Phylogeography of the Common Pheasant Phasianus Colchinus

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Phylogeography of the Common Pheasant Phasianus colchinus

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Phylogeography of the Common Pheasant Phasianus colchicus

NASRIN KAYVANFAR,1 MANSOUR ALIABADIAN,1,2* XIAOJU NIU,3 ZHENGWANG ZHANG3 & YANG LIU4* 1Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran 2Research Department of Zoological Innovation, Institute of Applied Zoology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran 3Key Laboratory for Biodiversity Sciences and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing 100875, China 4State Key Laboratory of Biocontrol and College of Ecology and Evolution, Sun Yat-sen University, Guangzhou 510275, China

The Common Pheasant Phasianus colchicus is widely distributed in temperate to subtropical regions of the Palaearctic realm. Populations of Common Pheasant have been classi- fied into five subspecies groups based on morphological variations in male plumage. Previous phylogeographical studies have focused on limited sets of subspecies groups in the eastern Palaearctic and knowledge on subspecies in the western Palaearctic region is still poor. In this study, we undertake the first comprehensive analysis of subspecies from all five defined subspecies groups across the entire Palaearctic region. Two mitochondrial (CYTB and CR) and two nuclear (HMG and SPI) loci were used to investigate genetic relationships of these subspecies groups and to infer their dispersal routes. Our results revealed that the subspecies elegans, with its range in northwestern Yunnan, China, was in the basal position among 17 studied subspecies, supporting a previous hypothesis that the Common Pheasant most probably originated in forests in southeastern China. Sub- species in the western Palaearctic region nested within the most subspecies-rich torquatus group (‘Grey-rumped Pheasants’), indicating that the torquatus group is not a clade but instead forms a gradation with other subspecies and subspecies groups. Our dating analysis suggested that the initial divergence among populations of Common Pheasant originated around 3.4 Mya with subsequent dispersal into the Western Palaearctic region during the Late Pliocene–Lower Pleistocene approximately 2.5–1.8 Mya. We propose two possible east-to-west colonization routes for the Common Pheasant and suggest conservation implications for some regional subspecies. Overall, this study demonstrates the lack of concordance between morphology-based subspecies delimitation and their genetic relationships. This is likely to be a consequence of initial isolation due to historical vicariance followed by population admixture due to recent range expansion of Common Pheasant in the western Palaearctic region. Keywords: mitochondrial DNA, morphology, nuclear DNA, subspecies, vicariance.

Natural populations with large geographical ranges through population subdivision may be a historical usually exhibit intra-speciﬁc variation, with sub- consequence of isolation due to geographical barri- populations explicitly differing from one another ers (Avise 2000) or evolutionary processes such as in aspects of morphology, genetics and ecology natural selection and genetic drift (Slatkin 1987). (Mayr 1963). Increased population structure Phylogeography aims to infer the historical biogeographical processes that shape contemporary patterns of genetic variation within and between *Corresponding authors. Emails: [email protected]; [email protected] species (Avise 2000). For species with large

