Inferences of biogeographical histories within subfamily Hyacinthoideae using S-DIVA and Bayesian binary MCMC analysis implemented in RASP (Reconstruct Ancestral State in Phylogenies) Syed Shujait Ali 1,3, *, Yan Yu 2, *, Martin Pfosser 3 and Wolfgang Wetschnig 1 1 Institute of Plant Sciences, Karl-Franzens-University Graz, Holteigasse 6, A-8010 Graz, Austria, 2 School of Life Sciences, Sichuan University, Chengdu 610064, Sichuan, China and 3 Biocenter Linz, J.-W.-Klein-Str. 73, A-4040 Linz, Austria * For correspondence. E-mail [email protected]or [email protected]Received: 5 May 2011 Returned for revision: 6 July 2011 Accepted: 22 September 2011 † Background and Aims Subfamily Hyacinthoideae (Hyacinthaceae) comprises more than 400 species. Members are distributed in sub-Saharan Africa, Madagascar, India, eastern Asia, the Mediterranean region and Eurasia. Hyacinthoideae, like many other plant lineages, show disjunct distribution patterns. The aim of this study was to reconstruct the biogeographical history of Hyacinthoideae based on phylogenetic analyses, to find the possible ancestral range of Hyacinthoideae and to identify factors responsible for the current disjunct distribution pattern. † Methods Parsimony and Bayesian approaches were applied to obtain phylogenetic trees, based on sequences of the trnL-F region. Biogeographical inferences were obtained by applying statistical dispersal-vicariance analysis (S-DIVA) and Bayesian binary MCMC (BBM) analysis implemented in RASP (Reconstruct Ancestral State in Phylogenies). † Key Results S-DIVA andBBM analyses suggest that the Hyacinthoideae clade seem to have originated in sub- Saharan Africa. Dispersal and vicariance played vital roles in creating the disjunct distribution pattern. Results also suggest an early dispersal to the Mediterranean region, and thus the northward route (from sub-Saharan Africa to Mediterranean) of dispersal is plausible for members of subfamily Hyacinthoideae. † Conclusions Biogeographical analyses reveal that subfamily Hyacinthoideae has originated in sub-Saharan Africa. S-DIVA indicates an early dispersal event to the Mediterranean region followed by a vicariance event, which resulted in Hyacintheae and Massonieae tribes. By contrast, BBM analysis favours dispersal to the Mediterranean region, eastern Asia and Europe. Biogeographical analysis suggests that sub-Saharan Africa and the Mediterranean region have played vital roles as centres of diversification and radiation within subfamily Hyacinthoideae. In this bimodal distribution pattern, sub-Saharan Africa is the primary centre of diversity and the Mediterranean region is the secondary centre of diversity. Sub-Saharan Africa was the source area for radiation toward Madagascar, the Mediterranean region and India. Radiations occurred from the Mediterranean region to eastern Asia, Europe, western Asia and India. Key words: Asparagaceae, biogeography, S-DIVA, Hyacinthoideae, Bayesian binary MCMC, RASP, Scilloideae. INTRODUCTION Phylogenetically based historical biogeographical reconstruc- tions are now an important way to illuminate the evolution- ary history of organisms in space and time. The enormous growth of biogeographical studies has resulted from the rapid accumulation of phylogenetic data during the last two decades. Recently, model- and event-based approaches have been used for biogeographical inferences. The Lagrange (likelihood analysis of geographical range evolution) imple- menting dispersal-extinction cladogenesis (DEC) model (Ree et al., 2005; Ree and Smith, 2008) and the BIB (Bayesian island biogeography) method (Sanmartı ´n et al., 2008, 2010) were recently applied to biogeographical ana- lysis, but the event-based method dispersal vicariance ana- lysis (DIVA; Ronquist, 1997, 2001) has remained the most popular and widely used method for reasons of simplicity. In the DIVA method, ancestral distributions are inferred based on a three-dimensional cost matrix derived from a simple biogeographical model (Ronquist, 1997). Two pro- blems, uncertainty in phylogeny and uncertainty in ancestral area optimization, are attached to it. Nylander et al. (2008) proposed a new method, Bayes-DIVA, to overcome the un- certainties in DIVA analysis. Similarly, Harris and Xiang (2009) proposed their approach, an alternative to Bayes-DIVA. Their method differs in its ability to handle un- certainty at some nodes. The Statistical DIVA (S-DIVA; Yan et al., 2010) method rectified the problems in DIVA analysis and the results are comparable with those obtained by Bayes-DIVA. RASP (Reconstruct Ancestral State in Phylogenies) (Yan et al., 2011) is a useful tool to reconstruct evolutionary histories in phylogeny. Three different methods, S-DIVA, Bayesian binary MCMC (BBM) and maximum-parsimony (MP) ana- lysis, are implemented in RASP to obtain ancestral ranges at each node. S-DIVA and BBM methods suggest possible ances- tral ranges at each node and also calculate probabilities of each ancestral range at nodes. # The Author 2011. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. 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Inferences of biogeographical histories within subfamily Hyacinthoideae usingS-DIVA and Bayesian binary MCMC analysis implemented in RASP
