Using phylogenomics to understand the link between biogeographic origins and regional diversification in ratsnakes
Graphical abstract
Introduction
Exploring the spatial and temporal modes of diversification as well as the factors influencing their patterns is critical for understanding the processes leading to biodiversity accumulation (Fritz et al., 2013). For species-rich assemblages with a global distribution, diversification is expected to be influenced by several mechanisms involving both biotic and abiotic factors (Moore and Donoghue, 2007). Adaptive radiation, defined as rapid diversification of descendants from a common ancestor into distinct environments, is considered one of the main mechanisms shaping biodiversity on earth (Simpson, 1953, Schluter, 2000). Ecological opportunity generated by the appearance of new resources, the mass extinction of competitors, or the colonization of new areas has typically been the prime motivator for adaptive radiation (Losos, 2010, Yoder et al., 2010). Adaptive radiation via ecological opportunity predicts diversity-dependent diversification, in which speciation rates are initially rapid, filling abundant unoccupied niches and declining as available niches become saturated (Schluter, 2000, Losos, 2010). Furthermore, enhanced diversification rates should be found only in diverse taxa experiencing adaptive radiation when compared to other groups not showing heightened diversity (Glor, 2010).
Inferring diversification processes requires a comprehensive phylogeny that incorporates clade age and biogeographic information (Moore and Donoghue, 2007). Using divergence-time estimation and ancestral area reconstruction, while considering events such as dispersal, geographic isolation and mass extinction, provide a context for understanding how diversification rates change across temporal and geographic dimensions. For example, Anolis lizards are an important case where dispersal to new areas accelerated diversification by colonizing the abundant open niches of the West Indies, permitting a set of ecomorphs to evolve repeatedly on distinct islands that share similar environmental conditions (Harmon et al., 2003, Losos, 2009).
However, just because regions were free from competitors when colonized does not guarantee that rates of speciation were elevated early in the history of a particular group. For instance, a signature of rapid early radiation was not found in Caribbean alsophiine snakes despite colonizing unoccupied regions that share a similar distribution and ecological opportunity with the Anolis lizards (Burbrink et al., 2012). Explanations for the lack of elevated diversification in alsophiines involve the young age of this group (they may not have had sufficient time to show a reduction in speciation rates), and waiting time between island colonization (offsetting early bursts of speciation; Burbrink et al., 2012). Therefore, it is important to properly estimate divergence time, ancestral area, and species diversification so that a comprehensive view of biodiversity accumulation is properly assessed.
While many examples of diversification and adaptive radiation have occurred in geographically more controlled areas such as islands, several continentally distributed examples are relevant as well. The ratsnakes (Coronellini), which historically have been used for systematics, ecological, behavioral, and physiological research (Boulenger, 1894, Underwood, 1967, Lawson and Dessauer, 1981, Schulz, 1996, Schulz and Gumprecht, 2013), are important examples of continental-level adaptive radiation, given their rapid diversification into unique ecological niches in biogeographically distinct regions. The ratsnakes, composed of 88 species (Table S1; Uetz, 2014), are widely distributed throughout the Palearctic, northern part of the Oriental, the Nearctic and portions of the Neotropical Zoogeographic regions (Fig. 1). Given their global distribution, ratsnakes occupy very heterogeneous habitats, including mountain forests, grassland, deserts, and tropical rain and dry forests (Schulz, 1996), which likely provided ecological opportunity for rapid divergence within this group. Unlike many other ectothermic animals, ratsnakes have attained their highest diversity in both the Old World (OW) and the New World (NW) temperate regions.
Previous biogeographic studies supported a tropical Asian origin of ratsnakes with dispersal to OW temperate regions and subsequent Beringial dispersal to the NW (Burbrink and Lawson, 2007, Burbrink and Pyron, 2010, Chen et al., 2013). This Cenozoic Beringian Dispersal Hypothesis (CBDH; Guo et al., 2012) is supported in several squamate groups as well as various plant and other animal groups. This unidirectional dispersal was likely important in shaping temperate Eurasian and North American faunas and floras (Enghoff, 1995, Wen, 1999, Smith et al., 2005, Burbrink and Lawson, 2007, Brandley et al., 2011). Importantly, diversification of the NW clade of ratsnakes, Lampropeltini, occurred rapidly upon arrival in the Americas (Burbrink and Lawson, 2007, Burbrink and Pyron, 2010). However, under similar environmental conditions, it is possible that the rapid bursts of diversification in the NW lineages were an extension of broadly rapid Holarctic diversification and not a phenomenon isolated to the Americas. Alternatively, after divergence between OW and NW clades, these lineages may have diversified uniquely in terms of tempo and trajectory of species accumulation in their respective regions. Nevertheless, neither of these hypotheses was tested in a biogeographical context where rates of diversification were examined across the phylogeny of ratsnakes while at the same time considering region of origin.