geographical ranges in particular, range-wide phylo- 1994, Johnsgard 1999, Liu et al. 2010). Because geography can provide deep insights into how geo- plumage variation may vary considerably with diet logical, environmental and evolutionary factors and habitat (Cramp & Brooks 1988), a dependence contribute to population structuring or species on morphological traits may be unreliable for phylo- divergence. Conducting comprehensive range-wide genetic assessment (Alstrom€ et al. 2013). In con- studies is a challenge, however, as it requires the trast, phylogeographical analysis of spatial and collection of field data on a very large scale, over temporal genetic variation can uncover population hundreds to thousands of kilometres and across or subspecies affinities and associated evolutionary many countries (Liu et al. 2011, 2012a,b). processes (Gu et al. 2013). For example, in a previ- One example of a species with a large geographi- ous study, Qu et al. (2009) uncovered the existence cal range and pronounced intra-specific divergence of a major genetic gap among principalis-chrysome- is the Common Pheasant Phasianus colchicus. This las, mongolicus and torquatus groups and could not species is the world’s most widespread pheasant, fully validate some subspecies. Although previous with a natural distribution in the Palaearctic region. phylogeographical studies have revealed some pat- Its range extends from eastern–southeastern Europe terns of populations/subspecies divisions within (east of the Black Sea) to far eastern Siberia and Common Pheasant (Qu et al. 2009, Liu et al. southwards to Indochina and Afghanistan (Hill & 2010), an analysis involving complete geographical Robertson 1988). Thirty recognized subspecies cat- coverage of all subspecies as well as the application egorized into five subspecies groups have been of multilocus DNA data with both mtDNA and defined, with some subspecies occasionally afforded nuclear DNA has not been conducted. specific status (Madge & McGowan 2002). The In this study, we undertake the most comprehen- validity of some subspecies, however, has been sive molecular phylogeographical analyses questioned because of the clinal variation existing conducted on this species to date, with continent- among them (Cramp & Simmons 1980, Johnsgard wide sampling of subspecies (17 of 30 recognized 1999, Madge & McGowan 2002). The five sub- subspecies). The analyses, which were based on a species groups are as follows: (1) the colchicus group multilocus dataset including both fast-evolving (‘Black-necked Pheasants’ west and south of the mtDNA genes and more moderate- to slow-evol- Caspian Sea) including P. c. persicus, P. c. talischen- ving nuclear DNA loci, allowed us to clarify sis, P. c. colchicus and P. c. septentrionalis; (2) the whether the molecular data reflect the traditional principalis-chrysomelas group (‘White-winged Pheas- taxonomy of all five morphological groups of Com- ants’ in Central Asia) including P. c. principalis, mon Pheasant subspecies in the Palaearctic region, P. c. zarudnyi, P. c. chrysomelas, P. c. bianchii, and to estimate the timing of divergence within P. c. zerafschanicus and P. c. shawii; (3) the tarimen- Common Pheasant subspecies or groups. In addi- sis group (population in Tarim Basin in southeastern tion, we attempted to infer possible east-to-west Xinjiang, China) including P. c. tarimensis; (4) the dispersal routes of Common Pheasant subspecies mongolicus group (Kirghiz Pheasants in northern based on our phylogeographical results and testing Xinjiang, China and eastern Kazakhstan) compris- proposed routes that have been based on morphol- ing P. c. mongolicus and P. c. turcestanicus; and (5) ogy (Solokha 1994). the most subspecies-rich group, the torquatus group (‘Grey-rumped Pheasants’, mostly distributed in METHODS East Asia) containing P. c. satscheuensis, P. c. pallasi, P. c. suehschanensis, P. c. torquatus, P. c. kiang- Taxonomic sampling suensis, P. c. rothschildi, P. c. karpowi, P. c. strauchi, P. c. elegans, P. c. vlangalii, P. c. hagenbecki, We collected 85 fresh tissue, blood and feather P. c. edzinensis, P. c. alaschanicus, P. c. sohokhoten- samples from 17 subspecies (57% of defined sub- sis, P. c. decollatus, P. c. takatsukasae and P. c. for- species) of Common Pheasant from all groups in mosanus (Madge & McGowan 2002) (Fig. 1). the Palaearctic region (Fig. 1). Voucher specimens The designations of the five groups and thus their were deposited at the Zoology Museum of Fer- constituent subspecies have been based on biogeog- dowsi University of Mashhad, Iran (ZMFUM; raphy and morphological characters in males, such colchicus, talischensis, persicus and principalis), Bei- as variation in body size, plumage patterns and the jing Normal University, China (satscheuensis, strau- presence or absence of a white neck ring (Solokha chi, rothschildi, vlangalii, kiangsuensis, karpowi,

Figure 1. The distribution map of 30 Common Pheasant Phasianus colchicus subspecies and Green Pheasant Phasianus versicolor in the Palaearctic region. Studied taxa are indicated with a star. The five main subspecies groups are indicated with Roman numer- als: I = colchicus, II = principalis-chrysomelas, III = tarimensis,IV= mongolicus and V = torquatus. pallasi, torquatus, elegans and suehschanensis) and SerpinCF/SerpinCR and HMG172F/HMG174R Sun Yat-sen University, China (mongolicus, shawii (Kimball et al. 1999) were used to amplify mito- and tarimensis). A list of studied taxa and out- chondrial cytochrome b (CYTB) and the control groups along with voucher numbers, localities and region (CR), and autosomal intronic regions of GenBank accession numbers are provided in Sup- nuclear genes High mobility group 17 (HMG) and porting Information Table S1. Serpin peptidase inhibitor clade C (SPI), respectively. For the two mitochondrial loci, PCR ampli- fications followed the protocols described in Liu DNA sequencing and alignment et al. (2010) except that an annealing temperature Total genomic DNA was extracted from tissue, of 60 °C was used. For the two nuclear introns, blood and feather samples. Muscle samples were PCR protocols followed Kimball et al. (2009). preserved in 96% ethanol and stored at À20 °C. After visualization on 1% agarose gels stained with Blood samples were mixed immediately in blood SYBR Gold (Invitrogen), PCR products were storage buffer (0.1 M Tris-HCl, 0.04 M EDTA-Na2, sequenced in both directions on an ABI 3730 XL 1.0 M NaCl, and 0.5% sodium dodecyl sulfate automated sequencer by Macrogen (Seoul, Korea). (SDS)). Feathers were kept in dry envelopes. DNA The samples of Iranian and Chinese Common was extracted using a QIA quick DNeasy kit (Qia- Pheasants were amplified separately in two differ- gen, Hilden, Germany) according to the manufac- ent laboratories, one at Ferdowsi University of turer’s instructions and the standard salt extraction Mashhad and one at Beijing Normal University. method (Bruford et al. 1992). Before DNA extraction, samples were incubated overnight at 55 °Cin Phylogenetic analysis extraction buffer (2% SDS and 0.5 mg/mL pro- teinase K). The sequences of the mitochondrial (CYTB and Primer pairs L14731/H16065 (Kimball et al. CR) and nuclear (HMG and SPI) loci were aligned 1999), L16757/H1259 (Randi & Lucchini 1998), using MAFFT v6.847b (Katoh & Toh 2008), with

