牦牛驯化和适应：线粒体基因组证据
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摘要
动物的驯化促使人类从狩猎生活模式向放牧生活模式转变。驯化的动物为人类提供稳定的动物蛋白来源和许多附属产品,促进了人类文明的发展。家养牦牛(Bos grunniens)是青藏高原地区最重要的家畜之一,它们为当地人民提供重要的生产生活资料,比如食物、皮毛、粪便做成的燃料以及运输工具等。家养牦牛的驯化起源于当地的野牦牛。目前青藏高原地区存在的野牦牛数量大约为15000头。这些野生个体为研究家养牦牛的驯化历史、驯化对牦牛所受选择压力的影响提供了一个良好的机会。此外,由于牦牛这一物种对青藏高原地区的高海拔环境有很好的适应,其适应的遗传学机制逐渐引起人们的关注。
本文分析了405头家养牦牛以及47头野牦牛的线粒体D-loop序列,其中96个家养牦牛个体以及34个野牦牛个体的序列是测序得到的,其余序列来自Genbank,并进一步对48头家养牦牛和21头野牦牛进行线粒体全基因组测序,然后结合Genbank中的3条家养牦牛线粒体基因组序列进行谱系地理学分析。对序列的遗传多样性分析表明野牦牛的单倍型多样性以及核苷酸多样性都高于家养牦牛。在所有的D-loop序列中共发现123种单倍型。基于D-loop数据以及线粒体全基因组数据的系统发育分析都检测到三个高度分化的遗传分支,其中两大主要分支在家养牦牛和野牦牛中都有分布,第三个分支包含的个体数较少,只分布在野牦牛居群之中。在家养牦牛中,检测到6个单倍型组,这些单倍型组在牦牛的各个形态学类群、各个分布地区都有分布。此外,对牦牛居群D-loop序列的AMOVA分析(analysis of molecular variance)表明,家养牦牛中93.91%的变异分布在居群内部,5.46%的变异分布于居群之间,只有0.64%的变异分布于地区之间,这一结果表明家养牦牛中没有明显的谱系地理结构。基于线粒体基因组数据,对牦牛种内三大分支的分化时间作了估计,结果显示,三大分支的分化时间在420000年到580000年之间,这一结果与青藏高原地区的第四纪冰期事件发生的时间相吻合。冰期气候可能驱使野牦牛到不同的避难所,从而引起牦牛的异域分化,在冰期结束后,由于避难所环境的不适宜,野牦牛经过迁移又聚合在一起,形成一个大的基因库。在全新世阶段,人类对这一基因库中的部分野牦牛进行驯化,导致两大主要分支的遗传资源在家养牦牛中分布,而第三分支中的野生个体没有被驯化,在家养牦牛居群中没有分布。
野牦牛生活在青藏高原的高海拔地区,为了寻找食物、配偶以及逃避天敌等活动的需要,其代谢效率要维持在一个高的水平,与之相反,驯化后家养牦牛的生活环境发生了大的变化,其运动能力下降,因此家养牦牛的代谢效率较低。由于线粒体变异对选择压力十分敏感,因此驯化可能会导致家养牦牛线粒体基因组所受选择压力减小。为了验证这一设想,分析了51头家养牦牛和21头野牦牛的线粒体蛋白编码序列,发现家养牦牛分支的非同义突变比率显著地高于野牦牛分支。这一结果表明尽管家养牦牛的驯化历史较短,但是驯化仍然导致了家养牦牛线粒体所受选择压力的减小。此外,驯化过程中的瓶颈效应也会促进非同义突变在家养牦牛中的增加。选择压力的变化以及瓶颈效应可能还会影响家养牦牛的核基因组,这就会导致家养牦牛基因组上非同义突变的快速积累,从而产生新的功能的遗传多样性。这些新的功能突变为人工选择提供了更多的素材,使得更多品种的培育成为可能。
牦牛长期生活在高海拔的青藏高原,对当地的环境,比如低氧、低温、强紫外线等,有很好的适应,但是这种适应的遗传学证据并不是很充分。比较了17头野牦牛和32头北美野牛的线粒体基因组蛋白编码序列,发现在牦牛线粒体蛋白跨膜螺旋区域中存在苏氨酸残基的增加。苏氨酸残基在形成氢键从而增强螺旋一螺旋作用这一过程中起到至关重要的作用,因此苏氨酸残基的增加可能会增强线粒体蛋白的稳定性,从而提高氧的结合效率以及氧化呼吸效率,对高海拔环境是一种适应。
The domestication of animals has played an important role in the transition from hunter organization to nomadic pastoralism in human history. As one of the most important domesticated species in the Qinghai-Tibetan Plateau (QTP), the yak (Bos grunniens) provides the most important resources (e.g. food, hides, dung fuel and transport power) for local people. The present domestic yaks are descended from wild yaks. Currently there are around 15,000 wild yaks roaming on the Plateau. These wild individuals provide unique opportunities, unavailable for most other domestic animals, to elucidate the domestication process of domestic yaks, and to investigate the selective constraints on domestic yaks after domestication. Furthermore, as the yaks thrive in the harsh environment on the QTP, it is interesting to trace the genetic signatures for such a high-altitude adaptation.
