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Evolutionary and Biogeographic Origins of High Tropical Diversity in Old World Frogs (Ranidae)

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Evolutionary and Biogeographic Origins of High Tropical Diversity in Old World Frogs (Ranidae) ORIGINAL ARTICLE doi:10.1111/j.1558-5646.2009.00610.x EVOLUTIONARY AND BIOGEOGRAPHIC ORIGINS OF HIGH TROPICAL DIVERSITY IN OLD WORLD FROGS (RANIDAE) John J. Wiens,1,2 Jeet Sukumaran,3 R. Alexander Pyron4 and Rafe M. Brown3 1Department of Ecology and Evolution, Stony Brook University, Stony Brook, New York 11794 2E-mail: [email protected] 3Natural History Museum, Biodiversity Research Center, Department of Ecology and Evolutionary Biology, University of Kansas, Dyche Hall, Lawrence, Kansas 66045-7561 4Department of Biology, The Graduate School and University Center, City University of New York, New York, New York 10016 Received May 24, 2008 Accepted November 17, 2008 Differences in species richness between regions are ultimately explained by patterns of speciation, extinction, and biogeographic dispersal. Yet, few studies have considered the role of all three processes in generating the high biodiversity of tropical regions. A recent study of a speciose group of predominately New World frogs (Hylidae) showed that their low diversity in temperate regions was associated with relatively recent colonization of these regions, rather than latitudinal differences in diversification rates (rates of speciation–extinction). Here, we perform parallel analyses on the most species-rich group of Old World frogs (Ranidae; ∼1300 species) to determine if similar processes drive the latitudinal diversity gradient. We estimate a time-calibrated phylogeny for 390 ranid species and use this phylogeny to analyze patterns of biogeography and diversification rates. As in hylids, we find a strong relationship between the timing of colonization of each region and its current diversity, with recent colonization of temperate regions from tropical regions. Diversification rates are similar in tropical and temperate clades, suggesting that neither accelerated tropical speciation rates nor greater temperate extinction rates explain high tropical diversity in this group. Instead, these results show the importance of historical biogeography in explaining high species richness in both the New World and Old World tropics. KEY WORDS: Amphibians, biogeography, phylogeny, speciation, species richness. Why are there more species in tropical regions than in temper- Special Issue of American Naturalist in 2007). For example, the ate regions? This question has perplexed evolutionary biologists latitudinal diversity gradient might arise because of higher rates and ecologists for hundreds of years, and dozens of hypotheses of speciation in the tropics, higher rates of extinction in the tem- have been proposed to answer it (e.g., Pianka 1966; Rosenzweig perate zone, or a tendency for groups that originate in the tropics 1995; Rahbek and Graves 2001; Willig et al. 2003; Mittelbach to disperse only recently and rarely to the temperate zone. et al. 2007). In recent years, there has been growing appreciation Surprisingly few studies have attempted to address the role for the idea that any reasonably complete explanation for the lat- of these processes in creating the latitudinal diversity gradi- itudinal diversity gradient must incorporate the three processes ent. For example, many ecological studies have sought corre- that directly change the number of species within and between lations between species richness and environmental variables regions: speciation, extinction, and biogeographic dispersal (e.g., (e.g., Francis and Currie 2003; Hawkins et al. 2003; Willig et al. Ricklefs 2004; Wiens and Donoghue 2004; Mittelbach et al. 2007; 2003; Buckley and Jetz 2007), without addressing any of these C 2009 The Author(s). Journal compilation C 2009 The Society for the Study of Evolution. 1217 Evolution 63-5: 1217–1231 JOHN J. WIENS ET AL. Hildebrandtia ornata Ptychadeninae Ptychadena subpunctata Ptychadena mascareniensis 96 50 Ptychadena pumilio Ptychadena cooperi 84 Ptychadena porosissima 60 88 Ptychadena aequiplicata 81 Ptychadena bibroni Ptychadena longirostris Ptychadena anchietae 86 Ptychadena oxyrhynchus 66 100 Ptychadena tellinii Phrynobatrachus sandersoni 98 Phrynobatrachus dendrobat Phrynobatrachinae Phrynobatrachus kreffti 82 Phrynobatrachus africanus 94 100 Phrynobatrachus auritus 96 Phrynobatrachus natalensis 100 Phrynobatrachus calcaratus 100 Phrynobatrachus dispar 98 Phrynobatrachus mababiens Conrauinae Conraua crassipes Conraua goliath 100 65 Conraua robusta Petropetidinae Petropedetes martiensseni 60 100 Petropedetes yakusini Petropedetes palmipes 100 100 Petropedetes newtoni 97 Petropedetes cameronensis 82 Petropedetes parkeri Aubria subsigillata Pyxicephalus adspersus Pyxicephalinae 99 Pyxicephalus adspersus 100 100 Pyxicephalus