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Phylogeography of the Endemic Gymnocypris Chilianensis

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Phylogeography of the Endemic Gymnocypris Chilianensis Molecular Phylogenetics and Evolution 59 (2011) 303–310 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeography of the endemic Gymnocypris chilianensis (Cyprinidae): Sequential westward colonization followed by allopatric evolution in response to cyclical Pleistocene glaciations on the Tibetan Plateau ⇑ Kai Zhao a,1, Ziyuan Duan b,c,1, Zuogang Peng d, Xiaoni Gan b, Renyi Zhang a, Shunping He b, , ⇑ Xinquan Zhao a, a Key Laboratory of Adaptation and Evolution of Plateau Biota (AEPB), Northwest Plateau Institute of Biology, The Chinese Academy of Science, Xining 810001, China b Laboratory of Fish Phylogenetics and Biogeography, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China c Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China d Key Laboratory of Freshwater Fish Resources, Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Beibei, Chongqing 400715, China article info abstract Article history: The schizothoracine Gymnocypris chilianensis is restricted to the Shiyang, Ruoshui and Shule Rivers, listed Received 19 June 2010 from east to west, along the northeast edge of the Tibetan Plateau. This distribution provides a valuable Revised 13 January 2011 system to test hypotheses about postglacial colonization. We used mitochondrial DNA sequence data (a Accepted 1 February 2011 control region and the cytochrome b gene; 1894 bp) to assess the phylogeographic structure of this spe- Available online 23 February 2011 cies based on 278 specimens sampled from throughout the species’ entire geographical range. We found three lineages corresponding geographically to the three rivers, suggesting three independent glacial dif- Keywords: ferentiation centers within the northeast edge of the Tibetan Plateau. The phylogenetic analysis sug- Mitochondrial control region and gested that the Shiyang River population forms a lineage that separated from the other populations of cytochrome b Schizothoracine fish G. chilianensis at the basal phylogenetic split within this species. The molecular data further demon- Phylogeography strated a clear pattern of decreasing genetic diversity from the eastern Shiyang River towards the central Pleistocene glaciations Ruoshui River and western Shule River lineages, a pattern consistent with sequential western coloniza- Tibetan Plateau tion. We therefore propose a phylogeographic scenario for G. chilianensis of a gradual westerly expansion from the Shiyang River population along the northeast edge of the Tibetan Plateau, with subsequent allo- patric evolution at approximately 0.37 and 0.05 million years ago (Ma), through at least two glacial max- ima. Together with the genetic evidence reported in other species, our findings suggest that this common biogeographic pattern emphasizes the importance of the northeastern edge region of the Tibetan Plateau as a hotspot of genetic diversity for some taxa. Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction region for the study of evolution of endemic specialized plateau species. In contrast to the large number of studies investigating Studies on the biotic consequences of Quaternary environmen- the phylogeography of widespread taxa, far less attention has tal change have increased rapidly during the last decade. The been given to the taxa endemic to the Tibetan Plateau. There is Pleistocene glacial and interglacial cycles have resulted in pro- a lack of phylogeographic studies below the species level, partly found shifts in the ranges of the biota. Through the application due to the inaccessibility of samples in this region. Despite this, of phylogeography and modern molecular techniques, these pat- a few such studies on the plant, fish, and avian species endemic terns have been repeatedly demonstrated across myriad taxa in to the Tibetan Plateau have provided empirical evidence of a Europe and America (Dick and Heuertz, 2008; Elderkin et al., common biogeographic pattern of glacier-induced fragmentation. 2008; Peters et al., 2008; Streicher et al., 2009; Phillipsen and These studies indicate that the genetic divergence observed in Metcalf, 2009; Acosta and Premoli, 2010). The Tibetan Plateau is most taxa is due to the isolation of populations in refugia during the youngest plateau on Earth, which has made it an important the Quaternary glacial advances (Zhao et al., 2005, 2007; Zhang et al., 2005; Liu et al., 2006; Yang et al., 2006; Qi et al., 2007; Jin et al., 2008; Jin and Liu, 2010). The topographical diversity ⇑ Corresponding authors. Fax: +86 971 6143282 (X; Zhao), fax: +86 27 68780071 of the Tibetan Plateau might have created networks of refugia (S. He). during glaciations, thus forming barriers to the subsequent E-mail addresses: [email protected] (S. He), [email protected] (X. Zhao). 1 These authors contributed equally to this work. expansion of endemic species (Hewitt, 2004; Qu et al., 2005). 