石鸡的分子生态及系统地理学研究
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摘要
石鸡(Alectoris chukar)隶属于鸟纲(Aves)、鸡形目(Galliforms)、雉科(Phasianidae)、石鸡属(Alectoris)。它是石鸡属鸟类中分布最广、亚种分化最多的物种,已报道的亚种多达16个。本文应用线粒体DNA (mtDNA)控制区和微卫星两种分子标记,研究了我国石鸡5个亚种、25个地理种群的分子生态和系统地理学；同时,以mtDNA控制区为分子标记研究了石鸡15个亚种的系统发生关系。本文的主要目的是：(1)通过分子手段构建石鸡亚种的系统发生关系,来探讨石鸡的起源；(2)通过检测石鸡不同地理种群的遗传多样性,揭示不同环境因子对我国石鸡遗传多样性的影响；(3)通过重建我国石鸡亚种不同种群间的系统地理结构,阐述更新世冷暖气候交替对它们系统发生的影响；(4)同时应用母系遗传和双亲遗传的两种分子标记,分析雌雄两性在石鸡种群扩散中的作用；(5)研究我国石鸡各种群的种群历史；(6)从遗传学角度为石鸡的保护提出合理建议。本研究共对石鸡15个亚种427个样本的mtDNA控制区序列和我国的5个亚种25个地理种群288个样本的8个多态性微卫星位点进行了分析,研究结果表明：
1.石鸡mtDNA控制区的碱基含量分别为：T 32.1%、C 27.3%、A 26.4%、G 14.2%,A和C的比例高于G和T的比例,碱基含量显示出一定的偏歧性。在427个样本中共发现127个变异位点,定义了139种单倍型,核苷酸多样性和单倍型多样性分别为0.961和0.0054。8对微卫星位点平均等位基因数为16.875,平均期望杂合度和观察杂合度分别为0.8624和0.7847,表现出较高的遗传多样性。
2.石鸡15亚种及我国石鸡25个地理种群中的大部分都表现出“高单倍型多样性、低核苷酸多样性”的遗传多样性模式。这一遗传多样性模式及mismatch单峰分布特征、Fu's Fs和Tajima's D检验结果都支持我国石鸡及大部分的石鸡种群都经历过种群扩张的历史。红回(HH)、东大山(DSH)、乌海(WH)、武都(WD)和景泰(JT)5个种群的扩张时间发生在0.063-0.144 Ma,即我国北方所处的第四温暖期；其它种群扩张发生在0.027-0.060 Ma之间,即我国北方所处的第五寒冷期。
3.石鸡的遗传多样性中仅有核苷酸多样性与纬度呈显著负相关关系,其它多样性指标(单倍型多样性、观测杂合度与期望杂合度)与各环境因子都没有显著的相关性。石鸡各种群的遗传多样性与各环境因子的变异系数呈现不显著的正相关关系,即在气候不稳定的地区石鸡的遗传多样性反而较高。
4.基于mtDNA控制区计算的石鸡各种群间的基因流高于基于微卫星得出的结果,表明在种群扩散过程中雌性石鸡向外扩散,从而在分子水平上证实了雉科鸟类以雌性为主导的扩散模式。
5.石鸡15个亚种的系统发生树和核苷酸多样性表明石鸡起源于西喜马拉雅山-帕米尔高原-西天山地区,支持了以前基于形态和亚种分布推测石鸡起源于中亚的结论。15个亚种在系统发生树上聚类成两个亚种组,它们的分歧时间大约在45万年前(基于mtDNA控制区遗传距离和MDIV),相当于中更新世晚期青藏高原发生加布拉间冰期(0.30-0.73 Ma)和天山高望峰冰期之后发生的间冰期(0.30-0.47 Ma)。之后,当气候趋向寒冷、干燥时,石鸡分别向外扩散并分歧成与现今形态一致的各亚种。15个亚种间发生分歧的时间相当于欧洲恭兹-民德间冰期(0.30-0.69 Ma)和民德-里斯间冰期(0.125-0.20Ma),以及我国北部的第三(0.24-0.36 Ma)和第四温暖期(0.06-0.15 Ma)发生的时间,表明石鸡是一种冰期扩散、间冰期隔离的物种。MP和贝叶斯树与基于mtDNA控制区遗传距离构建的系统发生树结果一致。
6.分布于我国的石鸡6亚种25种群的核苷酸多样性及亚种的系统发生树表明,我国石鸡起源于两个不同的地区——西喜马拉雅山-帕米尔高原和西天山-塔尔巴哈台地区,其中以起源于新疆部分地区及中亚的干旱半干旱地区即西天山-塔尔巴哈台地区为主。
7.两种分子标记都表明我国石鸡没有明显的系统地理结构,表明我国的石鸡在第四纪冰期-间冰期气候发生剧烈振荡时没有受到太大的影响,各分布区内的山脉也未对它们形成地理屏障。分子变异分析(AMOVA)显示石鸡各地理种群间的遗传差异不显著,但种群内遗传差异极显著(CR序列；FST=0.309,P<0.001；微卫星：FST=0.3093,P<0.001),地理种群内是主要的(CR序列：69.07%；微卫星；81.03%)。Mantel检验结果显示25个种群的FsT/(1-FST)与地理距离间没有显著的相关性(CR序列：r=0.468,P>0.05；微卫星：r=0.15,P>0.05),说明遗传分化不是单纯由地理距离决定的。