(Reconstruct Ancestral State in Phylogenies)
Syed Shujait Ali1,3,*, Yan Yu2,*, Martin Pfosser3 and Wolfgang Wetschnig1
1Institute of Plant Sciences, Karl-Franzens-University Graz, Holteigasse 6, A-8010 Graz, Austria, 2School of Life Sciences,Sichuan University, Chengdu 610064, Sichuan, China and 3Biocenter Linz, J.-W.-Klein-Str. 73, A-4040 Linz, Austria
Received: 5 May 2011 Returned for revision: 6 July 2011 Accepted: 22 September 2011
† Background and Aims Subfamily Hyacinthoideae (Hyacinthaceae) comprises more than 400 species. Membersare distributed in sub-Saharan Africa, Madagascar, India, eastern Asia, the Mediterranean region and Eurasia.Hyacinthoideae, like many other plant lineages, show disjunct distribution patterns. The aim of this study wasto reconstruct the biogeographical history of Hyacinthoideae based on phylogenetic analyses, to find the possibleancestral range of Hyacinthoideae and to identify factors responsible for the current disjunct distribution pattern.† Methods Parsimony and Bayesian approaches were applied to obtain phylogenetic trees, based on sequences ofthe trnL-F region. Biogeographical inferences were obtained by applying statistical dispersal-vicariance analysis(S-DIVA) and Bayesian binary MCMC (BBM) analysis implemented in RASP (Reconstruct Ancestral State inPhylogenies).† Key Results S-DIVA and BBM analyses suggest that the Hyacinthoideae clade seem to have originated in sub-Saharan Africa. Dispersal and vicariance played vital roles in creating the disjunct distribution pattern. Resultsalso suggest an early dispersal to the Mediterranean region, and thus the northward route (from sub-SaharanAfrica to Mediterranean) of dispersal is plausible for members of subfamily Hyacinthoideae.† Conclusions Biogeographical analyses reveal that subfamily Hyacinthoideae has originated in sub-SaharanAfrica. S-DIVA indicates an early dispersal event to the Mediterranean region followed by a vicariance event,which resulted in Hyacintheae and Massonieae tribes. By contrast, BBM analysis favours dispersal to theMediterranean region, eastern Asia and Europe. Biogeographical analysis suggests that sub-Saharan Africaand the Mediterranean region have played vital roles as centres of diversification and radiation within subfamilyHyacinthoideae. In this bimodal distribution pattern, sub-Saharan Africa is the primary centre of diversity and theMediterranean region is the secondary centre of diversity. Sub-Saharan Africa was the source area for radiationtoward Madagascar, the Mediterranean region and India. Radiations occurred from the Mediterranean region toeastern Asia, Europe, western Asia and India.
Phylogenetically based historical biogeographical reconstruc-tions are now an important way to illuminate the evolution-ary history of organisms in space and time. The enormousgrowth of biogeographical studies has resulted from therapid accumulation of phylogenetic data during the last twodecades. Recently, model- and event-based approaches havebeen used for biogeographical inferences. The Lagrange(likelihood analysis of geographical range evolution) imple-menting dispersal-extinction cladogenesis (DEC) model(Ree et al., 2005; Ree and Smith, 2008) and the BIB(Bayesian island biogeography) method (Sanmartın et al.,2008, 2010) were recently applied to biogeographical ana-lysis, but the event-based method dispersal vicariance ana-lysis (DIVA; Ronquist, 1997, 2001) has remained the mostpopular and widely used method for reasons of simplicity.In the DIVA method, ancestral distributions are inferredbased on a three-dimensional cost matrix derived from a
simple biogeographical model (Ronquist, 1997). Two pro-blems, uncertainty in phylogeny and uncertainty in ancestralarea optimization, are attached to it. Nylander et al. (2008)proposed a new method, Bayes-DIVA, to overcome the un-certainties in DIVA analysis. Similarly, Harris and Xiang(2009) proposed their approach, an alternative toBayes-DIVA. Their method differs in its ability to handle un-certainty at some nodes.
The Statistical DIVA (S-DIVA; Yan et al., 2010) methodrectified the problems in DIVA analysis and the results arecomparable with those obtained by Bayes-DIVA. RASP(Reconstruct Ancestral State in Phylogenies) (Yan et al.,2011) is a useful tool to reconstruct evolutionary histories inphylogeny. Three different methods, S-DIVA, Bayesianbinary MCMC (BBM) and maximum-parsimony (MP) ana-lysis, are implemented in RASP to obtain ancestral ranges ateach node. S-DIVA and BBM methods suggest possible ances-tral ranges at each node and also calculate probabilities of eachancestral range at nodes.
