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Cyrtodactylus) Reveals a West to East Pattern of Diversification ⇑ Perry L

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Cyrtodactylus) Reveals a West to East Pattern of Diversification ⇑ Perry L Molecular Phylogenetics and Evolution 65 (2012) 992–1003 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeny of bent-toed geckos (Cyrtodactylus) reveals a west to east pattern of diversification ⇑ Perry L. Wood Jr. 1, Matthew P. Heinicke , Todd R. Jackman, Aaron M. Bauer Department of Biology, 147 Mendel Hall, Villanova University, 800 Lancaster Ave., Villanova, PA 19085, USA article info abstract Article history: The Asian/Pacific genus Cyrtodactylus is the most diverse and among the most widely distributed genera Received 7 May 2012 of geckos, and more species are continually being discovered. Major patterns in the evolutionary history Revised 24 August 2012 of Cyrtodactylus have remained largely unknown because no published study has broadly sampled across Accepted 27 August 2012 the geographic range and morphological diversity of the genus. We assembled a data set including Available online 13 September 2012 sequences from one mitochondrial and three nuclear loci for 68 Cyrtodactylus and 20 other gekkotan spe- cies to infer phylogenetic relationships within the genus and identify major biogeographic patterns. Our Keywords: results indicate that Cyrtodactylus is monophyletic, but only if the Indian/Sri Lankan species sometimes Sundaland recognized as Geckoella are included. Basal divergences divide Cyrtodactylus into three well-supported Indonesia Biogeography groups: the single species C. tibetanus, a clade of Myanmar/southern Himalayan species, and a large clade Dispersal including all other Cyrtodactylus plus Geckoella. Within the largest major clade are several well-supported Myanmar subclades, with separate subclades being most diverse in Thailand, Eastern Indochina, the Sunda region, Papuan region the Papuan region, and the Philippines, respectively. The phylogenetic results, along with molecular clock and ancestral area analyses, show Cyrtodactylus to have originated in the circum-Himalayan region just after the Cretaceous/Paleogene boundary, with a generally west to east pattern of colonization and diver- sification progressing through the Cenozoic. Wallacean species are derived from within a Sundaland radi- ation, the Philippines were colonized from Borneo, and Australia was colonized twice, once via New Guinea and once via the Lesser Sundas. Overall, these results are consistent with past suggestions of a Palearctic origin for Cyrtodactylus, and highlight the key role of geography in diversification of the genus. Ó 2012 Elsevier Inc. All rights reserved. 1. Introduction 2009, 2010a, 2010b); and Wallacea, Australia, and New Guinea (Kraus, 2008; Oliver et al., 2011; Shea et al., 2012). Cyrtodactylus Gray, 1827 (bent-toed geckos), with more than Despite great activity in terms of alpha systematic studies, phy- 150 recognized species, is by far the most species-rich genus of logenetic research on Cyrtodactylus has been relatively limited thus gekkotan lizards (Uetz, 2012). Recently, as many as 19 new species far. Regional phylogenies with reasonably broad taxon sampling have been described in a given year from throughout the group’s have been generated for the bent-toed geckos of the Philippines broad range in Asia and the western Pacific (Fig. 1), and since the (Siler et al., 2010; Welton et al., 2010a, 2010b), Australia and Mel- start of the 21st century, known diversity of Cyrtodactylus has more anesia (Shea et al., 2012), and for some Malay Peninsula and than doubled. Virtually all regions occupied by Cyrtodactylus have Sundaland Cyrtodactylus (Grismer et al., 2010). Monophyly and seen a huge increase in the number of recognized species de- interrelationships of the bent-toed geckos of these and other geo- scribed, including Myanmar (Bauer, 2002, 2003; Mahony, 2009), graphic regions has yet to be established. Indeed, the composition Vietnam, (Ngo, 2008; Ngo and Bauer, 2008; Nguyen et al., 2006), of Cyrtodactylus as a whole remains unclear, especially with respect Sundaland (Chan and Norhayati, 2010; Grismer et al., 2010; Iskan- to certain taxa in Nepal, northern India, and Tibet, which have been dar et al., 2011; Oliver et al., 2009), the Philippines (Welton et al., variously assigned to Cyrtodactylus, Cyrtopodion, Altigekko, Altiphy- lax, Indogekko, and Siwaligekko (see Krysko et al. (2007) for a recent ⇑ Corresponding author. Present address: Department of Natural Sciences, review). In addition, the status of Geckoella, a presumably University of Michigan-Dearborn, 125 Science Building, 4901 Evergreen Road, monophyletic group of small, ground-dwelling bent-toed geckos Dearborn, Michigan 48128, USA. (regarded as either