8.基于本文的研究结果和可操作性的原则,我们建议分别将分布于陇东黄土高原、贺兰山、祁连山和西天山地区的石鸡作为四个独立的进化显著单元进行管理和保护；我国的6个亚种可以作为6个管理单元进行管理。对种群而言,霍尔果斯(HEG)、阿克塞(AKS)、肃北(SB)、桐川(TC)和武都(WD)种群应被作为独立的管理单元加以管理和保护,尤其是由于WD种群所处的独特的地理位置更应被加以关注。
The chukar (Alectoris chukar) is a kind of widely distributed wildfowls belonging to Aves, Galliformes, Phasianidae, Alectoris whose distribution is throughout Mediter-ranean islands, central Asia and the northeastern of China that. Currently, up to 16 subspecies have been identified. In this study, I addressed the phylogeny of 15 subspecies of chukars based on mitochondrial DNA control region (mtDNA CR), as well as the molecular ecology and phylogeography from 25 populations of five Chinese chukar subspecies based on mtDNA CR and microsatellite markers. The aims of this study are to:(1) explore the origin of chukars by molecular phylogenetic analysis of 15 subspecies of chukar; (2) examine the effects of environmental factors on population genetic diversity of the 25 chukar populations distributed in China; (3) reconstruct the phylogeographic relationship of Chinese chukars under the background of Pleistocene climate oscillation; (4) demonstrate the roles of either sex played in the population expansion, based on both the maternal and bi-parental inherited markers; (5) infer the geological or past demographic events that may probably have determined the current population structures; (6) offer the rational protect proposals of the chukars from the prospective of population genetics. In this study, we obtained mtDNA CR sequences of 427 specimens from 15 chukar subspecies, and sequences of mtDNA CR, as well as eight microsatellite loci, for 288 specimens from 25 Chinese chukar populations. The main results include:
1. The base compositions of mtDNA CR of chukar are T 32.1%, C 27.3%, A 26.4% and G 14.2%. Totally,139 haplotypes were defined by 127 variable sites that were detected in the 427 specimens from 15 chukar subspecies, with the mean haplotype diversity of 0.961 and the nucleotide diversity of 0.0054. The average expected and observed heterozygosity was 0.8624 and 0.7847, implying a relatively high genetic diversity of chukars.