# The Author 2011. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
The family Hyacinthaceae [¼ Asparagaceae subfamilyScilloideae sensu APG III (2009)and Chase et al. (2009)] con-sists of approx. 900 species and 70 genera (Speta, 1998a, b) intemperate and tropical regions (e.g. Mwafongo et al., 2010).Members of this family can be found in different habitats,but most species are adapted to seasonal climates with pro-nounced dry and wet periods. Southern Africa has thehighest diversity, followed by the Mediterranean region(Stedje, 1996). The Fynbos (Cape area) and succulent Karooregions of southern Africa have the highest species diversity.The molecular analyses of Pfosser and Speta (1999) andManning et al. (2004) resulted in the recognition of fourmonophyletic clades in the family Hyacinthaceae. These fourclades are treated as subfamilies Oziroeoideae, Urgineoideae,Ornithogaloideae and Hyacinthoideae (Pfosser and Speta,1999, 2001; Manning et al., 2004). Alternatively,Hyacinthaceae is nested within Asparagaceae sensu lato andcan be treated as subfamily Scilloideae. Hyacinthaceae aremonophyletic within Asparagaceae and the subfamilies men-tioned above are then treated as tribes Hyacintheae,Ornithogaleae, Oziroeeae and Urgineeae (e.g. APG III,2009; Chase et al., 2009). Here we use Hyacinthaceae at thefamily level. Subfamily Oziroeoideae is restricted to SouthAmerica and consists of five species. The number of speciesin subfamily Urgineoideae is .100 (Manning et al., 2004),and Ornithogaloideae consists of 200–300 species (Manninget al., 2009; Martınez-Azorın et al., 2011); the remaining400+ species form Hyacinthoideae. As most of thesub-Saharan African representatives of Hyacinthaceae occupyearly branching positions in the phylogenetic analyses(Pfosser and Speta, 1999, 2001; Pfosser et al., 2003, 2006;Manning et al., 2004; Martınez-Azorın et al., 2011), it is com-monly accepted that the whole family evolved from thatregion. Except for Oziroeoideae, all subfamilies exhibit abimodal distribution pattern. A primary centre of diversity islocated in sub-Saharan Africa, and a secondary centre of diver-sity occurs in the northern hemisphere around theMediterranean, extending, at least for subfamilyHyacinthoideae, as far as East Asia. This split between north-ern and predominantly southern hemisphere taxa is most pro-nounced in subfamily Hyacinthoideae, which has beenfurther subdivided into tribes Hyacintheae (northern hemi-sphere) and Massonieae (southern hemisphere, Madagascar,Arabia and India) (Pfosser and Speta, 1999; Pfosser et al.,2003; Wetschnig and Pfosser, 2003).
Pseudoprospero Speta occupies an early branching positionin the phylogenetic tree and is sister to Massonieae andHyacintheae. If Pseudoprospero is excluded fromMassonieae, then molecular data suggest that Massonieaeand Hyacintheae evolved independently (Pfosser et al.,2003). Tribe Massonieae is monophyletic upon the exclusionof genus Pseudoprospero (Pfosser et al., 2003), and it hasbeen suggested that Pseudoprospero should be placed into atribe of its own (Wetschnig et al., 2002; Pfosser et al.,2003). This led to the creation of a third monotypic tribePseudoprospereae (Manning et al., 2004).
Hyacinthaceae and its subfamilies (except Oziroeoideae),like many other plant lineages, show a disjunct distributionpattern. The Rand flora pattern is the best example of plant dis-junction between the flora of the Mediterranean region/western
Asia/north-west Africa and sub-Saharan Africa (Sanmartınet al., 2010). Vicariance and dispersal hypotheses have beenproposed to explain the origin of this disjunct distributionpattern. According to the first hypothesis, due to aridification(Sahara region), the widespread African flora underwentpartial extinction and created the current pockets ofdistribution of extant species. The dispersal hypothesis sug-gests long-distance dispersal among these regions, followedby local diversification. Two dispersal routes, southward andnorthward, have been proposed. The source area of the south-ward route is either the Mediterranean region or western Asiaand the dispersal is directed toward sub-Saharan Africa(Levyns, 1964), whereas the northward route is directedfrom sub-Saharan Africa to the Mediterranean region (Galleyet al., 2007).
The results of biogeographical histories of Hyacinthoideaeobtained by S-DIVA and BBM analyses are presented here.The aims of this study are to find the possible ancestralrange of Hyacinthoideae and to identify factors responsiblefor the current distribution pattern.
