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Molecular Data Resolve Placement of the Olympic Marmot and Estimate Dates of Trans-Beringian Interchange Author(S) :Scott J

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Molecular Data Resolve Placement of the Olympic Marmot and Estimate Dates of Trans-Beringian Interchange Author(S) :Scott J Molecular data resolve placement of the Olympic marmot and estimate dates of trans-Beringian interchange Author(s) :Scott J. Steppan, G. J. Kenagy, Christopher Zawadzki, Rafael Robles, Elena A. Lyapunova, and Robert S. Hoffmann Source: Journal of Mammalogy, 92(5):1028-1037. 2011. Published By: American Society of Mammalogists DOI: 10.1644/10-MAMM-A-272.1 URL: http://www.bioone.org/doi/full/10.1644/10-MAMM-A-272.1 BioOne (www.bioone.org) is a a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Mammalogy, 92(5):1028–1037, 2011 Molecular data resolve placement of the Olympic marmot and estimate dates of trans-Beringian interchange SCOTT J. STEPPAN,* G. J. KENAGY,CHRISTOPHER ZAWADZKI,RAFAEL ROBLES,ELENA A. LYAPUNOVA, AND ROBERT S. HOFFMANN Department of Biological Science, Florida State University, Tallahassee, FL 32306-4295, USA (SJS, CZ, RR) Burke Museum and Department of Biology, University of Washington, Seattle, WA 98195, USA (GJK) Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia (EAL) Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA (RSH) * Correspondent: [email protected] We reinvestigated the phylogeny of all 15 species of Marmota to resolve a conflict between 2 published analyses, one by Kruckenhauser et al. and another by Steppan et al., regarding the Olympic marmot (M. olympus) and to improve resolution in the genus. We acquired fresh samples of M. olympus, combined all available data on mitochondrial DNA (cytochrome b [Cytb] and ND3/ND4), new sequences for ND3/ND4, and 2,000 base pairs (bp) of the nuclear RAG1 gene. All analyses indicate that M. olympus is a much older, rather than more recent, offshoot of the widespread hoary marmot (M. caligata) or Vancouver Island marmot (M. vancouverensis). The mitochondrial data and some RAG1 results are largely congruent, but RAG1 differs on several points, including: the subgenus Marmota appears paraphyletic to Petromarmota, with reciprocally monophyletic Palearctic and Nearctic clades; and the long-tailed marmot (M. caudata) and Menzbier’s marmot (M. menzbieri) are not sister species, suggesting mitochondrial introgression. Asia was colonized by Marmota from North America at approximately 4.6 million years ago (mya), followed by rapid diversification of several major lineages. M. olympus diverged from the M. caligata–M. vancouverensis lineage at approximately 2.6 mya, whereas M. vancouverensis and M. caligata diverged at only about 0.4–1.2 mya. M. olympus might have survived in isolation on the Olympic Peninsula in a nunatak refugium throughout a series of glacial maxima. Key words: cytochrome b, historical biogeography, Marmota olympus, phylogeny, RAG1 E 2011 American Society of Mammalogists DOI: 10.1644/10-MAMM-A-272.1 Marmots (genus Marmota) are large, generally social ground the mountains of the Olympic Peninsula of Washington squirrels (family Sciuridae, tribe Marmotini) with a Holarctic (Edelman 2003). The analysis by Kruckenhauser et al. (1999) distribution (Fig. 1). The genus currently includes 15 species, found M. olympus to be a sister species of the Vancouver and various of these have been the subjects of conspicuous Island marmot (M. vancouverensis), an endangered species comparative studies of sociality and life history (Blumstein endemic to Vancouver Island and separated from the 2007; Ozgul et al. 2007), hibernation physiology (Arnold 1990), Olympic Peninsula to the south by waters of the Strait of and morphological evolution (Cardini et al. 2005, 2007, 2009; Juan de Fuca (Fig. 1). In contrast, Steppan et al. (1999) found Caumul and Polly 2005; Polly 2003). These comparative M. olympus to be a more basal member of the North interests led to 2 recent phylogenetic studies of the genus American clade Petromarmota. The result of Kruckenhauser (Kruckenhauser et al. 1999; Steppan et al. 1999), both of which et al. (1999) suggested that M. olympus is a recently diverged used the complete mitochondrial gene cytochrome b (Cytb). population of M. vancouverensis or of the parapatric and Kruckenhauser et al. (1999) also included mitochondrial ND4 much more widely distributed hoary marmot (M. caligata). data for a subset of species. The 2 studies produced nearly identical results, with one notable exception, the position of the Olympic marmot (M. olympus). This species, consisting of a small and geographically restricted population, is endemic to www.mammalogy.org 1028 October 2011 STEPPAN ET AL.