2. The 15 subspecies and 25 Chinese populations of chukars mainly showed the same pattern of "high haplotype diversity while low nucleotide diversity", which, in addition to the unimodal of mismatch distribution and the test of selective neutrality, all indicated that Chinese chukar populations had experienced population expansion at late Pleistocene. Most populations experienced expansion at the metaphase of Late Pleistocene (0.027-0.06 Ma), co-occurring with the fifth cold period, with the exception of populations from Honghui (HH), Wudu (WD), Dongdashan (DSH), Jingtai (JT) and Wuhai (WH) that experienced expandsion at 0.063-0.144 Ma ago, consistent with the forth warm period.
3. The nucleotide diversity was significantly negative-correlated with the latitude. Genetic diversity showed a positive correlation with varying environmental factors, whereas other index of genetic diversity such as haplotype diversity, expected heterozygosity and observed heterozygosity had statistically non-significant correlation with environmental factors. Such a relationship that the more unstable the climate was, the higher the genetic diversity we observed was, may be caused by wide sampling sites, remarkable climatic differences and high adaptative ability of chukars.
4. The gene flow detected from mtDNA CR is higher than that from micro satellite, indicating that female chukars played a dominating role in population expansion. It thus provided molecular evidence to the assumption that it's the female that spreads out of their natal territories in Phasianidae species.
5. The phylogenetic tree based on the mtDNA CR and the nucleotide diversity of 15 chukar subspecies indicated that chukars might originate from the region of western Himalayas-Pamirs-western Tianshan, which is consistent with the previous conclusion that chukar originated from central Asia based on the plumage features and the subspecies'distribution. On the phylogenetic tree, the 15 chukar subspecies clustered into two subspecies groups, of which the divergence time was about 0.45 Ma (calculated by mtDNA CR genetic distance and MDIV methods) that is consistent with Gablah interglacial period (0.30-0.73 Ma) on the Tibet Plateau or the interglacial period (0.030-0.047 Ma) after the Gaowangfeng Glaciation in late Mid-Pleistocene at the Tianshan Mountains. Thereafter, the climate became cold and dry so that the two groups spreaded out of their original habitats and differentiated separately into the current distribution pattern. The divergence time between 15 subspecies is equivalent to the Gunz-Mindel interglacial (0.30-0.69 Ma) and Mindel-Riss interglacial (0.125-0.20 Ma) at Europe or the third warm period (0.24-0.36 Ma) and the fourth warm period (0.06-0.15 Ma) in China, showing that the chukar is a kind of bird that expanded in glacial but was isolated in interglacial. Both the MP and Bayesian trees constructed by mtDNA CR sequences were same to the 15 subspecies phylogeny tree constructed based on the genetic distance of mtDNA CR.
6. The nucleotide diversity and phylogenetic tree of Chinese chukars supported the idea that Chinese chukars originated from two regions, the western Himalayans-Pamirs and the western Tianshan-Tarbagatay, with the predominant regions concentrated at the arid and semi-arid area of western Tianshan-Tarbagatay in central Asia. Then, they dispersed eastward and formed the subspecies with the same morphological characters.
7. Chinese chukar populations showed no unambiguous phylogeographic structure based on both the mtDNA CR and microsatellite markers. The reasons may be that i) the distributed area of chukars had little or no ice cover during the glacial period; ii) the climate fluctuations had no or little influence on the habitats of chukar during glacial-interglacial of Pleistocene; and iii) the mountains did not form physical barriers to chukar populations. Mantel test based on mtDNA CR and microsatellite suggested that there were no significant positive-correlations between FST/(1-FST) and geographic distances, which showed that the genetic differences were not simply resulted from geographical distances. The Analysis of Molecular Variance (AMOVA) showed that 69.07%(mtDNA CR) and 81.03% (microsatellite) of the total genetic variability were distributed within population.