MATERIALS AND METHODS
Taxon sampling and outgroup selection
This analysis is based on material of subfamilyHyacinthoideae published in an earlier paper (Wetschniget al., 2007). The trnL-F region is composed of the trnL(UAA) intron and the intergenic spacer (IGS) between thetrnL (UAA)-3′ exon and the trnF (GAA) gene. In manygroups of plants, the intron region evolves more slowly thanthe spacer region (Gielly and Taberlet, 1994, 1996; Kitaet al., 1995; Gielly et al., 1996). The different evolving ratesof these regions are helpful in providing useful information;slowly evolving regions support the older divergences andquickly evolving regions provide resolution among closer rela-tives (McDade and Moody, 1999). In this study, we include 59taxa (58 ingroups and one outgroup). Voucher information forall plant accessions, geographical origin and EMBL databaseaccession numbers are provided in the Appendix. Oziroeacaulis is closely related to Hyacinthoideae and was selectedas the outgroup in this analysis. Nomenclature follows thatof the most recent nomenclatural synopsis available for a par-ticular group of taxa. In particular, we adopted the nomencla-ture of Speta (1998a, b) for tribe Hyacintheae of subfamilyHyacinthoideae, and that of Manning et al. (2004) for allother taxa, with the exception of the genera Ledebouria,Drimiopsis and Resnova, which have later been treated as sep-arate genera by Lebatha et al. (2006).
Phylogenetic analysis
Clustal X (Jeanmougin et al., 1998) was used for DNAsequence alignment with a pairwise multiple alignment param-eter. On average, ,1 % of data matrix cells were scored asmissing data and the region with ambiguous alignment wasexcluded in this analysis. Phylogenetic analysis using MPwas performed in PAUP version 4.0b10 (Swofford, 2002).MP analyses were performed either without or with successivecharacter weighting (rescaled consistency index) until tree
Ali et al. — Biogeography of HyacinthoideaePage 2 of 13
lengths remained the same in two successive rounds.Most-parsimonious trees were obtained by 1000 replicates ofrandom sequence addition using tree bisection-reconnection(TBR) branch swapping under the Fitch criterion (Fitch,1971). Confidence limits for the resulting tree topologieswere assessed by 10 000 fast bootstrap replicates(Felsenstein, 1985) and the jackknife algorithm (50 % dele-tion). The Bayesian analysis was conducted in MrBayes 3.1(Hulsenbeck and Ronquist, 2001; Ronquist and Hulsenbeck,2003) under the GTR + I + G model. MrModeltest version2.2 (Nylander, 2004) was used to select the best fit modelunder the Akaike information criterion. The Markov chainMonte Carlo chains were run simultaneously for 1000 000generations. Trees were sampled every 100 generations. Thefirst 1000 trees were eliminated (burn-in) and the remainingtrees were used to construct a 50 % majority rule consensustree with posterior probability (PP) distribution. One of thepost-burn trees was drawn using Mesquite software(Maddison and Maddison, 2010), shown in Fig. 1A. The treetopologies obtained by Bayesian and parsimony analyses aresimilar (no significant differences). The Bayesian tree withBayesian PP and parsimony bootstrap (BS) values is shownin Fig. 1A.
Dating the tree
The lack of a fossil record is a major constraint in theestimation of the ages of Hyacinthaceae and its subfamilies.However, we used the Bayesian analyses to date the treewith BEAST v1.6.1 (Drummond et al., 2002; Drummondand Rambaut, 2007) under the hypothesis of the molecularclock based on the general substitution rates of the plastidsequence (u ¼ 1.0 × 1029 s s21 year21; Zurawski et al.,1984). Ten million generations of the MCMC chains wererun, sampling every 1000 generations. Convergence of the sta-tionary distribution was checked by visual inspection ofplotted posterior estimates using the software Tracer v1.5(Rambaut and Drummond, 2007). After discarding the first1000 trees as burn-in, the samples were summarized in themaximum clade credibility tree using TreeAnnotator v1.6.1(Drummond and Rambaut, 2007) with the PP limit set to 0and summarizing mean node heights. The results were visua-lized using Figtree v1.3.1 (Rambaut, 2009).
Biogeographical analysis
The distribution range of Hyacinthoideae plus Oziroe wasdivided into eight areas, based on the presence of one ormore endemic species, as shown in Fig. 1C. These areas are:A (India), B (South America), C (Madagascar), D(sub-Saharan Africa), E (Mediterranean region), F (WesternAsia), G (Europe) and H (eastern Asia). In this analysis dueto a lack of samples from eastern Africa, we treatedsub-Saharan Africa as a single unit.
We used recently developed S-DIVA and BBM analysesimplemented in RASP to reconstruct the possible ancestralranges of subfamily Hyacinthoideae on the phylogenetictrees. In these methods, the frequencies of an ancestral rangeat a node in ancestral reconstructions are averaged over alltrees (Yan et al., 2010). To account for uncertainties in
phylogeny, we used 9000 trees from MCMC output and ranS-DIVA on all of them. The number of maximum areas waskept as 2. The possible ancestral ranges at each node on aselected tree were obtained. BBM analysis was also conductedin a similar way. The MCMC chains were run simultaneouslyfor 5000 000 generations. The state was sampled every 100generations. Fixed JC + G (Jukes-Cantor + Gamma) wereused for BBM analysis with null root distribution. Themaximum number of areas for this analysis was kept as 6. Theancestral ranges obtained by BBM analysis are shown in Fig. 2.
