Received: 25 May 2018 | Revised: 30 March 2019 | Accepted: 2 April 2019 DOI: 10.1111/jbi.13592 RESEARCH PAPER The contribution of temperature and continental fragmentation to amphibian diversification Jonathan Rolland1 | Fabien L. Condamine2 1Department of Zoology, University of British Columbia, Vancouver, British Abstract Columbia, Canada Aim: Abiotic factors such as global temperature or continental fragmentation may 2 CNRS, UMR 5554, Institut des Sciences favour speciation through the ecological and geographical isolation of lineages, but de l'Evolution de Montpellier (Université de Montpellier), Montpellier, France macroevolutionary quantifications of such effect with both fossil and phylogenetic data are rarely performed. Here, we propose to use biogeographical estimations and Correspondence Jonathan Rolland, Department of Zoology, palaeo‐environmental diversification models to estimate whether and how palae‐ University of British Columbia, #4200‐6270 otemperature and the sequential break‐ups of Pangaea, Gondwana and Laurasia University Blvd., Vancouver, BC, Canada. Email: [email protected] have affected the diversification of amphibians through time. Location: Global. Funding information University of British Columbia, Grant/Award Methods: Using a time‐calibrated phylogeny for 3,309 amphibian species and a Number: 151042; Agence Nationale de la genus‐level fossil record, we estimated the diversification rates of the group with Recherche, Grant/Award Number: ANR‐10‐ LABX‐25‐01 birth–death models allowing rates to depend on the temporal variations of the envi‐ ronment. We used estimates of global palaeotemperature and an index of continental Editor: Richard Ree fragmentation through time to test the association between speciation and/or ex‐ tinction rates and past temperature and fragmentation. We also estimated the bio‐ geographical history based on a time‐stratified parametric model informed by the global palaeogeography. We inferred whether vicariance or dispersal events ex‐ plained the ancient and current geographical distribution of amphibians. Results: The diversification analyses on the whole amphibians showed that tempera‐ ture‐dependent models are better supported than tectonic‐dependent, time‐de‐ pendent and constant‐rate models for both the fossil and phylogenetic data. The best‐fitting temperature‐dependent model indicated a positive dependence of both speciation and extinction rates with the temperature through time. Biogeographical analyses indicated a Pangaean origin for amphibians and also showed that allopatric speciation (vicariance) explained important phases of the evolution of geographical ranges in the Mesozoic. Main conclusions: Our results support that palaeotemperatures have positively im‐ pacted amphibian diversification. Our study provides additional insights into how to quantify the effect of the landmass fragmentation on the diversification processes and shows with biogeographical reconstruction that continental fragmentation is linked to allopatric speciation in the early history of the clade. Jonathan Rolland and Fabien Condamine contributed equally to the study. Journal of Biogeography. 2019;1–17. wileyonlinelibrary.com/journal/jbi © 2019 John Wiley & Sons Ltd | 1 2 | ROLLAND and CONDAMINE KEYWORDS Anura, birth–death, Caudata, extinction, Gymnophiona, landmass fragmentation, macroevolution, plate tectonics, speciation 1 | INTRODUCTION linking explicitly the speciation rate with the number of landmasses through time has been addressed by some studies with fossil data Current species diversity has originated through the diversification and found mixed support for a link between diversification and con‐ process of ancestral lineages (Benton, 2015). The rates at which spe‐ tinental fragmentation through time (Jordan et al., 2016; Lehtonen cies originate and vanish have drastically varied through time and et al., 2017; Leprieur et al., 2016; Vavrek, 2016; Zaffos et al., 2017). across clades (Alfaro et al., 2009; Morlon, Parsons, & Plotkin, 2011; For example, Zaffos et al. (2017) found a positive correlation be‐ Rabosky, Slater, & Alfaro, 2012; Stadler, 2011). Explaining why di‐ tween global marine invertebrate generic richness and an inde‐ versification rates (speciation minus extinction) vary through time pendently derived quantitative index describing the fragmentation is a challenging task because many factors can alter the pace of of continental crust. On the contrary, Jordan et al. (2016) concluded speciation and extinction (Benton, 2009, 2015). Factors affecting that continental drift is not sufficient to account for the increase in the diversification of lineages are often placed in two categories: (a) terrestrial species richness observed in the fossil record. Tectonic