subsequent adjustments in BIOEDIT v7.0.5 (Hall We further combined the mtDNA–nuclear 1999). We constructed phylogenetic trees using DNA dataset to estimate divergence times between maximum likelihood (ML) and Bayesian inference major evolutionary clades of Common Pheasants in (BI) in PAUP v4.0b10 (Swofford 2003) and BEAST v1.7 (Drummond et al. 2012). XML files for MRBAYES v3.2.1 (Ronquist & Huelsenbeck 2003), the BEAST analyses were generated in BEAUTI v1.7 respectively. The phylogenetic trees were rooted (Drummond et al. 2012). Analyses were run under using homologous sequences of a Green Pheasant the Yule speciation model. We used separate P. versicolor individual, the closest sister species of nucleotide substitution models for each marker. For the Common Pheasant. The amino acid transla- the mtDNA data, we implemented a normal prior tions of gene coding regions were examined for for the substitution rate (ucld. mean parameter) stop codons to ensure all were functional proteins. using a robust overall divergence rate of To reveal different possible topologies and identify 2.1 Æ 0.1% per million years (Myr) (0.0105 Æ sources of conflict between genes, the three data- 0.0005 substitutions/site/Myr; Weir & Schluter sets (mtDNA, nuclear DNA and the concatenated 2008). For the nuclear intronic data, we used a data) were analysed for both ML and BI analyses, mean rate of 0.00135 Æ 0.00045 substitutions/ separately. All analyses were run under best-fit site/Myr (Ellegren 2007), also implemented as a nucleotide substitution models estimated in MODEL- normal prior. In preliminary runs, a relaxed uncor- TEST v3.7 (Posada & Crandall 1998) using the related lognormal rate distribution was used to Akaike information criterion (Akaike 1974). Using check whether a strict molecular clock was appro- MODELTEST, we identified TVM+I+G and priate for any of the datasets. Other priors were set GTR+I+G as the best-fitting substitution models with default values. For these analyses, 5 9 107 for the mtDNA and combined mtDNA–nuclear generations were performed, with sampling every datasets, respectively (Table S2). 1000 generations. Each analysis was run twice. The For ML analyses, the best-fit substitution models MCMC output was analysed in TRACER v1.6. (Ram- were used in a subsequent ML heuristic tree search baut et al. 2014) to evaluate whether valid esti- with 10 random addition sequence replicates and mates of the posterior distribution of the tree-bisection-reconnection branch swapping. To parameters had been obtained. The first 25% of assess nodal support, 100 bootstrap replicates were generations were discarded as burn-in, well after run under ML with the parameters estimated auto- stationarity of chain likelihood values had been matically. For BI analyses, we performed four inde- established. Trees were summarized using pendent runs of Metropolis-coupled Markov chain TREEANNOTATOR v1.7.4 (Rambaut & Drummond Monte Carlo (MCMC) analyses on the above three 2012) with options ‘Maximum clade credibility datasets starting from random trees. The MCMC tree’ and ‘Mean heights’ and were visualized in FIG- chains were run for 10 million generations with TREE v1.3.1. sampling every 10 000 generations. The first 10% of To test for historical rapid population expan- generations were discarded as burn-in, well after sta- sion, a mismatch distribution analysis among indi- tionarity of the chains had been established, and viduals was carried out using mtDNA loci (CYTB posterior probabilities were calculated from the and CR) only under a population growth–decline remaining samples (pooled from the two simultane- model in DNASP v5.0 (Rogers & Harpending ous runs). We determined convergence among the 1992). In such an analysis, demographic stability is independent runs observing the ESS values of the illustrated by multimodal distribution, and a uni- posterior distribution of all resulting parameters in modal pattern is consistent with sudden expansion TRACER v1.6 (Rambaut et al. 2014). The resulting (Slatkin & Hudson 1991). Using the same dataset, tree was visualized using FIGTREE v1.3.1 (Rambaut we also performed the neutrality test of Fu’s FS & Drummond 2009). and Tajima’s D. We visualized phylogenetic relationships in Com- mon Pheasants by incorporating the polymorphism RESULTS of the combined mtDNA–nuclear DNA dataset. Based on this combined dataset, we generated Sequence characteristics Neighbor-Net networks (Bryant & Moulton 2004) of P. colchicus samples using uncorrected p-distances Sequencing of 85 P. colchicus individuals from 17 in SPLITSTREE v4.10 (Huson & Bryant 2006). subspecies of six groups generated 2435 base pairs

