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The Phylogenetic Position and Speciation Dynamics of the Genus Perdix (Phasianidae, Galliformes)

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The Phylogenetic Position and Speciation Dynamics of the Genus Perdix (Phasianidae, Galliformes) ARTICLE IN PRESS Molecular Phylogenetics and Evolution xxx (2010) xxx–xxx Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev The phylogenetic position and speciation dynamics of the genus Perdix (Phasianidae, Galliformes) Xin-kang Bao a, Nai-fa Liu a,*, Jiang-yong Qu b, Xiao-li Wang a, Bei An a, Long-ying Wen c, Sen Song a a School of Life Science, Lanzhou University, Lanzhou 730000, China b Department of Biological Science and Technology, Qiongzhou College, Wuzhishan, Hainan 572200, China c Department of Chemistry & Life Sciences, Leshan Teachers College, Leshan, Sichuan 614004, China article info abstract Article history: The nuclear gene (c-mos) and mitochondrial genes (CYT B and ND2) sequences, representing 44 phasia- Received 30 December 2009 nid species and 26 genera (mainly distributed in China), were used to study the phylogeny of the genus Revised 24 March 2010 Perdix, which comprises three partridge species. Maximum parsimony and Bayesian methods were Accepted 29 March 2010 employed, and the analysis of mitochondrial sequence data and the combined dataset showed that Perdix Available online xxxx is specifically related either to typical pheasants or to Ithaginis. Phylogenetic trees also indicated that: (1) Perdix is monophyletic; (2) the Tibetan partridge (Perdix hodgsoniae) has been consistently placed as basal Keywords: to all other Perdix, and the Daurian partridge (Perdix dauuricae) is placed sister to gray partridge (Perdix Phasianidae perdix); (3) the Daurian partridge subspecies przewalskii and Tibetan partridge subspecies hodgsoniae are Perdix c-mos basal to other subspecies in their species clade, respectively. Speciation in Perdix was likely promoted by Cytochrome b the late Pliocene/early Pleistocene intensive uplift of the Tibetan Plateau and by Pleistocene glaciations. ND2 Ó 2010 Published by Elsevier Inc. Phylogenetics Speciation 1. Introduction evidence, Johnsgard (1988) constructed a highly speculative phy- letic dendrogram of perdicine genera, in which Perdix was placed The typical partridges (Perdix) contain three grassland-adapted sister to Francolinus. Another point of view is that Perdix belongs species: gray, Daurian and Tibetan partridge (Perdix perdix, Perdix to a clade of small ‘‘pheasants” (Hudson et al., 1966), and has a clo- dauuricae and Perdix hodgsoniae). They have a number of typical ser relationship with true pheasant species than with other genera partridge traits such as small build, little sexual dimorphism in traditionally considered ‘‘partridges”, such as Alectoris (Randi et al., weight and plumage and little or no plumage iridescence. They 1991; Wen et al., 2005). Some DNA-based evidences have sug- were traditionally placed in the tribe Perdicini, subfamily Phasiani- gested a novel hypothesis that gray partridge, wild turkey (Melea- nae and family Phasianidae (Johnsgard, 1988). The gray partridge is gris gallopavo) and grouse (Tetraoninae) might share a closer distributed across a wide range of Eurasian grasslands in eight sub- relationship (Kimball et al., 1999; Lucchini and Randi, 1999; Dim- species, which range from Scandinavia south to northern Spain and cheff et al., 2002; Pereira and Baker, 2006; Crowe et al., 2006). Re- Italy, and east to the western Siberia and Xinjiang (see Fig. 1). The cent molecular study (Kimball and Braun, 2008) supported the gray partridge was recently introduced into North America. Dauri- placement of the gray partridge at the base of a large clade contain- an partridge has three subspecies (Cheng et al., 1978; Zheng, 2005) ing typical pheasants, rather than the weakly supported with wild living across Asian grasslands from the Russian Altai east to Amur- turkey as indicated by Crowe et al. (2006). land and Ussuriland. There is limited overlap with the gray par- Johnsgard (1988) used fossil and zoogeographic data to postu- tridge in western Xinjiang and with Tibetan partridge in the late that Perdix species probably originated in northern Asia, and northern part of Qinghai. The four subspecies of Tibetan partridge glaciations may have isolated their ancestral form into a westerly are residents of montane grasslands around the Tibetan Plateau component that gave rise to gray partridge, an easterly form that (Fig. 1). produced Daurian partridge and a southern and more montane The phylogenetic position of Perdix within Phasianidae has been adapted population in the Himalayas that evolved into Tibetan par- controversial. Based on morphological and zoogeographic tridge. Based on morphologic and zoogeographic informations, Cheng et al. (1978) conjectured that Daurian and Tibetan par- * Corresponding author. Fax: +86 0931 8912561. tridges have a common origin, and gray partridge separated earlier E-mail address: [email protected] (N.