8. Phylogeographic analysis of intraspecific genetic variation provides valuable information on how to identify management units (MUs) and evolutionarily significant units (ESUs) for endangered species. According to the criteria of MUs and ESUs, we suggest that the chukars who distribute Longdong Loess Plateau, Helanshan Mountains, Qilianshan Mountains and western Tianshan mountains should be treated as ESU, respectively. And the six Chinese chukar subspecies should be treated as separate MUs. As for populations, the populations of Huoerguosi (HEG), Akesai (AKS), Subei (SB), Tongchuan (TC) and Wudu (WD) should be treated as MUs, especially the WD population, because it belongs to the Oriental realm, where the climate is more moderate and humidity than other locations of chukar populations.
1.石鸡mtDNA控制区的碱基含量分别为：T 32.1%、C 27.3%、A 26.4%、G 14.2%,A和C的比例高于G和T的比例,碱基含量显示出一定的偏歧性。在427个样本中共发现127个变异位点,定义了139种单倍型,核苷酸多样性和单倍型多样性分别为0.961和0.0054。8对微卫星位点平均等位基因数为16.875,平均期望杂合度和观察杂合度分别为0.8624和0.7847,表现出较高的遗传多样性。
2.石鸡15亚种及我国石鸡25个地理种群中的大部分都表现出“高单倍型多样性、低核苷酸多样性”的遗传多样性模式。这一遗传多样性模式及mismatch单峰分布特征、Fu's Fs和Tajima's D检验结果都支持我国石鸡及大部分的石鸡种群都经历过种群扩张的历史。红回(HH)、东大山(DSH)、乌海(WH)、武都(WD)和景泰(JT)5个种群的扩张时间发生在0.063-0.144 Ma,即我国北方所处的第四温暖期；其它种群扩张发生在0.027-0.060 Ma之间,即我国北方所处的第五寒冷期。
3.石鸡的遗传多样性中仅有核苷酸多样性与纬度呈显著负相关关系,其它多样性指标(单倍型多样性、观测杂合度与期望杂合度)与各环境因子都没有显著的相关性。石鸡各种群的遗传多样性与各环境因子的变异系数呈现不显著的正相关关系,即在气候不稳定的地区石鸡的遗传多样性反而较高。
4.基于mtDNA控制区计算的石鸡各种群间的基因流高于基于微卫星得出的结果,表明在种群扩散过程中雌性石鸡向外扩散,从而在分子水平上证实了雉科鸟类以雌性为主导的扩散模式。
5.石鸡15个亚种的系统发生树和核苷酸多样性表明石鸡起源于西喜马拉雅山-帕米尔高原-西天山地区,支持了以前基于形态和亚种分布推测石鸡起源于中亚的结论。15个亚种在系统发生树上聚类成两个亚种组,它们的分歧时间大约在45万年前(基于mtDNA控制区遗传距离和MDIV),相当于中更新世晚期青藏高原发生加布拉间冰期(0.30-0.73 Ma)和天山高望峰冰期之后发生的间冰期(0.30-0.47 Ma)。之后,当气候趋向寒冷、干燥时,石鸡分别向外扩散并分歧成与现今形态一致的各亚种。15个亚种间发生分歧的时间相当于欧洲恭兹-民德间冰期(0.30-0.69 Ma)和民德-里斯间冰期(0.125-0.20Ma),以及我国北部的第三(0.24-0.36 Ma)和第四温暖期(0.06-0.15 Ma)发生的时间,表明石鸡是一种冰期扩散、间冰期隔离的物种。MP和贝叶斯树与基于mtDNA控制区遗传距离构建的系统发生树结果一致。
6.分布于我国的石鸡6亚种25种群的核苷酸多样性及亚种的系统发生树表明,我国石鸡起源于两个不同的地区——西喜马拉雅山-帕米尔高原和西天山-塔尔巴哈台地区,其中以起源于新疆部分地区及中亚的干旱半干旱地区即西天山-塔尔巴哈台地区为主。
7.两种分子标记都表明我国石鸡没有明显的系统地理结构,表明我国的石鸡在第四纪冰期-间冰期气候发生剧烈振荡时没有受到太大的影响,各分布区内的山脉也未对它们形成地理屏障。分子变异分析(AMOVA)显示石鸡各地理种群间的遗传差异不显著,但种群内遗传差异极显著(CR序列；FST=0.309,P<0.001；微卫星：FST=0.3093,P<0.001),地理种群内是主要的(CR序列：69.07%；微卫星；81.03%)。Mantel检验结果显示25个种群的FsT/(1-FST)与地理距离间没有显著的相关性(CR序列：r=0.468,P>0.05；微卫星：r=0.15,P>0.05),说明遗传分化不是单纯由地理距离决定的。
8.基于本文的研究结果和可操作性的原则,我们建议分别将分布于陇东黄土高原、贺兰山、祁连山和西天山地区的石鸡作为四个独立的进化显著单元进行管理和保护；我国的6个亚种可以作为6个管理单元进行管理。对种群而言,霍尔果斯(HEG)、阿克塞(AKS)、肃北(SB)、桐川(TC)和武都(WD)种群应被作为独立的管理单元加以管理和保护,尤其是由于WD种群所处的独特的地理位置更应被加以关注。