(bp), including 1280 bp of mtDNA and 1155 bp (Supporting Information Figs S1 and S2). As our of nuclear DNA. The aligned CR sequence dataset nuclear data contained much lower levels of poly- comprised 483 bp, of which 37 sites (7.66%) were morphism, the concatenated analysis relied on the parsimony-informative, and the CYTB dataset con- information from the mtDNA loci (Fig. 2). Over- tained 797 bp including 24 (3.01%) parsimony- all, the topology of the trees generated by BI was informative sites. The alignments of HMG with generally congruent with those recovered by ML 641 bp and SPI with 514 bp contained no parsi- and also between the mtDNA and combined data- mony-informative sites. The total concatenated set (Supporting Information Fig. S3). We thus dataset comprised 61 parsimony-informative sites focus mainly on the results obtained from Bayesian (4.8%). analysis of the combined mtDNA–nuclear DNA dataset. In the trees generated from the combined data- Multilocus phylogeny set using MRBAYES (Fig. 2) and BEAST (Fig. 3), indi- Separate phylogenetic analyses were performed on viduals of the subspecies elegans formed a distinct the mitochondrial and nuclear datasets clade with relatively low support, 0.80 for BI

Figure 2. Condensed Bayesian inference tree of subspecies of Phasianus colchicus based on the concatenated dataset (each number in green represents the number of individuals condensed). Numbers on nodes represent ML bootstrap values (given only if > 70%). PP (posterior probability) values from the Bayesian inference only at the > 0.99 (**) and > 0.95 (*) signiﬁcance level are noted. The splits of the branches A–G are discussed in the text. Taxa names are represented in abbreviated forms. Subspecies are numbered separately and coloured bars refer to groups. Nona Karimzadeh drew the artwork of subspecies of Common Pheasant.

(Fig. 2) and 62% for ML (Fig. S3), which was sis- Estimated divergence times ter to a clade that contained all other subspecies. Within this clade, pre-defined morphological The dating analysis (Fig. 3) suggested that the basal groups did not correspond to monophyletic divergence separating the Green Pheasant from genetic groups. The genetic relationships of sub- Common Pheasant occurred approximately species within the most subspecies-rich group 4.3 million years ago (Mya). The separation of the torquatus were unresolved, with low support val- elegans group from the remaining taxa is estimated ues in both analyses. However, among subspecies to have taken place approximately 3.4 Mya, with in the western Palaearctic, we identified six subsequent divergence of the torquatus group from branches with high posterior probability values in other subspecies in the western groups around the analyses. Clade A encompassed all sampled 2.5 Mya. The split between the other western groups except for torquatus and elegans groups, groups and the tarimensis group took place later, consisting of P. c. shawii, P. c. tarimensis and beginning approximately 1.8 Mya. The principalis Clade B. Clade B in turn was divided into C and the colchicus groups diverged from their most (principalis) and D, with the latter further divided recent common ancestor approximately 1.6 Mya into E (mongolicus group) and F (colchicus group) and further divergences within these subspecies (Figs 2 and 3). Finally, Clade G, consisting of occurred approximately 1.4 Mya (Fig. 3). ‘Caucasus Pheasant’ P. c. colchicus individuals, was a distinct, strongly supported group nested Demographic analysis within F. The haplotype network analysis based on the Demographic histories were inferred by a pairwise concatenated dataset largely showed close genetic mismatch distribution analysis based on mitochon- relationships among subspecies in the western drial CYTB and CR haplotypes. The mismatch dis- Palaearctic (principalis-chrysomelas, mongolicus, tribution for the entire set of samples (Fig. 5A) colchicus). These taxa had closer relationships with and four pheasant subspecies groups (Fig. 5B–E) the tarimensis subspecies in the southern Xinjiang was bell-shaped, which would be expected under Uygur region than the torquatus subspecies group a sudden expansion model. Two groups (colchicus in eastern Asia and elegans group in southwestern and torquatus) fit both sudden and spatial expan- China (Fig. 4). sion models (Fig. 5B,E). The inferred population