All available D-loop sequences for 405 domesticated yaks and 47 wild yaks were examined, including new sequences from 96 domestic and 34 wild yaks. We further sequenced the complete mitochondrial genomes of 48 domesticated and 21 wild yaks. Meanwhile, three complete mitochondrial sequences of domestic yaks were downloaded from Genbank. Phylogeographic analyses were performed using the mitochondrial D-loop and the total genome datasets. The genetic diversity of wild yaks is higher than that of domestic ones. We recovered a total of 123 haplotypes based on the D-loop sequences in wild and domestic yaks. Phylogenetic analyses of this dataset and the mitochondrial genome data suggested three well-supported and divergent lineages. Two lineages with six D-loop haplogroups were recovered for all morphological breeds of domestic yaks across their distributions in the QTP, while one more lineage and more endemic haplogroups or haplotypes were found for wild yaks. Analysis of molecular variance (AMOVA) of the D-loop haplotypes suggested that within domestic yaks, most of the total variances (93.91%) were attributed within populations and 5.46% among populations, with a very small percentage (0.64%) among regions. These results reflected that the phylogeographic structure was weak among domestic populations. Based on the mitochondrial genome data, the divergences of the three lineages were estimated to have occurred around 420,000 and 580,000 years ago, consistent with the geological records of two large glaciation events experienced in the QTP. Three differentiated lineages of yaks probably evolved allopatrically in different regions during the Pleistocene glaciation events, then reunited into a single gene pool during post-glacial population expansion and migrations before the start of the domestication of yaks in the Holocene. Domestication from this gene pool led to the presence of two divergent lineages within domestic yaks, although a third remote lineage remained undomesticated.
Wild yaks roam the central QTP and move very rapidly because they have to seek food and mates, and also escape from hunters; therefore, they have to maintain high metabolic efficiency. However, the living conditions of domestic yaks have changed dramatically after domestication. Domestic yaks do not require such high efficiency because of their limited activity. Hence, domestication may have caused the relaxation of selective constraints on the yak mitochondrial genome because mitochondrial mutations are extremely sensitive to energy-related selective pressures. We have tested this hypothesis by analyzing the mitochondrial genomes of 51 domestic yaks and 21 wild yaks. The results show that the ratio of nonsynonymous/synonymous substitutions in mitochondrial protein-coding genes is significantly higher in domestic yak lineages than those of wild yaks. This genetic difference suggests that the relaxation of selective constraints following the domestication in addition to bottlenecks has allowed faster accumulation of non-silent substitutions in the yak mitochondrial genome, despite its short domestication history. If this change also affected other parts of the yak genome, it could have facilitated the generation of novel functional genetic diversity. This diversity could thus have contributed raw material upon which artificial selection could act in attempts to breed more phenotypic varieties, as in other domesticated animals.