The chukar (Alectoris chukar) is a kind of widely distributed wildfowls belonging to Aves, Galliformes, Phasianidae, Alectoris whose distribution is throughout Mediter-ranean islands, central Asia and the northeastern of China that. Currently, up to 16 subspecies have been identified. In this study, I addressed the phylogeny of 15 subspecies of chukars based on mitochondrial DNA control region (mtDNA CR), as well as the molecular ecology and phylogeography from 25 populations of five Chinese chukar subspecies based on mtDNA CR and microsatellite markers. The aims of this study are to:(1) explore the origin of chukars by molecular phylogenetic analysis of 15 subspecies of chukar; (2) examine the effects of environmental factors on population genetic diversity of the 25 chukar populations distributed in China; (3) reconstruct the phylogeographic relationship of Chinese chukars under the background of Pleistocene climate oscillation; (4) demonstrate the roles of either sex played in the population expansion, based on both the maternal and bi-parental inherited markers; (5) infer the geological or past demographic events that may probably have determined the current population structures; (6) offer the rational protect proposals of the chukars from the prospective of population genetics. In this study, we obtained mtDNA CR sequences of 427 specimens from 15 chukar subspecies, and sequences of mtDNA CR, as well as eight microsatellite loci, for 288 specimens from 25 Chinese chukar populations. The main results include:
1. The base compositions of mtDNA CR of chukar are T 32.1%, C 27.3%, A 26.4% and G 14.2%. Totally,139 haplotypes were defined by 127 variable sites that were detected in the 427 specimens from 15 chukar subspecies, with the mean haplotype diversity of 0.961 and the nucleotide diversity of 0.0054. The average expected and observed heterozygosity was 0.8624 and 0.7847, implying a relatively high genetic diversity of chukars.
2. The 15 subspecies and 25 Chinese populations of chukars mainly showed the same pattern of "high haplotype diversity while low nucleotide diversity", which, in addition to the unimodal of mismatch distribution and the test of selective neutrality, all indicated that Chinese chukar populations had experienced population expansion at late Pleistocene. Most populations experienced expansion at the metaphase of Late Pleistocene (0.027-0.06 Ma), co-occurring with the fifth cold period, with the exception of populations from Honghui (HH), Wudu (WD), Dongdashan (DSH), Jingtai (JT) and Wuhai (WH) that experienced expandsion at 0.063-0.144 Ma ago, consistent with the forth warm period.
