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Postglacial Colonization of the Tibetan Plateau Inferred from the Matrilineal Genetic Structure of the Endemic Red-Necked Snow F

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Postglacial Colonization of the Tibetan Plateau Inferred from the Matrilineal Genetic Structure of the Endemic Red-Necked Snow F Molecular Ecology (2005) 14, 1767–1781 doi: 10.1111/j.1365-294X.2005.02528.x PostglacialBlackwell Publishing, Ltd. colonization of the Tibetan plateau inferred from the matrilineal genetic structure of the endemic red-necked snow finch, Pyrgilauda ruficollis YAN HUA QU,* PER G. P. ERICSON,† FU MIN LEI* and SHOU HSIEN LI‡ *Institute of Zoology, Chinese Academy of Sciences, 25 Beisihuanxi Road, Haidian District, Beijing 100080, People’s Republic of China, †Department of Vertebrate Zoology, Swedish Museum of Natural History, PO Box 50007, SE-10405 Stockholm, Sweden, ‡Department of Life Sciences, National Taiwan Normal University, Taiwan Abstract Most phylogeographical studies of postglacial colonization focus on high latitude locations in the Northern Hemisphere. Here, we studied the phylogeographical structure of the red-necked snow finch Pyrgilauda ruficollis, an endemic species of the Tibetan plateau. We analysed 879 base pairs (bp) of the mitochondrial cytochrome b gene and 529 bp of the control region in 41 birds from four regional groups separated by mountain ranges. We detected 34 haplotypes, 31 of which occurred in a single individual and only three of which were shared among sampling sites within regional groups or among regional groups. Haplotype diversity was high (h = 0.94); nucleotide diversity was low (d = 0.00415) and genetic differentiation was virtually non-existent. Analyses of mismatch distributions and geographi- cally nested clades yielded results consistent with contiguous range expansion, and the expansion times were estimated as 0.07–0.19 million years ago (Ma). Our results suggest that P. ruficollis colonized the Tibetan plateau after the extensive glacial period (0.5–0.175 Ma), expanding from the eastern margin towards the inner plateau. Thus, in contrast to many of the postglacial phylogeographical structures known at high latitudes, this colonization occurred without matrilineal population structuring. This might be due to the short glacial cycles typical of the Tibetan plateau, adaptation of P. ruficollis to cold conditions, or refugia and colonized habitat being semicontinuous and thus promoting population mixing. Keywords: genetic structure, Pleistocene glaciations, postglacial colonization, Pyrgilauda ruficollis Received 5 September 2004; revision received 19 November 2004; accepted 7 February 2005 of phylogeographical structures are available for regions at Introduction different latitudes, studies that focus on previously glaciated Postglacial colonization has created a variety of phylogeo- montane areas are rare. Herein we present a study of a species graphical structures in species from different latitudes endemic to the Tibetan plateau. (Rising & Avise 1993; Hewitt 1996; Merila et al. 1997). Previ- The Tibetan plateau occupies an area of 2.5 million km2, or ously glaciated areas in the Arctic and the sub-Arctic regions approximately one-quarter of China, and has an average contain species with low levels of clade divergence, indicat- altitude of 4500 m above sea level (a.s.l.). It is the youngest ing recent colonization followed by population expansion. plateau on Earth; the most recent uplift event occurring In Europe and North America, such areas contain species between 3.6 and 1.7 million years ago (Ma) (Li & Zhou 1998). with intermediate clade divergences, indicating their sur- The uplift caused great climatic changes: grasslands replaced vival during several ice ages. In the tropics, this area contains forests while the climate gradually became drier, colder and species with deeply diverged clades, often within small geo- windier, and glaciers and deserts developed (Wu et al. 2001). graphical areas, indicating their survival there since the The unique geomorphological configuration, the complex land Pliocene (Hewitt 2000, 2004). Whereas many comparisons conditions, the diversified climate, and the unique geological evolution combine to make the Tibetan plateau an area of world- Correspondence: Yan Hua Qu, Fax: 0086 10 62565689; E-mail: wide importance for the evolution of endemic, specialized [email protected] montane species (Cheng 1981; Tang 1996; Macey et al. 1998). © 2005 Blackwell Publishing Ltd 1768 Y. H. QU ET AL. Glacial cycles in alpine regions have generated varied to avoid sampling relatives (Hansen et al. 1997). Blood or phylogeographical structures that reflect different routes tissue samples were obtained from 43 birds. Groups with of postglacial colonization (Mardulyn 2001; Despres et al. adequate sample sizes were created by pooling birds into 2002; Kropf et al. 2003). The topographical diversity of the