. 2008). Such observations have been inter-eted as evidence against saturation. As alluded to above,wever, the term “saturation” confuses the idea of somerd limit to the number of species in a region as opposeda stationary equilibrium reflecting the balance betweenposing processes. If one result of the Anthropocene hasen the increased spread of invasive species around theorld, this effect amounts to an increase in background col-ization or immigration rates (as in fig. 1C) and, hence, anpected increase in the equilibrial level of species richness.uman-facilitated dispersal of invasive species may also ef-ctively increase the size of the regional species pool bylowing colonization from more distant locales than wasssible in the past, again increasing the equilibrial richnesslue. As such, the observation that species richness has in-eased at particular sites in response to increased (human-ediated) colonization rates is fully consistent with a dy-mic equilibrial model of species richness and cannot, byelf, reject the ecological limits hypothesis.Something more difficult to ascertain is whether we arerrently at the new equilibrium set by increased rates ofman-assisted colonization or whether we are above it.arious authors have described the concept of “extinctionbt,” or the idea that there is often a time lag between whensystem is perturbed and when species actually go extinctilman et al. 1994; Jackson and Sax 2010). This impliesat in some locales or regions, the observed increase in spe-es richness may be temporary, with extinctions expected ine future. Two recent meta-analyses examining thousandslocal communities over recent decades concluded thatecies richness has exhibited no directional trend on aver-e (Vellend et al. 2013; Dornelas et al. 2014). These findingsggest that a balance between local colonizations and ex-ctions is the norm (Brown et al. 2001) and that invasionsnot perpetually increase species richness.

Phylogenetic Scale Matters
evna19m20of
ological limits based on an overarching energetic con-raint will typically apply to large inclusive clades overhich a zero-sum game is a reasonable characterizationurlbert and Stegen 2014b). The examination of smallades, such as genera or families, is expected to reveal a


hus, individual mammal clades appear to show largelynequilibrial dynamics at fine phylogenetic scales (Quen-l and Marshall 2013), but mammals as a whole (andore inclusive subgroups) show much greater evidence foruilibrial dynamics across the Cenozoic (Alroy 2009). Alated prediction is that the species richness of large, in-usive clades should be strongly correlated with total re-urce availability, while small clades might show variabled even negative relationships (Currie 1991; Hurlbert andegen 2014b).

Local-Regional Richness Correlations

ne argument against the idea of ecological limits at localales is the observation that local richness often increasesearly with the richness of the broader regional speciesol (Cornell and Lawton 1992; Karlson et al. 2004). If lim-exist, so the argument goes, then local richness should

vel off as regional richness increases. However, an effectregional richness on local communities is fully consis-nt with an equilibrial diversity framework, in that re-ons with a larger species pool should have immigrationrves and, consequently, equilibrial richness values shiftedward higher values (MacArthur and Wilson 1963; Loreaud Mouquet 1999; He et al. 2005; fig. 1C). Second, theamination of this relationship in isolation ignores thetentially confounding effects of environmental variablesat might drive both regional and local richness (Whited Hurlbert 2010; Gronroos and Heino 2012). Finally, amber of statistical and conceptual problems have beenised regarding the connection between the local-regionalchness relationship and inferences about limits (Srivastasa99; Hillebrand and Blenckner 2002; He et al. 2005).

Dynamics of Local Communities

t the biogeographic scales discussed here, the ecologicalits hypothesis does not make any claims about the equi-rium or nonequilibrium nature of local communities, aseasured over ecological timescales. If all local communi-s are at equilibrium, it necessarily follows that regionalotas must also be at equilibrium because diversity at thegional scale is the sum of local richness. However, specieschness at regional scales can show equilibrium propertiesen if local communities typically appear to be open, dy-mic assemblages of species (DeAngelis and Waterhouse87; Turner et al. 1993; McPeek 2007). This idea is funda-ental to metacommunity theory (Mouquet and Loreau03; Leibold et al. 2004) as well as more general theoriesspecies richness that describe how environmental hetero-



geneity and life-history trade-offs contribute to the mainte-nance of species richness at larger spatial scales, despitenosotrmnebuchthceimeqeqWacecciintuEqeqlosp

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nerozoic has undoubtedly become more diverse, suggest-ing to some that there is little evidence for constraints onspsiitnoth20aterga