3. The nucleotide diversity was significantly negative-correlated with the latitude. Genetic diversity showed a positive correlation with varying environmental factors, whereas other index of genetic diversity such as haplotype diversity, expected heterozygosity and observed heterozygosity had statistically non-significant correlation with environmental factors. Such a relationship that the more unstable the climate was, the higher the genetic diversity we observed was, may be caused by wide sampling sites, remarkable climatic differences and high adaptative ability of chukars.
4. The gene flow detected from mtDNA CR is higher than that from micro satellite, indicating that female chukars played a dominating role in population expansion. It thus provided molecular evidence to the assumption that it's the female that spreads out of their natal territories in Phasianidae species.
5. The phylogenetic tree based on the mtDNA CR and the nucleotide diversity of 15 chukar subspecies indicated that chukars might originate from the region of western Himalayas-Pamirs-western Tianshan, which is consistent with the previous conclusion that chukar originated from central Asia based on the plumage features and the subspecies'distribution. On the phylogenetic tree, the 15 chukar subspecies clustered into two subspecies groups, of which the divergence time was about 0.45 Ma (calculated by mtDNA CR genetic distance and MDIV methods) that is consistent with Gablah interglacial period (0.30-0.73 Ma) on the Tibet Plateau or the interglacial period (0.030-0.047 Ma) after the Gaowangfeng Glaciation in late Mid-Pleistocene at the Tianshan Mountains. Thereafter, the climate became cold and dry so that the two groups spreaded out of their original habitats and differentiated separately into the current distribution pattern. The divergence time between 15 subspecies is equivalent to the Gunz-Mindel interglacial (0.30-0.69 Ma) and Mindel-Riss interglacial (0.125-0.20 Ma) at Europe or the third warm period (0.24-0.36 Ma) and the fourth warm period (0.06-0.15 Ma) in China, showing that the chukar is a kind of bird that expanded in glacial but was isolated in interglacial. Both the MP and Bayesian trees constructed by mtDNA CR sequences were same to the 15 subspecies phylogeny tree constructed based on the genetic distance of mtDNA CR.
6. The nucleotide diversity and phylogenetic tree of Chinese chukars supported the idea that Chinese chukars originated from two regions, the western Himalayans-Pamirs and the western Tianshan-Tarbagatay, with the predominant regions concentrated at the arid and semi-arid area of western Tianshan-Tarbagatay in central Asia. Then, they dispersed eastward and formed the subspecies with the same morphological characters.
7. Chinese chukar populations showed no unambiguous phylogeographic structure based on both the mtDNA CR and microsatellite markers. The reasons may be that i) the distributed area of chukars had little or no ice cover during the glacial period; ii) the climate fluctuations had no or little influence on the habitats of chukar during glacial-interglacial of Pleistocene; and iii) the mountains did not form physical barriers to chukar populations. Mantel test based on mtDNA CR and microsatellite suggested that there were no significant positive-correlations between FST/(1-FST) and geographic distances, which showed that the genetic differences were not simply resulted from geographical distances. The Analysis of Molecular Variance (AMOVA) showed that 69.07%(mtDNA CR) and 81.03% (microsatellite) of the total genetic variability were distributed within population.
8. Phylogeographic analysis of intraspecific genetic variation provides valuable information on how to identify management units (MUs) and evolutionarily significant units (ESUs) for endangered species. According to the criteria of MUs and ESUs, we suggest that the chukars who distribute Longdong Loess Plateau, Helanshan Mountains, Qilianshan Mountains and western Tianshan mountains should be treated as ESU, respectively. And the six Chinese chukar subspecies should be treated as separate MUs. As for populations, the populations of Huoerguosi (HEG), Akesai (AKS), Subei (SB), Tongchuan (TC) and Wudu (WD) should be treated as MUs, especially the WD population, because it belongs to the Oriental realm, where the climate is more moderate and humidity than other locations of chukar populations.
引文
安蓓.西藏雪鸡种群遗传结构与分子系统地理学研究[博士论文].兰州：兰州大学.2009.
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