-f. Liu). from the proto-Perdix stock. 1055-7903/$ - see front matter Ó 2010 Published by Elsevier Inc. doi:10.1016/j.ympev.2010.03.038 Please cite this article in press as: Bao, X.-k., et al. The phylogenetic position and speciation dynamics of the genus Perdix (Phasianidae, Galliformes). Mol. Phylogenet. Evol. (2010), doi:10.1016/j.ympev.2010.03.038 ARTICLE IN PRESS 2 X.-k. Bao et al. / Molecular Phylogenetics and Evolution xxx (2010) xxx–xxx Fig. 1. Distribution of the Daurian (D), gray (G), Tibetan (T) partridges and the speciational course (as arrows indicate) inferred from the combined data (c-mos + CYT B + ND2) analyses. In this paper, nucleotide sequences of nuclear proto-oncogene Lucchini (1998); primers used for PCR amplification and sequenc- (c-mos) and two mitochondrial genes (cytochrome b and NADH ing of CYT B, ND2 and c-mos were gathered from the literature dehydrogenase subunit 2) representing all three extant species of (Table 2). Perdix and multiple genera of Phasianidae were analyzed to (1) To amplify DNA, 50 lL PCR reactions were performed using ascertain the evolutionary relationship between Perdix and other standard buffer and MgCl2 concentrations, 2.5 mM dNTP 4 lL, related phasianid genera, (2) produce a molecular phylogeny of 10 lM each primer 3 lL, 2 units of BIOTAQ DNA polymerase (Bio- the extant species of Perdix, and (3) correlate the inferred molecu- line, Randolph, MA), and 100 ng of genomic DNA. The thermal pro- lar phylogeny and extent of interspecific genetic divergence with file comprised an initial denaturation step at 94 °C for 5 min, Pliocene/Pleistocene biogeographical scenarios in the Qinghai–Ti- followed by 35 cycles of 94 °C for 1 min, 48–55 °C for 1 min and bet Plateau region to suggest speciational patterns in Perdix. 72 °C for 2 min, with a final extension step of 72 °C for 8 min. PCR products were gel-purified using 1.5% low melting point aga- 2. Materials and methods rose, and were sequenced using an ABI 377 DNA sequencer. The nucleotide sequences were double-stranded and aligned 2.1. Taxon sampling using CLUSTAL X with the default options (Thompson et al., 1997) and refined manually. Gene sequence boundaries were DNA samples were collected with a focus on the taxa distributed determined by comparison with published sequences of other gen- in China because the country is rich in gamebirds, especially in era of Galliformes downloaded from Genbank. Sequences collected phasianid species, and most of the distribution of Daurian and Tibe- for this study have been deposited in GenBank (accession numbers tan partridge is restricted to China. Multiple representatives of all are shown in Table 1). the phasianine genera and almost all perdicine genera (except the genus Lerwa) throughout China have been sampled. Taxa studied herein (Table 1, Classification of Galliformes cited from Johnsgard 2.3. Phylogenetic analysis (1988)) include 44 phasianid species and 26 of 37 phasianine genera. The choice of outgroup on which to root cladograms are based on the Considering that all mtDNA gene sequences are virtually inher- assumptions that the Anseriformes (ducks, geese and screamers) are ited as one linkage group, and CYT B and ND2 showed similar rates sister to the Galliformes (Sibley and Ahlquist, 1990; Groth and Bar- and types of both nucleotide and amino acid substitutions (John- rowclough, 1999; Cracraft et al., 2004; Hackett et al., 2008). son and Sorenson, 1998), the two mtDNA gene segments were con- catenated into a single partition and analyzed simultaneously. 2.2. Laboratory methods Congruence among the different DNA data sets was evaluated using the incongruence-length-difference (ILD) test (Farris et al., DNA was extracted from blood, pin feather or muscle tissue by 1995), which was conducted using only parsimony-informative the ethanol sedimentation procedure as described by Randi and characters. A total of 1000 replicates were conducted for the ILD Please cite this article in press as: Bao, X.-k., et al. The phylogenetic position and speciation dynamics of the genus Perdix (Phasianidae, Galliformes). Mol. Phylogenet. Evol. (2010), doi:10.1016/j.ympev.2010.03.038 ARTICLE IN PRESS X.-k. Bao et al. / Molecular Phylogenetics and Evolution xxx (2010) xxx–xxx 3 Table 1 Studied taxa and source of DNA sequence data (classification of Galliformes cited from Johnsgard (1988)). Avian species Sample locality/source GenBank Accession Nos. CYT B ND2 c-mos Order: Galliformes Family: Phasianidae Subfamily: Phasianinae Tribe: Perdicini Tetraogallus tibetanus tibetanus Artux, Xinjiang Uygur Autonomous Region EU839457 GU214303 GU214274 Tetraogallus tibetanus przewalskii Tianzhu county, Gansu province EU839456 EU845746 GU214273 Tanggula,
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