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nequilibrium dynamics at small spatial scales (Hutchin-n 1951; Andrewartha and Birch 1954; Huston 1979; Pe-aitis et al. 1989). For example, in McPeek’s (2007, 2008)etacommunity simulation model, global-scale species rich-ss achieved a dynamic speciation-extinction equilibrium,t community composition at the local scale was continuallyanging in response to colonizations and extinctions ate level of individual patches. Most naturalists would ac-pt that ecological succession following disturbance is anportant process in many communities, yet these non-uilibrium dynamics are fully compatible with fixed oruilibrial global species pools (Sousa 1979). We agree withiens (2011) that local community dynamics as measuredross paleontological timescales are relevant to testing theological limits hypothesis, but such samples are useful pre-sely because they average out the short-term fluctuationscommunity composition that can be attributed to dis-rbance, succession, and other nonequilibrial processes.uilibrium dynamics at continental scales do not requireuilibrium dynamics at the local scale, and hence tests ofcal-scale equilibrium are largely uninformative with re-ect to the ecological limits hypothesis.

onclusion: An Equilibrial World, Most of the Time
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ny general theory of diversity at continental or provin-al scales must address a core set of observations aboute dynamics of species richness in space and time. Theseservations include the striking variation in species rich-ss among geographic regions, the general stability of spe-es richness over geological timescales, and the responserichness to both mass extinctions and resource pulses.e believe that the ecological limits hypothesis can ac-unt for these observations with considerably fewer pa-meters than alternative models that postulate a diversity-dependent, nonequilibrial world. We have argued hereat the data are most consistent with a “strong” versionthe ELH, but we would agree that many other factorsn influence species richness. It is almost certainly the caseat provincial biotas include residual effects of historicalctors, and we also expect that the phylogenetic makeupbiotas has a substantial effect on the dynamics of re-urce use that ultimately determine richness. Nevertheless,e argue that richness reflects an equilibrium between spe-ation and extinction imposed by the finite nature of re-urces and that resource limits are the most important de-rminant of that equilibrial level.In our opinion, biologists face two prominent challengestesting the ELH. The first challenge involves defining thepropriate temporal and spatial scale over which limitse expected to operate. For example, life across the Pha-


ecies richness (Benton 2009). Yet this increase in diver-ty is fully consistent with the ELH: when diversity rises,often does so in response to rare but transformative in-vations that increase the flux of energy and materialsrough the biosphere (Vermeij 1995; Allmon and Martin14). Much evidence from the fossil record suggests that,the scale of geological periods, species richness is gov-ned by the equivalent of a macroevolutionary zero-summe.The second challenge arises from the intersection ofultiple competing factors that can account for large-scaleversity gradients. For example, Fine and Ree (2006) dem-strated that the correlation between the geographic area11 biomes and their present-day tree diversity was rel-ively weak but that the time-integrated area of biomesd much greater explanatory power. However, biome agealso correlated with energy and productivity: high-latitudereal regions are young and energy poor and have few spe-es relative to their area. In this essay, we have argued pro-catively for the ubiquity of ecological limits, but our fieldlikely to continue debating this question for some timepart because large-scale patterns are poorly replicated.g., there are only a few biogeographic provinces) andultiple factors covary systematically with respect to spe-es richness.For this perspective, we were asked to address the ques-n, What would it take to change your mind? We feelat the strong version of the ecological limits hypothesisould be rejected if species richness at continental/provin-al scales is ultimately found to correlate more stronglyith historical factors such as biome age than with aread energy, once collinearity of other variables has beenken into account. Likewise, we would be convinced if theparent “epochal steady state” (Rosenzweig 1975) of spe-es richness in the fossil record is found to be illusory. Fi-lly, clear predictions about speciation dynamics at mac-evolutionary scales emerge from the ecological limitsodel. In a diversity-dependent world, species diversityould increase primarily in response to evolutionary in-vations that facilitate novel patterns of resource use.he diversity-independent model, in contrast, predicts thatecies diversity should rise as lineages acquire innova-ns that promote lineage splitting. Under the ELH, split-g is not enough: without ecological divergence, split-g merely carves a fixed pool of resources into smallerr capita shares, leading to low persistence of diverged lin-ges over geological timescales. At the risk of grossly over-mplifying a complex topic, we find it striking that so manyctors that are expected to increase the evolution of re-oductive isolation between diverging lineages (e.g., lineagelitting) are, at best, weakly correlated withmacroevolution-



ary speciation dynamics (Kraaijeveld et al. 2011; Raboskyand Matute 2013), yet innovations that increase resourcecasit

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diversity. Proceedings of the Royal Society B: Biological Sciences277:3437–3443.

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pacities are consistently associated with large-scale diver-y increase.

Acknowledgments

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e thank L. Harmon and S. Harrison for an engaging de-te on this topic and T. Price for organizing this specialent at the 2014 ASN conference in Asilomar. We thankFine, T. Price, A. Rabosky, R. Ricklefs, D. Schluter, andembers of the Rabosky lab for comments on the manu-ript. Both authors contributed equally to this work.

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