RESULTS
The aligned matrix consisted of 1613 characters, 282 of whichwere excluded from this analysis. Of the remaining 1331 char-acters, 1070 were constant, 119 were autapomorphic and 142were potentially parsimony-informative. The mean G + Ccontent was 33.22 %. The pairwise divergence estimate was0–6.18 %.
More than 1000 equally parsimonious trees had 418 steps,consistency index (CI) ¼ 0.72, retention index (RI) ¼ 0.86and rescaled consistency index (RC) ¼ 0.62. Withoutuninformative characters the parsimony trees had 290 steps,CI ¼ 0.60, RI ¼ 0.86 and RC ¼ 0.51.
PP and BS support for the majority of clades were .0.95and . 90 %, respectively, thus showing high support for thetree topology. The tree topology also reflects the classificationof subfamily Hyacinthoideae into a strictly northern hemi-sphere tribe Hyacintheae, a southern hemisphere tribeMassonieae and a monotypic sub-Saharan African tribePseudopropereae. Within the Hyacinthoideae clade, threesub-Saharan African, two Mediterranean, one southern hemi-sphere and one Eurasian subclade can be distinguished.
S-DIVA suggests a complex biogeographical history inwhich dispersal and vicariance have been vital in theshaping of the current distribution pattern in Hyacinthoideae.S-DIVA postulates 18 dispersals, the majority of which arelocated on the backbone of the tree. S-DIVA suggests two pos-sible ancestral ranges, D (sub-Saharan Africa) and DE(sub-Saharan Africa + Mediterranean region), for node 116and the occurrence of these ranges are 84.91 and 12.21 %,respectively (Fig. 1A). S-DIVA postulates that the ancestorsof Hyacinthoideae originated in sub-Saharan Africa (optimalarea reconstruction at basal node 116). This node suggestsan early dispersal to the Mediterranean region, as shown inFig. 3. The possible ancestral ranges at node 115 are DE andDH, the frequency of occurrence of these ranges being 82.81and 17.17 %, respectively, with 68 % Bayesian supportvalue. The most favoured ancestral range at node 115 is DE(sub-Saharan Africa + Mediterranean). A vicariance event isevident at this node, resulting in the Eurasian andsub-Saharan African lineages.
Node 83 represents members of tribe Hyacintheae, and thepossible ancestor range at this node is EH (Mediterranean +eastern Asia) with 100 % marginal probability. This node sug-gests a vicariance event. One descendant remained in easternAsia and another linage underwent in situ diversification inthe Mediterranean region. This in situ diversification resultedin two Mediterranean subclades. The ancestors of the node(82) of terminals 36–59 originated in the Mediterranean
Ali et al. — Biogeography of Hyacinthoideae Page 3 of 13
FI G. 1. Graphical output from S-DIVA (RASP). (A) Graphical results of ancestral distributions at each node of the phylogeny of subfamily Hyacinthoideaeobtained by S-DIVA. Alternative ancestral ranges of nodes 117, 116 and 115 (with frequency of occurrence) are shown in pie chart form. Bootstrap supportvalues (50 % and higher) and Bayesian credibility values (PP) are indicated above the pie chart on one of the post-burn Bayesian trees. (B) Colour key to possibleancestral ranges at different nodes; black with an asterisk represents other ancestral ranges. (C) Biogeographical regions: A, India; B, South America; C,
Madagascar; D, sub-Saharan Africa; E, Mediterranean; F, Western Asia; G, Europe; H, Eastern Asia.
Ali et al. — Biogeography of HyacinthoideaePage 4 of 13
region (E) with 100 % marginal probability (Fig. 1A);however, the Bayesian support value for this node is low(35 %). This is followed by a series of dispersals to Europeand western Asia. One dispersal event occurred from westernAsia to India. These dispersals resulted in a Eurasian subclade.
Node 114 of terminals 3–14 includes the taxa of tribeMassonieae. The ancestors of the node of terminals 3–14 ori-ginated in sub-Saharan Africa (D) with 100 % marginal prob-ability. The members of this tribe underwent local radiation insub-Saharan Africa. The ancestral area reconstruction at node100 suggests sub-Saharan Africa (D) + Madagascar (C) asancestral areas with 100 % support value; the probability ofthis result is 100 %. This probably indicates a trans-oceanic
dispersal to Madagascar, with the source area of this dispersalbeing sub-Saharan Africa.
Node 107 of terminals 11–14 has two possible ancestralranges, AD and CD. The most favoured ancestral range atthis node is AD (India + sub-Saharan Africa) with 83.45 %marginal probability, indicating a second event of transoceanicdispersal (Fig. 3). The ancestral reconstruction at the next nodeis AC (India + Madagascar), suggesting another transoceanicdispersal. S-DIVA suggests that no dispersal occurred fromsub-Saharan Africa to western Asia. Dispersals occurred towestern Asia from the Mediterranean region. Similarly, no dis-persal occurred from the Mediterranean region and westernAsia to sub-Saharan Africa.