edulis 86 Anhydrophryne rattrayi Tomopterna natalensis Tomopterna tandyi 68 100 99 Tomopterna cryptotis 71 Tomopterna delalandii Natalobatrachus bonebergi 58 98 Arthroleptella bicolor 98 Arthroleptella villiersi Afrana fuscigula 57 96 Afrana angolensis 98 Amietia vertebralis Poyntonia paludicola Cacosternum boettgeri 88 100 Cacosternum platys Strongylopus grayii 100 Strongylopus bonaespei Micrixalinae 97 Strongylopus fasciatus Micrixalus fuscus 100 Micrixalus kottigharensis Ingerana tenasserimensis 100 Occidozyga borealis Occidozyga baluensis 100 Occidozyga laevis 100 97 Occidozyga lima 58 Occidozyga lima 54 Occidozyga martensii Nannophrys ceylonensis 100 Nannophrys marmorata Euphlyctis hexadactylus 88 61 Euphlyctis cyanophlyctis 100 Euphlyctis ehrenbergii 92 Hoplobatrachus occipitalis Hoplobatrachus crassus 63 Hoplobatrachus rugulosus 100 60 Hoplobatrachus tigerinus 96 Fejervarya cancrivora 96 Fejervarya vittigera Dicroglossinae Fejervarya orissaensis Fejervarya triora 87 Sphaerotheca breviceps Fejervarya brevipalmata 72 100 Fejervarya nilagirica Fejervarya rufescens 96 Fejervarya kirtisinghei 85 Fejervarya limnocharis 100 Fejervarya syhadrensis Paa shini Paa verrucospinosa Paa yei 92 Paa exilispinosa 98 Paa jiulongensis 64 Paa spinosa 91 Paa boulengeri 98 Paa robertingeri 96 Paa conaensis Chaparana quadranus Chaparana unculuana 58 Paa liui 99 Paa yunnanensis 100 Paa liebigii Nanorana ventripunctata 81 Nanorana parkeri 92 Nanorana pleskei 58 Paa medogensis Paa maculosa 70 64 90 Paa arnoldi 100 Paa chayuensis Limnonectes fragilis Limnonectes kuhlii 56 Limnonectes fujianensis 76 100 Limnonectes kuhlii Limnonectes kadarsani Limnonectes laticeps 89 Limnonectes limborgi 56 Limnonectes dabanus 58 86 Limnonectes gyldenstolpei Limnonectes sp Sulawesi 100 Limnonectes grunniens Limnonectes leporinus Limnonectes blythii 100 Limnonectes poilani Limnonectes malesianus 100 68 Limnonectes paramacrodon Limnonectes leytensis Limnonectes acanthi 100 Limnonectes arathooni 96 Limnonectes magnus Limnonectes heinrichi 80 68 Limnonectes modestus 66 Limnonectes woodworthi 86 Limnonectes macrocephalus 98 Limnonectes visayanus Ranixalinae Indirana leptodactyla Indirana sp 88 95 Indirana sp Indirana sp 100 Ingerana baluensis Ceratobrachinae Platymantis dorsalis 100 Platymantis naomiae 100 100 Platymantis hazelae 100 Platymantis montanus 100 Ceratobatrachus guentheri Batrachylodes vertebralis 100 Discodeles guppyi 78 Platymantis weberi Platymantis papuensis Nyctibatrachinae 100 100 Platymantis pelewensis Lankanectes corrugatus Nyctibatrachus aliciae 85 100 Nyctibatrachus major Boophis albilabris 100 Boophis tephraeomystax Mantellinae Boophis xerophilus 100 Aglyptodactylus madagasca 99 100 Laliostoma labrosum Mantella aurantiaca 71 100 Mantella nigricans Spinomantis peraccae 99 Mantidactylus femoralis 76 100 Mantidactylus ulcerosus Buergeria japonica 78 Buergeria buergeri 98 Buergeria oxycephalus 96 57 Buergeria robusta Nyctixalus pictus 100 Nyctixalus spinosus 98 Theloderma asperum 98 Philautus rhododiscus 94 98 Theloderma bicolor 72 Theloderma corticale Philautus ingeri Philautus aurifasciatus Rhacophorinae Philautus petersi Philautus mjobergi 86 68 Philautus acutirostris 100 Philautus surdus 98 Rhacophorus verrucosus 96 Kurixalus eiffingeri 100 Kurixalus idiootocus Philautus charius 96 Philautus griet 96 Philautus signatus 95 Philautus luteolus 100 Philautus neelanethrus 67 Philautus leucorhinus 75 100 Philautus wynaadensis 100 Philautus femoralis 52 Philautus microtympanum 54 Philautus schmarda Philautus gracilipes Chirixalus palpebralis SE Asia Chirixalus vittatus 69 Chirixalus doriae N Asia 100 Chiromantis rufescens 98 Chiromantis xerampelina S Asia Polypedates eques 100 Polypedates fastigo Polypedates otilophus Australasia 96 Polypedates colletti Polypedates cruciger Europe 86 68 Polypedates maculatus 74 Polypedates megacephalus 100 Polypedates leucomystax Africa 100 Polypedates mutus Rhacophorus monticola Madagascar Rhacophorus dulitensis Rhacophorus dennysi N America 91 Rhacophorus moltrechti Rhacophorus arboreus Rhacophorus schlegelii M America Rhacophorus lateralis Rhacophorus pardalis Polypedates pleurostictus S America Rhacophorus angulirostris 98 Rhacophorus gauni ambiguous Rhacophorus calcaneus Raninae 98 Rhacophorus orlovi 88 Rhacophorus malabaricus Rhacophorus nigropalmatus 98 Rhacophorus rhodopus 76 Rhacophorus annamensis 71 Rhacophorus bipunctatus 98 Rhacophorus reinwardtii 100 80 60 40 20 Millions of years ago 1218 EVOLUTION MAY 2009 LATITUDINAL DIVERSITY IN FROGS processes. Even though climatic variation almost certainly plays were not. Specifically, they found that the low species richness of an essential role in generating the latitudinal diversity gradient, hylids in temperate North America, Europe, and Asia was seem- climatic variables do not directly change the number of species ingly explained by their relatively recent dispersal
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