Figure 3. Phylogenetic relationships and estimation of divergence times among subspecies of Phasianus colchicus based on the concatenated dataset. Values at nodes represent posterior probabilities at the > 0.99 (**) and > 0.95 (*) signiﬁcance level. Numbers below nodes indicate estimated divergence times and their 95% highest posterior density (HPD) in million years before the present.

semi-arid forests, arable lands and along hillsides ranging in elevation between À10 m (along the Caspian Sea and Xinjiang) and 3000 m (Chang et al. 2008, Kayvanfar & Aliabadian 2013). This species has a long history as a captive gamebird, with inter-subspecies hybrid populations having been intentionally introduced beyond its natural range, for example to Western Europe and North America. Common Pheasant plumage patterns, especially the presence of a white collar and varied coloration on rump and wings in males, have long been considered important diagnostic characters for intra-specific taxonomy and have even been used to reconstruct evolutionary relationships among subspecies (Johnsgard 1999). Figure 4. Multilocus networks based on the combined dataset Although subspecies groupings were previously of mitochondrial and nuclear DNA sequences of Phasianus defined using morphological discontinuities among colchicus inferred by SPLITSTREE. subspecies, the present study demonstrates some size expansion was further supported by signifi- incongruence between morphology-based sub- cantly negative values of Fu’s FS and Tajima’s D species divisions and genetic relationships. In par- (Table 1). The mismatch distribution suggested ticular, the elegans subspecies, previously within the colchicus and torquatus groups of Common the torquatus group because of morphological simi- Pheasant underwent a rapid, recent population larity, probably forms the earliest subspecies and range expansion. The principalis-chrysomelas (although support was low). In addition to being group showed neutral variation according to Taji- genetically distinct, individuals in the elegans sub- ma’s D value and recent population expansion species are distinguished from those of subspecies based on Fu’s FS value. The tarimensis group may within the torquatus group by the black bars on have decreased population sizes or has experienced the basal part of the much wider central tail feath- over-dominant selection. No mismatch analysis was ers. Mantle and scapular feathers are darker, the conducted on the mongolicus and elegans groups upper feathers of the mantle are more spotted at because of their small sample sizes (Table 1). their extremities with dark green, and lower back and rump feathers have rather wide sub-terminal Table 1. Statistics from mismatch analyses of Phasianus dark-green bands. colchicus subspecies. Morphologically there is a major split between western (tarimensis, principalis-chrysomelas, mon- ’ ’ Dataset (n) Tajima s D Fu s FS golicus and colchicus) and eastern groups (torquatus Total samples (46) À0.2134** À17.948** and elegans) of Common Pheasant. In general, sub- colchicus (12) À0.283** À0.622* species of the western groups have darker plumage principalis-chrysomelas (5) 0.000** À0.701* and possess brownish-red or blackish-brown tarimensis (29) 0.087** 2.680* rumps, whereas most members of the eastern torquatus (50) À0.512* À9.837* groups have lighter plumage and bluish to darkish- Parameters were calculated under sudden and spatial expan- grey rumps (Fig. 2). Geographically, the eastern sion models. n = number of polymorphic sites. The signifi- groups are allopatric with the four western groups, ’ ’ cance of Tajima s D and Fu s FS-values is indicated as with the former distributed in humid and sub- * < ** < follows: P 0.010; P 0.001. humid zones and the latter occupying arid regions. However, our findings revealed that subspecies in DISCUSSION the western Palaearctic are nested within the most subspecies-rich torquatus group (‘Grey-rumped Phylogeography and taxonomic Pheasants’), making the latter a grade of subspecies implications and subspecies groups (Figs 2–4), probably indicat- The Common Pheasant is widely distributed in ing rapid morphological evolution. In addition, no the Palaearctic region, mainly in forest grasslands, obvious clinal geographical variation in rump

Figure 5. Demographic history (pairwise differences and allelic frequency graphs) of Phasianus colchicus subspecies inferred from the concatenated CR and CYTB dataset. Observed mismatch distributions (red line) for the dataset are compared with expected distributions under a population growth–decline model (green line). Numbers of pairwise differences are on the x-axis and relative fre- quencies on the y-axis. A: with total samples, B: colchicus,C:principalis-chrysomelas,D:tarimensis,E:torquatus.