FI G. 2. Graphical output from BBM analysis (exported from RASP). Graphical results of ancestral distributions at each node of the phylogeny of subfamilyHyacinthoideae obtained by BBM analysis. Pie charts at each node show probabilities of alternative ancestral ranges. Colour key to possible ancestral ranges
at different nodes; black with an asterisk represents other ancestral ranges.
Ali et al. — Biogeography of Hyacinthoideae Page 5 of 13
BBM analysis suggests slightly different ancestral ranges atbasal nodes (Fig. 2). Node 116 represents all members of sub-family Hyacinthoideae. BBM analysis postulates that theancestors of subfamily Hyacinthoideae originated in area D
(sub-Saharan Africa). The marginal probability for D is96.63 %. Similarly, at node 115, the ancestral reconstructionindicates that sub-Saharan Africa is the ancestral area of term-inals 14–35, with 95.06 % marginal probability. BBM
Radiation to Madagascar & IndiaRadiation to Eurasia
AF
C
H
D
C C
HA
F
G
E
D
B
HAF
G
E
D
BB
E
G
Radiation toMediterranean
V
G
EHF
A
C
DFirst majorextinction
B
I
II
IV
IIISecond majorextinction
Radiation to Eastern Asia
C
HAF
D
B
E
G
6162
116
117
6566
6768
6970
8586
8788
99
100
105106
107103
104108
101102109
110
111
9495
96
90
93
9192
97
98
89
112
113
11484
115
81
82
8363
60
FI G. 3. Major radiation and extinction events in subfamily Hyacinthoideae. Major radiations from southern Africa and the Mediterranean region are shown onthe blank world maps.
Ali et al. — Biogeography of HyacinthoideaePage 6 of 13
analysis suggests that the ancestors of Hyacinthoideae under-went in situ diversification in sub-Saharan Africa, as evidentfrom ancestral ranges at basal nodes.
The ancestral reconstruction at node 83 is ambiguous andsuggests four possible ancestral ranges, E, H, G and D. Theoccurrence of these ranges is: E, 29.00 %; H, 20.41 %; G,19.67 %; and D, 10.07 %. BBM analysis suggests three disper-sal events (internode leading to node 83) to eastern Asia, theMediterranean region and Europe. Dispersal to theMediterranean region occurred from sub-Saharan Africa. It isnot clear whether dispersal to Europe and eastern Asiaoccurred from sub-Saharan Africa or the Mediterraneanregion. This node also suggests a vicariance event and one des-cendant underwent in situ diversification in EG (Mediterraneanregion + Europe), followed by dispersal to western Asia andIndia.
The ancestral reconstruction at node 106 is ambiguous,suggesting a number of possible ancestral ranges. Threeranges, A (India), C (Madagascar) and D (sub-SaharanAfrica), had higher marginal probabilities of 32.43, 29.17and 28.63 %, respectively. This suggests two transoceanic dis-persals (Fig. 3).
DISCUSSION
Several biogeographical inferences can be made from this ana-lysis. S-DIVA suggests that the ancestors of Hyacinthoideaeoriginated in range D (sub-Saharan Africa, 84.91 %). Thiswas followed by an early dispersal to the Mediterraneanregion indicated by the ancestral ranges at node 115. Thefavoured ancestral range at node 115 is DE (82.81 %), andthe support value and this node also suggests a vicarianceevent between sub-Saharan Africa and the Mediterranean.Aridification of the Sahara region from the Miocene onwardcould explain this vicariance event, which resulted in thepartial extinction of the widespread African flora and the cre-ation of the current pockets of distribution of extant species. Asimilar vicariance pattern has been suggested withinAdenocarpus (Fabaceae) (see Sanmartın et al., 2010). Theage of this event based on dated tree material in Fig. 4 is17.92 Ma, consistent with the accelerated African aridificationin the early Miocene due to the uplift of the continent and theformation of the East African Rift Valley (Axelrod, 1972;Baker et al., 1972).
BBM analysis suggests that Hyacinthoideae originated insub-Saharan Africa (D) with marginal probability .96 %(node 116). Dispersal to the Mediterranean region andeastern Asia took place early in the history ofHyacinthoideae (nodes 115 and 83). A similar pattern ofsub-Saharan Africa origin and dispersal to the Mediterraneanregion has been suggested within Androcymbium(Colchicaceae) (del Hoyo et al., 2007; Sanmartın et al.,2010) and Senecio flavus (Coleman et al., 2003). The arrivalof members of Hyacinthaceae in the Mediterranean regionwould have been possible in the Oligocene/Miocene throughnorth-west Africa (Pfosser and Speta, 2004). The dated treein Fig. 4 suggests that Hyacinthoideae originated in the earlyMiocene (19 Ma) and arrived in the Mediterranean regionbetween 19 and 18 Ma. Further northward movement wasnot possible due to the large Tethys Ocean (Rogl, 1998,
1999) barrier. The formation of the Gomphotherium landbridge (19 Ma) allowed the free exchange of floras andfaunas between Africa and Eurasia (Rogl, 1998). The treedata in Fig. 4 suggests that dispersal to Eurasia took placeabout 15.3 Ma.