the abiotic factors (Barnosky, 2001) and (b) the biotic factors (Van changes have also been examined recently by studies evaluating the Valen, 1973). Thanks to recent methodological developments, the effect of mountain orogeny on diversification using phylogenies of relative contribution of abiotic and biotic factors to the variation of plants (Lagomarsino et al., 2016; Pérez‐Escobar et al., 2017) and an‐ speciation and extinction rates has been assessed in various groups imals (Condamine et al., 2018; Xu, Kuntner, Liu, Chen, & Li, 2018). using fossil data (Ezard, Aze, Pearson, & Purvis, 2011; Lehtonen A second important abiotic factor likely playing an important role et al., 2017; Liow, Reitan, & Harnik, 2015; Roalson & Roberts, in species diversification is temperature. Previous palaeontological 2016; Silvestro, Antonelli, Salamin, & Quental, 2015) or phyloge‐ studies have already indicated that palaeotemperature had a posi‐ netic data (Condamine, Rolland, Höhna, Sperling, & Sanmartín, tive effect on biodiversity (Erwin, 2009; Ezard et al., 2011; Jaramillo, 2018; Condamine, Sperling, Wahlberg, Rasplus, & Kergoat, 2012; Rueda, & Mora, 2006; Mayhew, Bell, Benton, & McGowan, 2012). Lagomarsino, Condamine, Antonelli, Mulch, & Davis, 2016; Pérez‐ Temperature has been related to higher rate of speciation and lower Escobar et al., 2017). rate of extinction in plants (Jaramillo et al., 2006) and in macroper‐ Among the abiotic factors potentially impacting diversification, forate planktonic foraminifera (Ezard et al., 2011). The reasons why one can distinguish factors related to geography with the fragmenta‐ temperature should be related to diversification rates are still de‐ tion and the movements of landmasses (Valentine & Moores, 1970; bated. The metabolic theory proposes that temperature is associated Zaffos, Finnegan, & Peters, 2017), and factors related to climate and positively with faster rate of mutation, smaller generation time and palaeotemperature (Erwin, 2009; Hannisdal & Peters, 2011; Peters, ultimately higher speciation rate (Allen, Gillooly, Savage, & Brown, 2008). First, plate tectonics and continental fragmentation are likely 2006; Brown, Gillooly, Allen, Savage, & West, 2004). Hypotheses instrumental for understanding species diversification since evolu‐ related to the latitudinal diversity gradient have also proposed that tionary biologists often evidence the role of allopatric speciation warmer tropical regions have more stable climate through geolog‐ at small scales (Baselga, Recuero, Parra‐Olea, & Garcia‐Paris, 2011; ical scales, which might have considerably decreased the rates of Coyne & Orr, 2004; Funk, 1998), while biogeographers stress the extinction, comparatively to temperate regions at higher latitudes role of vicariance at large scales (Leprieur et al., 2016; Lomolino, (Dynesius & Jansson, 2000; Pianka, 1966; Rohde, 1992). Riddle, Whittaker, & Brown, 2010; Losos & Glor, 2003; Mao et al., Although the role of temperature has been already tested in 2012; Orr & Smith, 1998). The break‐up and isolation of landmasses several clades (Condamine, Rolland, & Morlon, 2013; Condamine might trigger the divergence of spatially isolated populations. A et al., 2018; Pyron & Wiens, 2013; Roalson & Roberts, 2016), the positive association between geographical fragmentation and net link between diversification and continental fragmentation remains diversification rates has already been proposed for global marine seldom tested empirically with birth–death models. Recent develop‐ biodiversity (Belanger et al., 2012; Jablonski & Bottjer, 1991; Peters, ments in the field of diversification models permit to assess the role 2005; Peters, Kelly, & Fraass, 2013; Valentine & Moores, 1970), for of variables that vary through time on the diversification processes mammalian lineages in the Late Cretaceous (100.5–66 million years (Condamine et al., 2013; Morlon et al., 2016). Given this progress, ago, Ma; Hedges, Parker, Sibley, & Kumar, 1996), and in Cupressaceae it is now possible to test whether the palaeotemperature and the (gymnosperms) during the break‐up of Pangaea (183–124 Ma; Mao number of landmasses have affected speciation and/or extinction et al., 2012). Despite a large number of biogeographical studies sug‐ through time in a given clade. To address this question, amphibi‐ gesting that continental fragmentation might impact diversification ans (frogs, salamanders and caecilians) are a relevant clade because (Cermeño, Benton, Paz, & Vérard, 2017; Hedges et al., 1996; Jordan, their relatively long evolutionary history (ca. 300–270 Ma; Feller & Barraclough, & Rosindell, 2016; Mao et al., 2012), the hypothesis Hedges, 1998; Feng et al., 2017; Pyron, 2014) has allowed long‐term ROLLAND and CONDAMINE | 3