a genus or a subgenus of Cyrtodactylus; Kluge, E-mail addresses: [email protected] (P.L. Wood Jr.), heinicke@umd. 2001; Bauer, 2002) remains uncertain. umich.edu (M.P. Heinicke), [email protected] (T.R. Jackman), aaron. A practical problem engendered by the lack of broader scale [email protected] (A.M. Bauer). phylogenetic resolution in Cyrtodactylus is that each newly de- 1 Present address: Department of Biology, Brigham Young University, Provo, UT 84602, USA. scribed species must be diagnosed relative to all of its congeners, 1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2012.08.025 P.L. Wood Jr. et al. / Molecular Phylogenetics and Evolution 65 (2012) 992–1003 993 Fig. 1. Global distribution of Cyrtodactylus, with place names mentioned in the text listed. or the assumption must be made that geographically coherent and themselves or photographic vouchers were examined by one or morphologically similar species are monophyletic. While this ap- more authors but in some cases we were dependent on the species pears to be the case in some instances, it is likely that not all such identifications of collectors or other institutions. Given the rapid groups are natural, and without broad sampling monophyly cannot rate of description of Cyrtodactylus spp. and the break-up of ‘‘spe- be conclusively demonstrated even for regional clades that do ap- cies’’ previously believed to be widespread (e.g. Johnson et al., pear monophyletic (e.g., Philippines: Siler et al., 2010; Welton 2012), it is possible that some identifications may need subsequent et al., 2010a, 2010b; Queensland: Shea et al., 2012). A phylogeny revision, however, all may be considered accurate to at least spe- spanning the geographic distribution and morphological variation cies group. Genomic DNA was extracted from tissue samples using of Cyrtodactylus and having sufficient sampling to provide a ‘‘back- Qiagen DNeasy™ tissue kits under manufacturers’ protocols. All bone’’ for the genus would make a major contribution in providing genes were amplified using a double-stranded Polymerase Chain a preliminary estimate of the monophyly of as yet unevaluated Reaction (PCR). Included in the reaction were 2.5 ll genomic presumptive clades. In addition, such a phylogeny can provide DNA, 2.5 ll light strand primer 2.5 ll heavy strand primer, 2.5 ll information about relevant outgroups for future regional Cyrto- dinucleotide pairs, 2.5 ll5Â buffer, MgCl 10Â buffer, 0.18 ll Taq dactylus phylogenies, allow evaluation of the generic allocation of polymerase, and 9.82 llH2O, using primers listed in Table 2. PCR the problematic taxa that have been variously assigned to Cyrto- reactions were executed on an Eppendorf Mastercycler gradient dactylus or other genera, and provide a framework for comparative theromocycler under the following conditions: initial denaturation analyses of Cyrtodactylus biology, including biogeography and mor- at 95 °C for 2 min, followed by a second denaturation at 95 °C for phological evolution. To this end we used nucleotide sequence data 35 s, annealing at 50–55 °C for 35 s, followed by a cycle extension from approximately 45% of recognized bent-toed gecko species, at 72 °C for 35 s, for 34 cycles. All PCR products were visualized via including exemplars encompassing the morphological range of 1.5% agarose gel electrophoresis. Successful PCR amplifications variation and from across the geographic range of Cyrtodactylus, were purified using AMPure magnetic bead solution (Agencourt to erect such a backbone phylogeny for the genus. We use this data Bioscience). Purified PCR products were sequenced using Applied set to evaluate current taxonomy and make preliminary observa- Biosystems BigDye™ Terminator v3.1 Cycle Sequencing ready tions of Cyrtodactylus historical biogeography. reaction kit or DYEnamic™ ET Dye Terminator kit (GE Healthcare). Products were purified using a Cleanseq magnetic bead solution (Agentcourt Bioscience). Purified sequence reactions were ana- 2. Materials and methods lyzed using an ABI 3700 or ABI 3730XL automated sequencer. All sequences were analyzed from the 30 and the 50 ends indepen- 2.1. Taxon sampling, data collection, and sequence alignment dently to ensure congruence between the reads. The forward and the reverse sequences were imported and edited in Geneious™ We constructed a nucleotide sequence dataset for 68 species of version v5.4 (Drummond et al., 2011); ambiguous bases were Cyrtodactylus from throughout the range of the genus, plus two corrected by eye. All edited sequences were aligned by eye. Pro- species of Geckoella, six Hemidactylus, and six genera and species tein-coding sequences were investigated in MacClade v4.08 of Palearctic naked-toed gecko. For purposes of establishing a time- (Maddison and Maddison, 2003) to ensure the
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