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A Case Study of the Crotalus Triseriatus Species Group of Montane Rattlesnakes Robert W

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A Case Study of the Crotalus Triseriatus Species Group of Montane Rattlesnakes Robert W Journal of Biogeography (J. Biogeogr.) (2011) 38, 697–710 ORIGINAL Evolutionary drivers of ARTICLE phylogeographical diversity in the highlands of Mexico: a case study of the Crotalus triseriatus species group of montane rattlesnakes Robert W. Bryson Jr1*, Robert W. Murphy2,3, Amy Lathrop2 and David Lazcano-Villareal4 1School of Life Sciences, University of Nevada, ABSTRACT Las Vegas, Las Vegas, NV, USA, 2Centre for Aim To assess the genealogical relationships of widespread montane rattlesnakes Biodiversity and Conservation Biology, Royal Ontario Museum, Toronto, ON, Canada, in the Crotalus triseriatus species group and to clarify the role of Late Neogene 3State Key Laboratory of Genetic Resources and mountain building and Pleistocene pine–oak forest fragmentation in driving the Evolution, Kunming Institute of Zoology, diversification of Mexican highland taxa. The Chinese Academy of Sciences, Kunming, Location Highlands of mainland Mexico and the south-western United States 4 China, Laboratorio de Herpetologı´a, (Texas, New Mexico, and Arizona). Universidad Auto´noma de Nuevo Leo´n, San Nicolas de los Garza, Nuevo Leo´n, Me´xico Methods A synthesis of inferences was used to address several associated questions about the biogeography of the Mexican highlands and the evolutionary drivers of phylogeographical diversity in co-distributed taxa. We combined extensive range-wide sampling (130 individuals representing five putative species) and mixed-model phylogenetic analyses of 2408 base pairs of mitochondrial DNA to estimate genealogical relationships and divergence times within the C. triseriatus species group. We then assessed the tempo of diversification using a maximum likelihood framework based on the birth– death process. Estimated times of divergences provided a probabilistic temporal component and questioned whether diversification rates have remained constant or varied over time. Finally, we looked for phylogeographical patterns in other co-distributed taxa. Results We identified eight major lineages within the C. triseriatus group, and inferred strong correspondence between maternal and geographic history within most lineages. At least one cryptic species was detected. Relationships among lineages were generally congruent with previous molecular studies, with differences largely attributable to our expanded taxonomic and geographic sampling. Estimated divergences between most major lineages occurred in the Late Miocene and Pliocene. Phylogeographical structure within each lineage appeared to have been generated primarily during the Pleistocene. Although the scale of genetic diversity recognized affected estimated rates of diversification, rates appeared to have been constant through time. Main conclusions The biogeographical history of the C. triseriatus group implies a dynamic history for the highlands of Mexico. The Neogene formation of the Transvolcanic Belt appears responsible for structuring geographic diversity among major lineages. Pleistocene glacial–interglacial climatic cycles and resultant expansions and contractions of the Mexican pine–oak forest appear *Correspondence: Robert W. Bryson Jr, School of Life Sciences, University of Nevada, Las to have driven widespread divergences within lineages. Climatic change, paired Vegas, 4505 Maryland Parkway, Las Vegas, NV with the complex topography of Mexico, probably produced a myriad of species- 89154-4004, USA. specific responses in co-distributed Mexican highland taxa. The high degree of E-mail: [email protected] ª 2010 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/jbi 697 doi:10.1111/j.1365-2699.2010.02431.x R. W. Bryson Jr et al. genetic differentiation recovered in our study and others suggests that the Mexican highlands may contain considerably more diversity than currently recognized. Keywords Biogeography, divergence dating, diversification rates, Mexico, phylogeography, pine–oak forest, reptiles, Transvolcanic Belt, Viperidae. and allopatric populations are generally monophyletic (Sulli- INTRODUCTION van et al., 1997; Harris et al., 2000; Hafner et al., 2005; Leo´n- The geographical location, complex topography, and dynamic Paniagua et al., 2007). Several morphologically cryptic mater- tectonic and climatic history of the Mexican highlands provide nal lineages occur within the Transvolcanic Belt, Sierra Madre a matrix for the evolution of a spectacularly diverse biota. The Oriental and Sierra Madre del Sur (small mammals: Sullivan Mexican highlands harbour a significant amount of western et al., 1997; Harris et al., 2000; Arellano et al., 2005; Leo´n- North America’s biodiversity (Ramamoorthy et al., 1993; Paniagua et al., 