1055-7903/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2011.02.001 304 K. Zhao et al. / Molecular Phylogenetics and Evolution 59 (2011) 303–310 Fig. 1. A map of the Hexi River system showing the sampling sites (see Table 1) and the geographical distribution of the phylogenetic lineages (see Fig. 2). Black represents the Shiyang River lineage, grey represents the Ruoshui River lineage, and white represents the Shule River lineage. The dashed lines represent the ridge of the Qilian Mountains in the northeast Tibetan Plateau. The complex plateau conditions and the diversified climate tion. This study uses phylogeographic methods to infer the genetic could allow for different patterns of postglacial colonization to pre- structure and population history of a schizothoracine fish species dominate in the species endemic to the Tibetan Plateau. One such endemic to the Hexi River system, Gymnocypris chilianensis. pattern is indicated in phylogeographical studies of two endemic Gymnocypris chilianensis is restricted to the Hexi River system, species: the red-necked snow finch Pyrgilauda ruficollis and the tree and it is the only schizothoracine fish in the system (Li and species Juniperus przewalskii. These studies reveal that the two spe- Chang, 1974; Wu and Wu, 1992). This species has been found cies colonized the plateau using a similar route from a single refu- at altitudes ranging from 1500 to 2500 m (Zhao, 1991). We gium in the northeast and eastern edge of the Tibetan Plateau after recently found that G. chilianensis also inhabits mountain streams the extensive glacial period (Qu et al., 2005; Zhang et al., 2005). at altitudes of 3800 m, showing irregular altitudinal movement Whether the pattern of genetic variation observed in P. ruficollis and remarkable adaptability. The species status of G. chilianensis and J. przewalskii is shared among the other Tibetan Plateau fauna has been disputed, and is currently classified as a subspecies of remains to be determined. Gymnocypris eckloni (Zhao, 1986; Chen and Cao, 2000). Recent The Hexi River system in the northeastern edge of the Tibetan evidence suggests that the morphological differences between G. Plateau comprises the Shiyang, Ruoshui, and Shule Rivers, listed chilianensis and G. eckloni may be corroborated by genetic data, from east to west (Fig. 1). All three rivers derive from the Qilian with a high mean sequence divergence of 2.5% in mtDNA (the Mountains in the northeast plateau, flow north into the Hexi re- combined control region and cytochrome b gene) (Zhao et al., gion, and finally disappear in the desert. Stratigraphic evidence 2009). However, prior to this study, genetic surveys had not been shows that the northeast Tibetan Plateau was dramatically affected conducted across the entire distribution range of G. chilianensis. by the geological and climatic upheaval caused by the large-scale The initial genetic study of G. chilianensis was based on a small uplift of the plateau during the Pleistocene (Chen, 1988; Pan, sample (17 individuals) and was restricted to one river and two 1994; Pan et al., 1996; Zhang et al., 2003). Thus, the fauna that in- localities (Zhao et al., 2009). The present study is based on 278 habit the Hexi River system are a model group well suited for samples from 13 locations across the three rivers, covering the studying the patterns of glacial refugia and postglacial coloniza- entire range of the species. K. Zhao et al. / Molecular Phylogenetics and Evolution 59 (2011) 303–310 305 Table 1 The sampling locations, number of specimens (n), and river systems for the samples of G. chilianensis used in this study. Coordinates: eastern longitude/northern latitude. The location codes correspond to those in Fig. 1. Lineages Location codes Coordinates Sampling location n Shiyang River SW 103°100/38°620 Shiyang River, Wuwei 17 HS 103°040/37°770 Hongshui River, Wuwei 16 XY 101°990/38°040 Xiying River, Wuwei 20 DD 102°410/38°010 Dongda River, Sunan 18 Ruoshui River SD 100°850/38°880 Shandan River, Shandan 21a RS 99°460/39°820 Ruoshui River, Gaotai 20a HH 100°400/39°190 Heihe River, Zhangye 16 JT 98°900/39°990 Tuole River, Jinta 18 TL 98°610/38°710 Tuole River, Qilian 32 Shule River CM 96°800/39°900 Changma, Yumen 23 YM 96°940/40°500 Yumenzhen, Yumen 23 SH 95°530/40°560 Shule River, Anxi 29 YL 95°980/39°960 Yulin River, Anxi 25 a Eight specimens from the Shandan River (SD) and nine specimens from the Ruoshui River (RS) were provided in a previous work and were utilized in this study (see Appendix 1 for the GenBank accession numbers; Zhao et al., 2009). This study aims to analyze mitochondrial DNA sequence data control region (including the first and second hypervariable (the control region and cytochrome b gene) to examine the popu- sequences) was amplified and sequenced with the new specific lation genetic structure and evolutionary history of G. chilianensis, primers GEDL200 (50-CAC CCC TGG CTC CCA AAG CCA G-30) and to present a hypothesis of population dynamics explaining the and GEDH860 (50-AGG GGT TTG ACA AGA ATA ACA GGA-30).
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