coloration or the presence of a white collar is evi- between slightly isolated subspecies. To analyse dent. Where subspecies ranges are contiguous, further the boundaries and genetic admixture however, some degree of gradual changes in plu- among subspecies, efforts to quantify morphology mage characters (Liu & Sun 1992), and shared and to genotype populations using high-poly- genetic polymorphism has been documented pre- morphic genetic markers will be necessary (Wang viously (e.g. Qu et al. 2009, Liu et al. 2010, et al. 2017). Zhang et al. 2014) and in the present study (Figs S1 and S2). This probably suggests frequent Biogeographical conclusions admixture among adjacent subspecies and violates the status of some Common Pheasant subspecies Cyclical Pleistocene climatic oscillations are pre- (Zhang et al. 2014). In contrast, differences in sumed to have played important roles in shaping morphology (Madge & McGowan 2002) and per- the geographical distribution, demographic history haps genetic variation can be more abrupt and ultimately patterns of genetic diversiﬁcation of

many plant and animal species in the Palaearctic northern foothills of the East Tian Shan Depres- region (Avise 2000, Hewitt 2000). According to sion to the Black Sea. Such a colonization wave our study, the Green Pheasant and the Common would have continued along the southern shore of Pheasant are estimated to have diverged from each the Caspian Sea, the foothills of the Elburz Moun- other approximately 2.5–6.5 Mya (Fig. 3). This tains and the Caucasus. In central and southern timeframe may be due to vicariance speciation Afghanistan and Iran, the distribution range of that was associated with the isolation of the Japan Common Pheasant was probably restricted to the archipelago from the East Asian mainland in the Parapamisus and Kopet Dagh mountains during late Early Miocene (Millien-Parra & Jaeger 1999). the Early to Middle Pleistocene because of the The divergence between the elegans group and cool and dry climate (Potapov 1978, Kehl 2009). other P. colchicus groups happened approximately The dispersal of western groups in an easterly 3.4 Mya, with the torquatus group diverging from direction was probably limited by the ancient the latter around 2.8 Mya (Fig. 3). These events Dzungar Desert (Solokha 1994). The aridification immediately pre-date the shift to a cooler and fluc- of Central Asia, which began at the end of the tuating climate that characterized the Pleistocene. Neogene, took place when the Amu Darya, The placement of subspecies elegans at the the major river in Central Asia, began flowing into most basal position within the species implies that the Aral-Sary Kamysh Depression, with conse- Common Pheasant might have its origin in the quent formation of the Garagum (Karakum) subtropical forests of Yunnan and Sichuan in Desert. With increasing desertification, Pheasant southwestern China, as postulated by Delacour populations were gradually confined to river val- (1977). These regions are hypothesized to have leys and humid foothills, resulting in disruption of been refugia for several avian species during the the species’ range (Fet & Atamuradov 1994). last glaciations (Qu et al. 2011). Yunnan and Subsequent disruption of their western range and Sichuan are adjacent to the Himalayan and Heng- evolution of isolated populations led to the genetic duan mountains and are surrounded by massive differentiation of members in the colchicus group forests (Liu 1983). It is likely that populations of (P. c. persicus, P. c. talischensis and P. c. colchicus). elegans were isolated and evolved independently in The shorter dispersal route was associated with these regions. the formation of the principalis group out of China. Based on our phylogenetic relationships within These populations could have penetrated valleys of the western group (Fig. 2), we tentatively propose the Murghab and Tedzhen mountains and the East the existence of two dispersal routes into the west- Kopet Dagh foothills, leading to the colonization of ern Palaearctic region. Under our colonization the principalis subspecies in accordance with the hypothesis, Common Pheasant may have dispersed findings of Solokha (1994) (Fig. 6). As the mongoli- from east to west during the Late Pliocene-Early cus and colchicus groups appeared more closely Pleistocene, approximately 1.8 Mya; such a sce- related to each other than to the principalis group, nario is consistent with Solokha’s suggestion (Solo- these two groups might have descended from a kha 1994) that pheasants migrated from the Tarim common ancestor from the Tarim basin with one Basin to the South Tajik Depression when popula- ancestral group colonizing the upper Tian Shan tions dispersed ‘out of China’. This is a long route Mountains to give rise to the mongolicus group involving the division of tarimensis into the ranges (Figs 2–4, 6). The haplotype network analysis of mongolicus and colchicus. This route was open also confirmed that the mongolicus group was repre- until the Middle Pleistocene, as the Pamir-Alay sented by a distinct haplotype. This finding suggests mountain system might not yet have been a major that populations of Common Pheasant from these barrier to species dispersal (Bidos 1985). At the regions probably remained isolated throughout the same time, the already extant mountain ranges of Pleistocene irrespective of climatic oscillations and Kunlun could have been a barrier to pheasant dis- desertification of northern China (Qu et al. 2009). persal from the Tarim River drainage toward India In conclusion, our proposed scenario based on in the southwest (Solokha 1994). genetic analysis is partially in agreement with the The other short route is associated with the scenario by Solokha (1994), who proposed three expansion of tarimensis to principalis. After its col- dispersal waves of the Common Pheasants in cen- onization to the west, the range of Common tral Asia and the Caucasus based on phenotypic Pheasant may have been continuous from the variation and palaeo-geographical data (Fig. 6).

