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Biogeographic Analysis Reveals Ancient Continental Vicariance and Recent Oceanic Dispersal in Amphibians ∗ R Syst. Biol. 63(5):779–797, 2014 © The Author(s) 2014. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: [email protected] DOI:10.1093/sysbio/syu042 Advance Access publication June 19, 2014 Biogeographic Analysis Reveals Ancient Continental Vicariance and Recent Oceanic Dispersal in Amphibians ∗ R. ALEXANDER PYRON Department of Biological Sciences, The George Washington University, 2023 G Street NW, Washington, DC 20052, USA; ∗ Correspondence to be sent to: Department of Biological Sciences, The George Washington University, 2023 G Street NW, Washington, DC 20052, USA; E-mail: [email protected]. Received 13 February 2014; reviews returned 17 April 2014; accepted 13 June 2014 Downloaded from Associate Editor: Adrian Paterson Abstract.—Amphibia comprises over 7000 extant species distributed in almost every ecosystem on every continent except Antarctica. Most species also show high specificity for particular habitats, biomes, or climatic niches, seemingly rendering long-distance dispersal unlikely. Indeed, many lineages still seem to show the signature of their Pangaean origin, approximately 300 Ma later. To date, no study has attempted a large-scale historical-biogeographic analysis of the group to understand the distribution of extant lineages. Here, I use an updated chronogram containing 3309 species (~45% of http://sysbio.oxfordjournals.org/ extant diversity) to reconstruct their movement between 12 global ecoregions. I find that Pangaean origin and subsequent Laurasian and Gondwanan fragmentation explain a large proportion of patterns in the distribution of extant species. However, dispersal during the Cenozoic, likely across land bridges or short distances across oceans, has also exerted a strong influence. Finally, there are at least three strongly supported instances of long-distance oceanic dispersal between former Gondwanan landmasses during the Cenozoic. Extinction from intervening areas seems to be a strong factor in shaping present-day distributions. Dispersal and extinction from and between ecoregions are apparently tied to the evolution of extraordinarily adaptive expansion-oriented phenotypes that allow lineages to easily colonize new areas and diversify, or conversely, to extremely specialized phenotypes or heavily relictual climatic niches that result in strong geographic localization and limited diversification. [Amphibians; caecilians; dispersal; frogs; historical biogeography; oceanic dispersal; salamanders; vicariance.] at Gelman Library - George Washington University on August 18, 2014 Amphibians are one of the most diverse and are reduced due to niche conservatism (Wiens et al. conspicuous radiations of terrestrial vertebrates, with 2006; Pyron and Wiens 2013). However, the diversity over 7000 described species in most habitats on most of areas, habitats, and climates inhabited by modern continents (AmphibiaWeb 2014). Recent studies have amphibians indicates that dispersal must have occurred investigated historical patterns of diversification in a number of times (Buckley and Jetz 2007). the group (Roelants et al. 2007; Wiens 2007), as well One recent analysis (Pyron and Wiens 2013) used as the biogeographic distribution of species richness a dated tree containing approximately 41% of extant (Wiens et al. 2009; Pyron and Wiens 2013). Similarly, amphibians (2871 species), and estimated ancestral many recent studies have examined the complex areas using maximum likelihood (ML). However, biogeographic history of some broadly distributed the purpose of that study was simply to identify amphibian subgroups, such as toads (Pramuk et al. the earliest colonization of major ecoregions, not to 2008), hylid frogs (Smith et al. 2005), ranoid frogs describe the biogeographic history of amphibians or (Bossuyt et al. 2006), dendrobatid frogs (Santos estimate dispersal and vicariance patterns between et al. 2009), caecilians (Zhang and Wake 2009b), and ecoregions. Additionally, the effectiveness of traditional salamandrids (Weisrock et al. 2001; Zhang et al. 2008). ML methods for estimating ancestral areas is limited Other studies examined early biogeographic history, (Ree et al. 2005), as they make assumptions that do finding evidence for Gondwanan vicariance of major not comport with historical processes in biogeography lineages (Biju and Bossuyt 2003; Van Bocxlaer et al. 2006) (e.g., assuming that ranges can shift instantaneously). and a Pangaean origin of early amphibians (Roelants and Newer algorithms explicitly designed for biogeographic Bossuyt 2005; San Mauro et al. 2005). reconstruction now allow for processes such as dispersal, To date, no study has performed a comprehensive extinction, and