This single colonization from sub-Saharan Africa to theMediterranean region, followed by rapid diversification andmovements, resulted in the monophyletic Eurasian tribeHyacintheae (Pfosser et al., 2003; Wetschnig and Pfosser,2003). Pseudoprospero occupies an early branching positionin Hyacinthoideae in most of the trnL-F trees and is sister tothe rest of the subfamily.
Barnardia sinensis occupies the earliest branching positionin tribe Hyacintheae and suggests an early evolution of thisgenus. Its presence at an early diverging branch indicates thatits ancestor was among the first members to colonize theMediterranean region. Pfosser and Speta (1999) suggestedthat Barnardia was distributed from northern Africa toeastern Asia. Barnardia sinensis is found in Korea, Japan,China and Russia, whereas Barnardia numidica is distributedin northern Africa and the Balearic Islands. However, it isnow believed that B. numidica is not related to Barnardia(data not shown) and should be transferred to a genus ofits own.
S-DIVA suggests EH (Mediterranean + eastern Asia) as apossible ancestral range at node 83 with a 100 % marginalprobability, and the most favoured ancestral range at node115 is DE. Thus, S-DIVA suggests dispersal from theMediterranean region to eastern Asia. BBM analysis suggestsambiguous ancestral ranges at node 83, but the Mediterraneanis the most favoured ancestral range at this node. Node 83 alsosuggests a vicariance event between the Mediterranean andeastern Asia. Geological and climatic changes (aridificationand the uplift of Tibet) were instrumental in the extinctionof widespread flora and created the Mediterranean–easternAsia disjunct distribution pattern. The aridification of centralAsia and North China occurred between 22.0 and 6.2 Ma(Guo et al., 2002). The dated tree in Fig. 4 suggests that thisextinction event occurred about 13.74 Ma. A similarMediterranean–eastern Asia disjunct distribution pattern hasbeen suggested within Helleborus (Ranunculaceae) (Sunet al., 2001).
According to S-DIVA, one descendant underwent local radi-ation in the Mediterranean region, followed by a series of dis-persals to Europe (G), western Asia (F) and India (A). BBManalysis suggests an early dispersal to Europe. In situ diversi-fication took place in these areas and then dispersals occurredto western Asia and India. Only one dispersal event was direc-ted to India via western Asia. The Mediterranean region actedas a source area for these dispersals toward Europe and westernAsia in tribe Hyacintheae.
The node (114) of terminals 3–14 represents all members oftribe Massonieae. Both S-DIVA and BBM analysis suggest D(sub-Saharan Africa) as the ancestral range at this node, with100 and 99.05 % marginal probability, respectively. Thesub-Saharan African ancestors underwent local radiation andin situ diversification within sub-Saharan Africa. Three trans-oceanic dispersals occurred in Massonieae to Madagascarand India. Ledebouria nossibeensis (Madagascar) showsstrong affinity to L. hyacinthina from India and to members
Ali et al. — Biogeography of Hyacinthoideae Page 7 of 13
from the Arabian Peninsula, such as L. grandifolia fromSocotra. The monophyly of L. nossibeensis from the north ofMadagascar with L. hyacinthina from India is well supported(99/98 % bootstrap support and PP of 1.00).
BBM analysis suggests different ancestral ranges at nodes107 and 106. The ancestral reconstruction at node 107 suggestssub-Saharan Africa as the sole ancestor area. The most recentcommon ancestors of nodes 106 and 104 are distributed in
FI G. 4. Molecular clock based on the general substitution rates of the plastid sequence. Divergence age is shown below each node. Geological epoch is shownbelow the tree.
Ali et al. — Biogeography of HyacinthoideaePage 8 of 13
sub-Saharan Africa. Discussing multiple overseas dispersals inamphibians, Vences et al. (2003) mentioned that the importantpart of the Malagasy fauna was the result of dispersal fromAfrica. This dispersal was probably facilitated by currentlysubmerged islands via a stepping-stone mechanism (McCall,1997). Important examples of long-distance dispersalbetween Africa, Madagascar and the Seychelles are providedby multiple lineages of frogs (Vences et al., 2003, 2004), cha-meleons (Raxworthy et al., 2002), snakes (Nagy et al., 2003)and lemurs (Yoder and Yang, 2004). Slow climbing lorisesdistributed in Africa and Asia provide another strikingexample of dispersal between Africa and Asia (Masterset al., 2005). A number of recent studies have attempted toexplain the plant disjunction in Africa, Madagascar andAsia. The stepping-stone mechanism, birds capable of long-distance flight and monsoon trade winds coupled withoceanic currents are important tools of dispersal. Dispersalby a stepping-stone mechanism occurred through theSeychelles, Comoros and Chagos Archipelago betweenAfrica and Asia. Diaspore dispersal and successful speciationoccurred in both directions. Dispersal from Africa to Asia hasbeen suggested in Osbeckia (Melastomataceae) (Renner andMeyer, 2001; Renner, 2004), Gaertnera (Rubaceae)(Malcomber, 2002), Exacum (Gentianaceae; fromMadagascar to Asia) (Yuan et al., 2005), Cucumis (Renneret al., 2007) and tribe Sonerileae (Melastomataceae; fromAfrica to Madagascar and Asia) (Renner, 2004). Dispersalhas been suggested from Asia to Africa in Uvaria(Annonaceae) (Richardson et al., 2004), Bridelia(Phyllanthaceae) (Li et al., 2009), and Macaranga andMallotus (Euphorbiaceae) (Kulju et al., 2007).