—MARMOT PHYLOGENY AND HISTORY 1029 FIG.1.—Polar-view map showing Holarctic distribution of the genus Marmota. Fifteen currently recognized species are labeled, and dots represent the locations of the samples sequenced for this study. Stippling (M. flaviventris) and darkest shading (M. caligata) are used to distinguish 2 species with large, overlapping ranges in western North America. Further, if M. olympus is specifically distinct, as suggested by understanding of the historical and phylogenetic relationship morphology (Cardini 2003, 2004), then its sibling relationship between M. olympus and M. vancouverensis and their further to M. vancouverensis would represent a case of rapid relationship to M. caligata, we sought to resolve this question diversification among all 3 species because genetic distances by acquiring and sequencing fresh tissues of M. olympus and among them are very low and less than those among most other reanalyzing the phylogeny of the genus. species of marmot (Kruckenhauser et al. 1999; Steppan et al. Here we report the new phylogenetic analysis based on 1999). If the result of Steppan et al. (1999) is correct, speciation additional sequences from 2 individual M. olympus. We also and divergence were not rapid, and the date of isolation of M. sequenced the gene region including portions of transfer olympus from other Petromarmota would be much earlier. A RNAGLY (tRNAGLY), ND3, tRNAARG, ND4L, and ND4 for subsequent study of short, interspersed elements (SINEs) lacked the individuals included by Steppan et al. (1999) so as to data for M. olympus (Brandler et al. 2010) and so could not overlap the ND4 data of Kruckenhauser et al. (1999). We also resolve this issue. sequenced 2,147 base pairs (bp) of the nuclear RAG1 gene to Steppan et al. (1999) examined the data presented by complement the SINE results of Brandler et al. (2010) and Kruckenhauser et al. (1999) and suggested that the olympus allow a concatenation and integration of all available data. This sequence in Kruckenhauser et al. (1999) contained a effort expanded the number of species with ND4 data from 6 to contaminant. Neither study had access to fresh tissue from 12, including M. olympus. By combining the sets of data we also olympus, and both relied on DNA extracted from the skin were able to test species boundaries and improve the survey of (Kruckenhauser et al. 1999) or from skull scrapings (Steppan intraspecific genetic variation to place the divergences of M. et al. 1999) of museum specimens. Both marmot phylogenies vancouverensis and M. olympus in context. We further used have been cited together repeatedly (e.g., Brandler and relaxed molecular-clock dating to estimate divergence dates Lyapunova 2009; Cardini 2004; Cardini et al. 2009; Cardini within the genus and improve estimation of dates for historical and O’Higgins 2005; Kruckenhauser et al. 2009; Nagorsen and trans-Beringian interchange within the genus Marmota. Cardini 2009), but some studies (Herron et al. 2004) have cited only Kruckenhauser et al. (1999) and others (Cardini et al. 2009) only Steppan et al. (1999). Because of the MATERIALS AND METHODS conflicting results in the original papers and in the subsequent Materials and molecular techniques.—The DNA from liver citations and because conservation issues related to both tissue of 2 specimens accessioned of M. olympus by the Burke M. vancouverensis and M. olympus require a more accurate Museum, University of Washington (UWBM), in 2002 was 1030 JOURNAL OF MAMMALOGY Vol. 92, No. 5 extracted by standard proteinase K–phenol–chloroform pro- heuristic search, tree-bisection reconnection, and 20 random- cedures (Maniatis et al. 1982). The entire Cytb gene was addition replicates. Callospermophilus and Otospermophilus amplified with primers and protocols outlined by Steppan together form the sister group to Marmota in ML analyses of et al. (1999). The ND3/ND4 region was amplified for most Cytb (Harrison et al. 2003; Herron et al. 2004) and thus were marmots with primers and conditions from Engel et al. (1998). elevated to generic status in a review by Helgen et al. (2009). This region overlapped the sequences of Kruckenhauser
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