cladogenesis (DEC) within and among evaluation of amphibian biogeography using a large- regions, increasing power to estimate ancestral areas scale phylogeny sampling all major geographic (Ree and Smith 2008). radiations in all major lineages, with explicit Recent authors have also pointed out that even these ancestral-area estimations. The biogeographic history DEC models are limited in terms of how biogeographic of amphibians is of particular interest due to the history can unfold (Matzke 2013b). Specifically, DEC potentially constrained nature of their movements and models disallow “founder-event” speciation, where dependence on homeostasis in local environments. a lineage newly colonizes one area from another Amphibians show remarkable stasis in ecological (such as an island). Under the DEC models, for niches, suggesting that intercontinental dispersal will range B to be colonized from range A, the range of have been historically constrained between similar the lineage must expand (via dispersal) to A + B. climatic zones (Wiens 2011a). Recent evidence suggests Allowing the ancestral area to be A alone with a that transitions between tropical and temperate areas “jump” colonization to B significantly increases both 779 [13:12 30/7/2014 Sysbio-syu042.tex] Page: 779 779–797 780 SYSTEMATIC BIOLOGY VOL. 63 numerical model-fit in many cases, and consilience seems to be related to specialization of both ecological with traditional biogeographic understanding (Matzke niches (where a restricted niche limits distribution 2012). Such processes are relatively common for other and increases extinction) and phenotypic adaptations terrestrial vertebrates, such as squamates (Raxworthy (where certain ecomorphologies are more or less suited et al. 2002; Vidal et al. 2008; Townsend et al. 2011). to dispersal and colonization). Both ecological and Contrastingly, many studies have assumed that long- evolutionary processes affecting speciation, extinction, distance over-water dispersal was essentially impossible and dispersal have had a strong impact over long periods for amphibians due to salt intolerance (Bossuyt and of time on the diversity and distribution of amphibians. Milinkovitch 2001; Wilkinson et al. 2002; Van Bocxlaer et al. 2006). However, recent evidence increasingly suggests a role for oceanic dispersal in explaining MATERIALS AND METHODS Downloaded from distributional patterns (Vences et al. 2003; de Queiroz 2005), which might be obscured by DEC models. Phylogeny These issues can be most directly addressed in The phylogeny used here is an update of a a large-scale phylogenetic framework using explicit previous tree and set of divergence times (Pyron and biogeographic analyses. Here, I present such an analysis, Wiens 2011; 2013), updated to incorporate additional http://sysbio.oxfordjournals.org/ based on a dated phylogeny containing 3309 species, recent sequence data. Most families, subfamilies, and approximately 47% of approximately 7000 extant genera are represented, notable exceptions being the amphibians. With data on the occurrence of these recently described Chikilidae (Kamei et al. 2012) species in 12 major global ecoregions, I use explicit and Odontobatrachidae (Barej et al. 2014). Following biogeographic methods to estimate ancestral areas the protocols detailed in recent supermatrix-based across the tree. Given a time scale for both amphibian studies (Pyron 2011, 2013; Pyron and Wiens 2011;I evolution and the motion of continents, I evaluate searched GenBank by family (stopping in February support for dispersal versus vicariant explanations for 2013), adding in sequence data for nine nuclear genes: the distribution of major lineages. Finally, I evaluate C–X–C chemokine receptor type 4 (CXCR4), histone the potentially under-appreciated role of extinction 3a (H3A), sodium–calcium exchanger (NCX1), pro- at Gelman Library - George Washington University on August 18, 2014 from intervening areas for explaining intercontinental opiomelanocortin (POMC), recombination-activating disjunctions (Chen et al. 2013), and founder-event gene 1 (RAG1), rhodopsin (RHOD), seventh-in-absentia speciation for explaining oceanic-dispersal patterns (SIA), solute-carrier family 8 (SLC8A3), and tyrosinase (Matzke 2013a). (TYR), and three mitochondrial genes: cytochrome The ancient origin of amphibians provides a classic b (cyt-b), and the large and small subunits of the null model; a vicariant-origin hypothesis for their mitochondrial ribosome genes (12S/16S; omitting the biogeographic distribution. Nearly all studies have adjacent tRNAs as they were difficult to align and placed the crown-group age of extant amphibians in the represented only a small amount of data). Carboniferous to Permian, between 359 and 252 Ma (San Unlike previous studies
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