Our analysis also suggests different patterns of (Braasch et al. 2011), primarily because of anthro- demographic histories among subspecies groups. pogenic activities. In addition, the destruction of The results of the mismatch distribution analysis natural habitats has led to the reduction of the suggest that some of the subspecies groups (colchi- geographical range of some subspecies. For exam- cus, torquatus and principalis-chrysomelas) have ple, the destruction of Tamarix pentandra and Pop- experienced a rapid, recent population and range ulus euphratica forests in the foothills of the Kopet expansion. Whereas the recent expansion hypothe- Dagh range and the introduction of irrigation in sis is supported by the non-significant mismatch the Tedzhen Oasis have caused a two-fold increase distribution, no evidence for changes in population in the distribution range of P. c. principalis on for- size can be inferred for the principalis-chrysomelas mer farm lands in the last 40 years without any group based on Tajima’s D (Table 1). Because artificial breeding attempts; this situation is similar Fu’s FS is a more sensitive indicator of population to the southeastern range extension of P. c. persi- expansion and genetic hitchhiking compared with cus (Fet & Atamuradov 1994, Solokha 1994). The Tajima’s D (Fu 1997), the former may provide distribution of the ‘Northern Caucasus Pheasant’ better evidence for expansion of the principalis- P. c. septentrionalis is highly fragmented and only chrysomelas group. In contrast, the tarimensis remains genetically pure in the lower reaches of group may have suffered a recent bottleneck, pos- the Samur River. Currently, many conservation sibly due to desertification (Fig. 5). programmes are introducing pheasants into their historical ranges in most North Caucasian countries; however, the genetic purity of those intro- Conservation applications duced pheasants is not clear (Koblik et al. 2006). Dispersal and shifts in the ranges of various sub- The in situ population of P. c. turcestanicus is now species of Common Pheasant are still occurring extinct as a result of the aridification of the Aral

Figure 6. Proposed dispersal routes of Phasianus colchicus from the eastern to western side of the Palaearctic region: the long route itself divides into two sub-routes, from the Tarim Basin to the range of subspecies mongolicus and from the Tarim Basin to the range of subspecies colchicus (yellow arrows), separately; the short one expanded from the Tarim Basin to the range of subspecies principalis (red arrow). Dashed lines refer to potential historical colonization routes that are most likely geographical barriers at present. The colours within each pie chart reﬂect the haplotypes.