four regional groups: QR (Qinghai region, average altitude Tibetan plateau might have created both networks of refugia 4000 m a.s.l.), TR (Tanggulashan region, average altitude during glaciation and complex barriers to subsequent expan- 5500 m a.s.l.), WTR (west Tibet region, average altitude 4800 m sion (Hewitt 2004). In comparison to species that colonized a.s.l.), and ETR (east Tibet region, average altitude 4500 m their present-day ranges from lower latitudes, montane a.s.l.) (Fig. 1b, c and Table 1). species undergoing postglacial colonization would have needed to undertake altitudinal shifts, and might have been DNA extraction, polymerase chain reaction and able to spread more widely across tundra and steppe plains. sequencing In this study, we assessed these possibilities by conducting a phylogeographical study of an alpine bird endemic to Genomic DNA was extracted from blood or tissue samples the Tibetan plateau, the red-necked snow finch Pyrgilauda using the QIAamp DNA Mini Kit (QIAGEN) following manu- ruficollis. facturer’s instructions. Initially, 879 bp of the cytochrome b Pyrgilauda ruficollis is one of the four species of the genus gene was amplified as a single fragment with the primer pair Pyrgilauda (Eck 1996), three of which (Pyrgilauda ruficollis, L14841 (5′-CCATCCAACATCTCAGCATGATGAAA-3′) Pyrgilauda blanfordi and Pyrgilauda davidiana) have similar (Kocher et al. 1989) and H15915 (5′-AACTGCAGTCATCT- ranges in the Tibetan plateau (Qu et al. 2002). This species CCGGTTTACAAGAC-3′) (Edwards & Wilson 1990). The is a year-round resident across the mountain steppe zone thermocycling program consisted of an initial denaturation at altitudes of 3500–5300 m a.s.l., or higher (Fig. 1a), where at 94 °C for 5 min, followed by 40 cycles of 94 °C for 40 s, 49 °C it occurs in alpine meadows and breeds inside pika for 40 s, and 72 °C for 5 min. For the sequencing reactions, (Ochotona spp.) burrows. Pyrgilauda ruficollis makes irregular the following primers were used: L14841, H15915, P5L (5′- altitudinal movements, descending to lower altitudes in CCTTCCTCCACGAAACAGGCTCAAACAACCC-3′) and large flocks during autumn and winter when driven by H658 (5′-TCTTTGATGGAGTAGTAGGGGTGGAATGG-3′) extreme weather conditions (Cramp & Perrins 1994). The (Irestedt et al. 2002), with P5L and H658 as internal primers highest known records of P. ruficollis are from 5300 m a.s.l. on the light and heavy strands, respectively. in the Tanggula Mountains. Several mountain ranges, A 529-bp fragment of the control region was amplified some with peaks over 6500 m a.s.l., occur within the distribu- using the primer pair, F304 (5′-CTTGACACTGATGCAC- tion of P. ruficollis, and these might create barriers to gene TTG-3′) and H1261 (5′-AGGTACCATCTTGGCATCTTC- flow because they are believed to be major zoogeographi- 3′) (Marshall & Baker 1997). The thermocycling program cal barriers associated with evolutionary divergence consisted of an initial denaturation at 94 °C for 5 min, (Mayr 1963; Macey et al. 1998; Bos & Sites 2001; Roslin 2001; followed by 40 cycles of 94 °C for 40 s, 56 °C for 40 s, and Sorenson & Payne 2001). 72 °C for 5 min. The same primers were used for the sequen- Here, we assume that the present-day distribution of cing reactions. P. ruficollis stems directly from postglacial colonization. We The polymerase chain reaction (PCR) products were hypothesize that isolation in different refugia surrounding purified using QIAquickTM PCR purification Kit (QIAGEN), the Tibetan plateau led to phylogeographical divergence in and then sequenced on a Perkin-Elmer 377 semiautomated this species. We also hypothesize that the mountain ranges DNA sequencer (Applied BioSystems), using Perkin-Elmer within the present distribution range constitute barriers to Prism terminator cycle sequencing kits (Applied BioSystems) gene flow that have led to population differentiation. The with AmpliTaq FS polymerase with BigDye terminators. goal of the study is to test these hypotheses by describing the Both strands of each PCR product were sequenced. The phylogeographical and population structures of Pyrgilauda sequencing program consisted of 25 cycles of denaturation ruficollis in the Tibetan plateau and using these structures at 96 °C for 30 s, annealing at 50 °C for 15 s, and extension to infer evidence for population bottlenecks and expansion, at 60 °C for 4 min. and genetic divergence. Multiple sequence fragments were obtained by sequen- cing with different primers for each gene and individual. While a pair of internal primers (P5L and H658) of the cyto- Materials and methods chrome b was used to sequence approximately half of the gene (about 400 bp and 500 bp, respectively), other pair of Study area and sample collections primers (L14841 and H15915) obtained whole sequence. The birds were collected using mist nets from 10 sites covering No length variation in the control region was found, mak- major parts
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