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Genus Lycodon) Zoologica Scripta Multilocus phylogeny reveals unexpected diversification patterns in Asian wolf snakes (genus Lycodon) CAMERON D. SILER,CARL H. OLIVEROS,ANSSI SANTANEN &RAFE M. BROWN Submitted: 6 September 2012 Siler, C. D., Oliveros, C. H., Santanen, A., Brown, R. M. (2013). Multilocus phylogeny Accepted: 8 December 2012 reveals unexpected diversification patterns in Asian wolf snakes (genus Lycodon). —Zoologica doi:10.1111/zsc.12007 Scripta, 42, 262–277. The diverse group of Asian wolf snakes of the genus Lycodon represents one of many poorly understood radiations of advanced snakes in the superfamily Colubroidea. Outside of three species having previously been represented in higher-level phylogenetic analyses, nothing is known of the relationships among species in this unique, moderately diverse, group. The genus occurs widely from central to Southeast Asia, and contains both widespread species to forms that are endemic to small islands. One-third of the diversity is found in the Philippine archipelago. Both morphological similarity and highly variable diagnostic characters have contributed to confusion over species-level diversity. Additionally, the placement of the genus among genera in the subfamily Colubrinae remains uncertain, although previous studies have supported a close relationship with the genus Dinodon. In this study, we provide the first estimate of phylogenetic relationships within the genus Lycodon using a new multi- locus data set. We provide statistical tests of monophyly based on biogeographic, morpho- logical and taxonomic hypotheses. With few exceptions, we are able to reject many of these hypotheses, indicating a need for taxonomic revisions and a reconsideration of the group's biogeography. Mapping of color patterns on our preferred phylogenetic tree suggests that banded and blotched types have evolved on multiple occasions in the history of the genus, whereas the solid-color (and possibly speckled) morphotype color patterns evolved only once. Our results reveal that the colubrid genus Dinodon is nested within Lycodon—a clear finding that necessitates the placing of the former genus in synonymy with the latter. Corresponding author: Cameron D. Siler, Department of Biology, University of South Dakota, Vermillion, SD 57069, USA. E-mail: [email protected] Carl H. Oliveros, Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, 66045-7561, USA. E-mail: [email protected] Anssi Santanen, Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, 66045-7561, USA. E-mail: [email protected] Rafe M. Brown, Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, 66045-7561, USA. E-mail: [email protected] Introduction be monophyletic based on both morphological (Rieppel The superfamily Colubroidea (sensu Pyron et al. 2011), or 1988; Zaher 1999; Lee & Scanlon 2002) and molecular advanced snakes, represents one of the most strikingly data (Cadle 1988; Heise et al. 1995; Kraus & Brown 1998; diverse terrestrial radiations of living vertebrates (Lawson Gravlund 2001; Slowinski & Lawson 2002, 2005; Wilcox et al. 2005; Burbrink & Pyron 2008; Pyron et al. 2011). et al. 2002; Lawson et al. 2005; Pyron et al. 2011). Over Currently, more than 2500 species are recognized (Lawson the last decade, numerous studies have investigated rela- et al. 2005; Pyron et al. 2011) in this relatively young clade tionships among advanced snakes within the superfamily dating only to the Cenozoic (Burbrink & Pyron 2008; Colubroidea with widely varying degrees of taxonomic Vidal et al. 2009). Seven families of snakes are considered inclusion (Lawson et al. 2005; Burbrink & Pyron 2008; members of the clade (Colubridae, Elapidae, Homalopsi- Wiens et al. 2008; Kelly et al. 2009; Vidal et al. 2009; dae, Lamprophiidae, Pareatidae, Viperidae and Xenoder- Zaher et al. 2009; Pyron et al. 2011). To date, the superm- matidae; Pyron et al. 2011), which has been determined to atrix of Pyron et al. (2011) has been by far the most 262 ª 2013 The Norwegian Academy of Science and Letters, 42, 3, May 2012, pp 262–277 C. D. Siler et al. Multilocus phylogeny of Asian wolf snakes extensive of these studies, including 761 species represent- morphological data, sufficient genetic sampling has recently ing 299 genera (29% of the global species diversity of been amassed to allow for an initial molecular appraisal of advanced snakes). the genus’ phylogenetic relationships and affinities to other The computational obstacles involved in estimating phy- SE Asian genera. The geographic ranges of species in the logenies for this and other highly diverse radiations are genus Lycodon fall along a divergent spectrum, from substantial; moreover, when combined with the absence of widespread species whose range spans nearly