Sea area but this subspecies is still present in the Alstrom,€ P., Barnes, K.N., Olsson, U., Barker, F.K., region of the Syr Darya river in northeast Uzbekistan Bloomer, P., Khan, A.A., Qureshi, M.A., Guillaumet, A., and southern Kazakhstan (Scott et al. 1987, Abdu- Crochet, P.A. & Ryan, P.G. 2013. Multilocus phylogeny of the avian family Alaudidae (larks) reveals complex salyamov 1988, Clements 2000, Lepage 2007). morphological evolution, non-monophyletic genera and Although our study has provided the first multi- hidden species diversity. Mol. Phylogenet. Evol. 69: 1043– locus phylogeographical picture of Common 1056. Pheasant at a subspecies-group level, interesting Atamuradov, K.I. 1994. Biogeography and Ecology of questions still remain. First, the torquatus group Turkmenistan. Dordrecht: Springer. Avise, J.C. 2000. Phylogeography: the History and Formation and some subspecies in the torquatus group do not of Species. Boston, MA: Harvard University Press. represent monophyletic groups (see also Qu et al. Bidos, V.S. 1985. Ekologiya tadzhikskogo cherno-zolotogo 2009) and relationships among these remain unre- fazana [Ecology of the Tajik Black Gold Pheasant]. Abstr. solved in the present study. On the other hand, Ph.D. Thesis, Unpublished. the overlap of P. c. persicus and P. c. talischensis in Braasch, T., Pes, T., Michel, S. & Jacken, H. 2011. The subspecies of the Common Pheasant Phasianus colchicus the phylogenetic tree challenges the validity of in the wild and captivity. Int. J. Galliformes Conserv. 2:6– these subspecies. This pattern is probably caused 13. by shallow divergence and frequent recent popula- Bruford, M.W., Hanotte, O., Brookfield, J.F.Y. & Burke, T. tion admixture (Liu et al. 2011). Genomic-scale 1992. Single-locus and multi locus DNA fingerprint. In markers derived from next-generation sequencing Hoelzel, A.R. (ed.) Molecular Genetic Analysis of Populations: A Practical Approach: 225–270. Oxford: Oxford can provide higher resolution (Ekblom & Galindo University IRL Press. 2011), and may be able to answer these remaining Bryant, D. & Moulton, V. 2004. Neighbor-net: an questions associated with speciation and local agglomerative method for the construction of phylogenetic adaptation of Common Pheasant (Seehausen et al. networks. Mol. Biol. Evol. 21: 255–265. 2014). Chang, J., Wang, B., Zhang, Y.Y., Liu, Y., Liang, W., Wang, J.C., Shi, H.T., Su, W.B. & Zhang, Z.W. 2008. Molecular evidence for species status of the endangered Hainan We thank the Department of the Environment, Ferdowsi peacock pheasant. Zool. Sci. 25:30–35. University of Mashhad, Iran, for giving sampling permis- Clements, J.F. 2000. Birds of the World: a Checklist. Ithaca, sion to N.K. We also extend our appreciation to Per NY: Cornell University Press. Alstrom€ and Seyyed Mahmood Ghasempouri for their Cramp, S. & Brooks, D. 1988. The Birds of the Western useful comments and thank Ying Liu, Jun Gou, Jie Xu, Palearctic: vol. 5: Tyrant Flycatchers to Thrushes. Oxford: Mohammad-Reza Masoud, Koros Rabii, Ahmad Delar- Oxford University Press. ami, Hamid Amini, Arash Delfanian, Masoud Kayvanfar, Cramp, S. & Simmons, K.E.L. 1980. The Birds of the Ali Gholamhosseini and Kiyumars Moladoost for help Western Palearctic: vol. 2: Hawks to Bustards. Oxford: with sampling. Ying Liu, De Chen, Guoling Chen, Niloo- Oxford University Press. far Alaie, Shigeki Asai, Tooba Mohammadian and Beh- Delacour, J. 1977. The Pheasants of the World, 2nd edn. noush Moodi are acknowledged for their assistance with Hindhead and Lamarsh: Spur Publications and World molecular laboratory work. Special thanks are due to Bar- Pheasant Association. bara Goodson for editing the English text and Edouard Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. Jelen for acquiring skin images of Common Pheasants. 2012. 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microsatellite markers for the common pheasant. Phasianus Figure S2. Condensed Bayesian inference tree colchicus using RAD-Seq. Avian Res. in press, DOI: 10. of subspecies of Phasianus colchicus based on con- 1186/s40657-017-0060-y catenate nuclear High mobility group 17 (HMG) Weir, J.T. & Schluter, D. 2008. Calibrating the avian molecular clock. Mol. Ecol. 17: 2321–2328. and Serpin peptidase inhibitor clade C (SPI) data- Zhang, L., An, B., Backstrom,€ N. & Liu, N. 2014. set. PP (posterior probability) values from the Phylogeography-based delimitation of subspecies Bayesian analysis (10 million replicates) are indi- boundaries in the Common Pheasant (Phasianus colchicus). cated at the > 0.90 (**) and > 0.75 (*) signiﬁcance – Biochem. Genet. 52:38 51. level. Letters on branches represent similar branch splits on the phylogenetic tree in Figure 2. Received 12 April 2016; revision accepted 22 December 2016. Figure S3. Maximum likelihood inference tree Associate Editor: Martin Collinson. of subspecies of Phasianus colchicus based on the concatenated mtDNA and nuclear DNA dataset. Numbers on nodes represent ML bootstrap values SUPPORTING INFORMATION (given only if > 70%). The splits of the branches Additional Supporting Information may be found A, B, C, D, E, F and G are discussed in the text. in the online version of this article: Taxa names are represented in abbreviated forms. Figure S1. Condensed Bayesian inference tree Table S1. List of samples of subspecies of Pha- of subspecies of Phasianus colchicus based on mito- sianus colchicus included in this study along with chondrial cytochrome b (CYTB) and control region museum voucher numbers, GenBank accession (CR) dataset. PP (posterior probability) values numbers and collection localities. from the Bayesian analysis (10 million replicates) Table S2. Data partitions, estimated models of are indicated at the > 0.90 (**) and > 0.75 (*) sig- sequence evolution and total number of characters niﬁcance level. Letters on branches represent simi- in each partition used in Phasianus colchicus phylo- lar branch splits on the phylogenetic tree in genetic analyses. Figure 2.

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