2007; birds: Garcı´a-Moreno et al., 2004; Mittermeier et al., 2005) and a level of biotic endemism Navarro-Sigu¨enza et al., 2008; Puebla-Olivares et al., 2008). scarcely rivalled elsewhere (Peterson et al., 1993). The evolu- These high levels of genetic divergence suggest that endemism tionary drivers of this diversity, however, remain poorly in the Mexican highlands may be vastly underestimated. documented. Despite early broad-scale inferences about the Studies of genetic structuring in other co-distributed taxa are biogeographical history of Mexico, dating back to Dunn (1931), needed in order to develop a more complete understanding of few studies explore the historical diversification of Mexican the evolutionary drivers of diversification. highland taxa. This impedes the ability of researchers to identify The relatively small-bodied montane rattlesnakes (Viperi- fine-scale biogeographical patterns and the extent to which dae) inhabiting the pine–oak forests of mainland Mexico these apply to co-distributed taxa (McCormack et al., 2008a). represent an ideal model system for investigating historical Neogene vicariance, largely due to orogenesis, and Quater- patterns of diversification in the Mexican highlands. This large nary climate change have been the postulated drivers of group includes 40% of the total number of currently recog- evolutionary diversification in western North America (e.g. nized species of rattlesnakes (Campbell & Lamar, 2004) and is Jaeger et al., 2005; Riddle & Hafner, 2006). Although most of found in all of the major mountainous regions of Mexico. The the major mountain ranges in Mexico are relatively ancient phylogenetic relationships among these rattlesnakes, however, (Ferrusquı´a-Villafranca, 1993; Ferrusquı´a-Villafranca & Gon- are contentious. Those species currently allied with the za´lez-Guzma´n, 2005), the Transvolcanic Belt of central Mexico Crotalus triseriatus species group (C. triseriatus, C. aquilus, was formed during the Neogene (Ferrusquı´a-Villafranca, 1993; C. lepidus, C. pusillus and C. ravus; Murphy et al., 2002; Castoe Becerra, 2005). This development may have had a significant & Parkinson, 2006) are especially difficult to classify. The impact on the diversification of highland taxa, because the content of this species group varies despite more than 65 years uplift created new geographical barriers and montane habitats, of intensive systematic effort (Gloyd, 1940; Smith, 1946; and linked previously isolated highland biotas (Anducho- Klauber, 1952, 1972; Brattstrom, 1964; Dorcas, 1992; Murphy Reyes et al., 2008). Historical diversification of highland taxa et al., 2002). Furthermore, several authors suggest that the may also have been influenced by dramatic habitat fluctuations Mexican highlands may harbour one or more cryptic species during the Pleistocene that resulted in the cyclical downward within the C. triseriatus species group (Armstrong & Murphy, displacement and retraction of Mexican pine–oak woodlands 1979; Murphy et al., 2002). (Martin & Harrell, 1957; Van Devender, 1990; McDonald, Our study addresses several questions relating to the 1993). This displacement could have resulted in population evolutionary history of the C. triseriatus species group. We and range expansions in highland species during glacial combine extensive range-wide sampling and mixed-model periods, and isolation in high elevation refugia during the phylogenetic analyses to formulate a robust hypothesis of interglacials (Moreno-Letelier & Pin˜ero, 2009). Subsequent phylogenetic relationships and to address long-standing post-glacial fragmentation of Mexican pine–oak woodlands uncertainties about cryptic diversity. We also estimate dates (Van Devender, 1990) may have caused fragmentation of these of lineage divergences based on a relaxed molecular clock to isolated refugial populations (e.g. McCormack et al., 2008b). provide a probabilistic temporal calibration for the phylogeny. Gene flow would have been affected by these events. We model the temporal distribution of divergence events to Molecular studies of montane Mexican taxa often discover assess the potential effects of Late Neogene mountain building complex phylogeographical patterns. In small mammals, for and Pleistocene pine–oak forest fragmentation on the tempo of example, mitochondrial DNA (mtDNA) differentiation is high diversification. Finally, we look for phylogeographical patterns 698 Journal of Biogeography 38, 697–710 ª 2010 Blackwell Publishing Ltd Phylogeography of the Crotalus triseriatus group in the C. triseriatus group that are shared with other aquilus’). Based on recent phylogenetic analyses (Murphy co-distributed highland taxa. et al., 2002; Castoe & Parkinson, 2006; Wu¨ster et al., 2008), we used Sistrurus catenatus and S. miliarus as outgroup taxa. We sequenced relatively slowly evolving and more quickly MATERIALS AND METHODS evolving
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