The second route of dispersal was opened after the collision ofthe African and Eurasian plates. In the Miocene, the collision ofthe African and Eurasian plates was followed by a series ofpalaeogeographical reorganizations in the circum-Mediterranean region (Rogl, 1998; Scotese et al., 1988).Finally, a new dispersal route was established in the earlyPliocene (5 Ma) between Africa and south-western Asia viathe Arabian Peninsula and the Levant region (Thompson,2000; Fernandes et al., 2006) due to the closing of the RedSea to the Mediterranean. Extensive faunal exchange occurredthrough this route between Africa and Eurasia (Vrba, 1993;Cox and Moore, 2005; Nylander et al., 2008). The dispersalroute between Africa and Eurasia via the Arabian Peninsulaand the Levant region was used by the ancestors of currentCampanulaceae (Roquet et al., 2009) and other plants(Mummenhoff et al., 2001; Oberprieler, 2005; Inda et al.,2008; Mansion et al., 2008).
Birds are considered to be important tools of dispersal.Birds that can cross the 400-km Mozambique Channelinclude the Madagascan squacco heron, the Madagascancuckoo, the Madagascan pratincole, the broad-billed rollerand the Mascarene martin (Moreau, 1966; Renner, 2004).The first three species spend winters in eastern Africa andthe last one is a casual visitor (Moreau, 1966; Renner, 2004).
S-DIVA and BBM analyses suggest two independent trans-oceanic dispersals to Madagascar from the source area ofsub-Saharan Africa. According to S-DIVA reconstruction,African ancestors colonized the Mediterranean region (115),Madagascar (nodes 106 and 100) and India (node 107).
BBM analysis suggests that African ancestors could have colo-nized Eurasia (node 83), Madagascar and India (node 106).
S-DIVA suggests early dispersal to the Mediterraneanregion in Hyacinthoideae, followed by a vicariance event(due to aridification of the Sahara region) betweensub-Saharan Africa and the Mediterranean region, whichresulted in sub-Saharan African and the Mediterraneanlineages. A southward dispersal route is not plausible formembers of Hyacinthoideae because the results of S-DIVAand BBM analyses suggest that sub-Saharan Africa is theancestral area of the subfamily. Results also suggest an earlydispersal to the Mediterranean region, and thus the northwardroute of dispersal is plausible for members of the subfamily. Asimilar dispersal route was shown for Androcymbium(Colchicaceae) (Sanmartın et al., 2010). In the present study,no samples from eastern Africa were available; therefore, wetreated the region south of Sahara as a single block(sub-Saharan Africa). The absence of taxa from easternAfrica will surely have had impact on the results becausewithout representation from this area, a northward route of dis-persal would not be clarified. Sanmartın et al. (2010) suggestthat southern Africa has highest dispersal rates with easternAfrica, while eastern Africa has highest dispersal rates withnorth-west Africa (Macaronesia). Therefore, sub-SaharanAfrica was treated as a single block in this study, to understandthe northward dispersal scenario from southern Africa to theMediterranean region in the absence of taxa from the import-ant eastern African region. In their latest study onOrnithogaloideae, Martınez-Azorın et al. (2011) includedtaxa from eastern Africa, which nested within predominantlysouthern African taxa, probably suggesting dispersal fromsouthern Africa to eastern Africa. The formation of theeastern African mountains was instrumental in the migrationof some southern African lineages to eastern Africa via theGrand Rift and the Drakensberg mountains, which resultedin the eastern African endemic flora (Linder, 2005; Galleyet al., 2007; Sanmartın et al., 2010). No nuclear gene dataare available for this study; however, Martınez-Azorın et al.(2011) included the ITS region of nuclear ribosomal DNA intheir study of Ornithogaloideae, a closely related group toHyacinthoideae. They found the position of two clades weredifferent in the phylogenetic tree based on the ITS region com-pared with the combined tree. Whether we include or exclude anuclear region, sub-Saharan Africa is the ancestral area, butinclusion of this region will be helpful to explain some otherdispersal and vicariance scenarios.
ACKNOWLEDGEMENTS
We are grateful to the handling editor, Dr Michael F. Fay, andtwo anonymous reviewers for their valuable suggestions andconstructive criticisms. We thank John Munson for suggestedcorrections to the English text.
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