We use the Anchored phylogenomics platform to sample and sequence hundreds of loci across the entire ratsnake genome (Lemmon et al., 2012) to infer a dated species tree using coalescent-model based methods to overcome potential gene-tree/species-tree conflicts from incomplete-lineage sorting (Pamilo and Nei, 1988, Maddison, 1997, Page and Charleston, 1997, Slowinski et al., 1997, Slowinski and Page, 1999, Edwards, 2009). This represents the first attempt to infer phylogeny using genomic data across most species and all 20 genera of ratsnakes (Utiger et al., 2002, Utiger et al., 2005, Burbrink and Lawson, 2007). Specifically, with this dated tree we examine monophyly of all genera and tribes (Coronellini and Lampropeltini) and estimate ancestral area and dispersal probabilities to test the CBDH, previously examined only using 2 loci (Burbrink and Lawson, 2007). With phylogenomic estimates, we examine species diversification as the interaction between speciation and extinction for understanding the buildup of biodiversity (Ricklefs, 2007, Morlon et al., 2010, Pyron and Burbrink, 2013). With clade age, diversity, branch length, and topology available, we use time- and taxon-dependent models to examine speciation and extinction rate changes to understand the potential factors influencing diversification patterns (Rabosky and Lovette, 2008a, Rabosky and Lovette, 2008b, Morlon et al., 2010, Morlon et al., 2011, Etienne et al., 2011, Stadler, 2011). Finally, linking diversification back to biogeography, we determine if diversification processes are heterogeneous across different lineages (Alfaro et al., 2009, Rabosky, 2014) and test correlation between diversification changes and geographic regions. Ultimately, investigating the tempo and mode of diversification, we find that (a) the radiation of the entire ratsnake group shows a diversity-dependent pattern of diversification, and (b) speciation rate- heterogeneity is prominent within the NW subclade. We discuss potential alternative scenarios that link diversification variation and the inter-continental colonization event.
Section snippets
DNA sample preparation
We collected tissue or DNA samples from 79 ratsnake species (91% of 88 putative members of this clade) as well as 9 outgroups (7 taxa representing main clades in Colubrinae and 2 non-colubrine species; Table S1). This includes all OW genera of ratsnakes, Archelaphe, Coronella, Elaphe, Euprepiophis, Oocatochus, Oreocryptophis, Rhinechis, Zamenis, Gonyosoma and Coelognathus, and New World genera, Arizona, Bogertophis, Cemophora, Lampropelits, Pantherophis, Pituophis, Pseudelaphe, Rhinocheilus and
Gene-tree comparisons and species-tree inference
We obtained 304 loci (total length: 452,698 bp; mean length: 1489 bp/locus) for tree inference. The BLAST results showed that 97% of the loci matched to known genes, particularly from the Python bivittatus genome (Castoe et al., 2011; Table S3). The best-fit substitution model for 58% of the loci was HKY, including either gamma or the invariable sites parameter or both (Table S3).
The gene-tree distance distributions show that the among-loci distance of PP trees sets were smaller than the
Biogeography
Ancestral area reconstruction showed that the ratsnakes (Coronellini) originated in the Eastern Palearctic and subsequently dispersed to the Western Palearctic and likely crossed Beringia into Nearctic (Fig. 5). This result supports the CBDH, which indicates that OW taxa seeded the diversification of ratsnakes in the NW. All extant colubroid snake groups occurring in the NW, originated in the OW and dispersed to the Americas during the Oligocene or Miocene (Chen et al., 2014a, Chen et al., 2014b
Acknowledgments
We would like to thank the following for providing tissues, specimens and support for this study: American Museum of Natural History (D. Frost, C. Raxworthy, D. Kizirian, J. Feinstein, R. Pascocello) Louisiana State University Museum of Natural Sciences (J. Boundy, D. Dittman, R. Brumfeld, F. Sheldon), Museum of Vertebrate Zoology (J. McGuire, C. Spencer), Smithsonian Institution National Museum of Natural History (A. Wynn, J. Jacobs), California Academy of Sciences (J. Vindum, D. Blackburn, R.
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