the entire dis- available genetic samples for a large number of recognized tribution of the genus (i.e., L. aulicus) to a number of species, we likely are far from a complete understanding range-restricted, microendemic lineages (i.e., L. alcalai, of species-level relationships within advanced snakes. L. bibonius, L. chrysoprateros, L. fausti, L. ferroni, L. solivagus, Despite the relative success of new approaches and meth- L. tesselatus). Coloration varies greatly across this unique odologies to employing supermatrices in phylogenetic group of snakes; however, most species can be grouped studies of species-rich groups (Sanderson et al. 2003; into one of four distinct colour pattern categories: banded, Driskell et al. 2004; Philippe et al. 2004; Wiens et al. blotched, solid and speckled (Fig. 2). Variation in colour 2005; de Queiroz & Gatesy 2007; Thomson & Shaffer patterns among species representing each of these 2010; Pyron et al. 2011), there is still a clear need for con- morphotypes has consistently led to confusion over species tinued research aimed at filling many of the gaps in taxo- boundaries (Lanza 1999). nomic coverage and resolving more fine-scale relationships Nearly one-third of the diversity within the genus occurs among the many poorly understood genera within Colu- in the Philippines, with nine of the 11 species now consid- broidea. A characteristic example of one of these enig- ered endemic to this island archipelago (Lanza 1999; Gau- matic genera is the Wolf Snakes of the genus Lycodon lke 2002). Faunal demarcations in the archipelago have within the subfamily Colubrinae (family Colubridae). traditionally been explained by the geography of Pleisto- Although this radiation of non-venomous Asian snakes is cene aggregate island complexes (PAICs: Brown & Dies- only moderately diverse (36 currently recognized species; mos 2002, 2009; Heaney 1985; Heaney et al. 1998, 2005; The Reptile Database 2012), only three species have ever Siler et al. 2010, 2012b). During glacial periods, adjacent been included in phylogenetic studies (L. capucinus, L. lao- islands separated by shallow waters experienced greater ensis, and L. zawi; Heise et al. 1995; Kraus & Brown 1998; connectivity as decreased sea levels (100–140 m below cur- Lawson et al. 2005; Kelly et al. 2003, 2009; Pyron et al. rent levels) resulted in increased land-positive regions. The 2011). Among the studies that have included representa- cyclical nature of this process has provided an explanatory tives of Lycodon, the genus has been consistently recovered tool for explaining the distribution of biotic diversity in the as the sister species to the genus Dinodon with moderate Philippines. Although recent studies have resulted in mixed support (Kelly et al. 2003, 2009; Lawson et al. 2005; Pyron support for the PAIC model of diversification (review: Siler et al. 2011). When wider taxonomic sampling has been et al. 2010, 2012b), this model remains a heuristic tool for included in phylogenetic analyses, the genera Lycodon and exploring and understanding many of the evolutionary pro- Dinodon are recovered as members of a larger clade that cesses underlying the accumulation of biodiversity in the includes the colubrid genera Boiga, Dasypeltis, Dipsadoboa, Philippines. Crotaphopeltis, and Telescopus, albeit with weak support In this study, we investigate the patterns of diversifica- (Kelly et al. 2003, 2009; Lawson et al. 2005; Pyron et al. tion among species of Lycodon from a phylogenetic perspec- 2011). tive, providing the first estimate of genealogical In just the last two decades, 14 new species of snakes of relationships for this unique radiation of Asian snakes. the genus Lycodon have been described, increasing the First, we attempt to estimate the phylogenetic position of known diversity of this Indian and Southeast Asian colubrid Lycodon among recognized, closely related colubrid snakes genus by nearly 40% (Ota & Ross 1994; Lanza 1999; to provide insight into patterns of morphological evolution Slowinski et al. 2001; Daltry & Wüster 2002; Gaulke 2002; and regional diversification. Second, we provide a first Mukherjee & Bhupathy 2007; Vogel et al. 2009; Vogel & assessment of the evolution of major colour patterns in Lyc- David 2010; Vogel & Luo 2011; Zhang et al. 2011; Vogel odon. Finally, we test the following suite of biogeographic, et al. 2012). The 36 recognized species of Lycodon occur morphological and taxonomic hypotheses aimed at better throughout central to Southeast Asia, from regions east of understanding how diversity is partitioned among Wolf the Caspian Sea, eastern Iran and India to southern China, Snakes. Here, we address three general questions: (i) Are the Indo-Australian Archipelago, the Ryukyu
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