In addition, the yaks have well adapted to the high altitude conditions, such as: hypoxia, low temperature and high solar radiation. It is a good model to study the adaptation of animals to the high altitudes. In order to trace such genetic signatures in yaks, we compared the mitochondrial sequences of 17 wild yaks and 34 bison. Our analyses indicate that in the yak lineage there is a remarkable increase in threonine (Thr) residues in the transmembrane regions of mitochondrial proteins. Because crucial roles of Thr in membrane proteins have been proposed to be the formation of hydrogen bonds enhancing helix-helix interactions, the Thr increase detected in yaks might be adaptive by serving to reinforce stability of mitochondrial proteins in the inner membrane. This Thr increase may enhance the efficiency of oxygen utilization and oxidative phosphorylation.
本文分析了405头家养牦牛以及47头野牦牛的线粒体D-loop序列,其中96个家养牦牛个体以及34个野牦牛个体的序列是测序得到的,其余序列来自Genbank,并进一步对48头家养牦牛和21头野牦牛进行线粒体全基因组测序,然后结合Genbank中的3条家养牦牛线粒体基因组序列进行谱系地理学分析。对序列的遗传多样性分析表明野牦牛的单倍型多样性以及核苷酸多样性都高于家养牦牛。在所有的D-loop序列中共发现123种单倍型。基于D-loop数据以及线粒体全基因组数据的系统发育分析都检测到三个高度分化的遗传分支,其中两大主要分支在家养牦牛和野牦牛中都有分布,第三个分支包含的个体数较少,只分布在野牦牛居群之中。在家养牦牛中,检测到6个单倍型组,这些单倍型组在牦牛的各个形态学类群、各个分布地区都有分布。此外,对牦牛居群D-loop序列的AMOVA分析(analysis of molecular variance)表明,家养牦牛中93.91%的变异分布在居群内部,5.46%的变异分布于居群之间,只有0.64%的变异分布于地区之间,这一结果表明家养牦牛中没有明显的谱系地理结构。基于线粒体基因组数据,对牦牛种内三大分支的分化时间作了估计,结果显示,三大分支的分化时间在420000年到580000年之间,这一结果与青藏高原地区的第四纪冰期事件发生的时间相吻合。冰期气候可能驱使野牦牛到不同的避难所,从而引起牦牛的异域分化,在冰期结束后,由于避难所环境的不适宜,野牦牛经过迁移又聚合在一起,形成一个大的基因库。在全新世阶段,人类对这一基因库中的部分野牦牛进行驯化,导致两大主要分支的遗传资源在家养牦牛中分布,而第三分支中的野生个体没有被驯化,在家养牦牛居群中没有分布。
野牦牛生活在青藏高原的高海拔地区,为了寻找食物、配偶以及逃避天敌等活动的需要,其代谢效率要维持在一个高的水平,与之相反,驯化后家养牦牛的生活环境发生了大的变化,其运动能力下降,因此家养牦牛的代谢效率较低。由于线粒体变异对选择压力十分敏感,因此驯化可能会导致家养牦牛线粒体基因组所受选择压力减小。为了验证这一设想,分析了51头家养牦牛和21头野牦牛的线粒体蛋白编码序列,发现家养牦牛分支的非同义突变比率显著地高于野牦牛分支。这一结果表明尽管家养牦牛的驯化历史较短,但是驯化仍然导致了家养牦牛线粒体所受选择压力的减小。此外,驯化过程中的瓶颈效应也会促进非同义突变在家养牦牛中的增加。选择压力的变化以及瓶颈效应可能还会影响家养牦牛的核基因组,这就会导致家养牦牛基因组上非同义突变的快速积累,从而产生新的功能的遗传多样性。这些新的功能突变为人工选择提供了更多的素材,使得更多品种的培育成为可能。
牦牛长期生活在高海拔的青藏高原,对当地的环境,比如低氧、低温、强紫外线等,有很好的适应,但是这种适应的遗传学证据并不是很充分。比较了17头野牦牛和32头北美野牛的线粒体基因组蛋白编码序列,发现在牦牛线粒体蛋白跨膜螺旋区域中存在苏氨酸残基的增加。苏氨酸残基在形成氢键从而增强螺旋一螺旋作用这一过程中起到至关重要的作用,因此苏氨酸残基的增加可能会增强线粒体蛋白的稳定性,从而提高氧的结合效率以及氧化呼吸效率,对高海拔环境是一种适应。
The domestication of animals has played an important role in the transition from hunter organization to nomadic pastoralism in human history. As one of the most important domesticated species in the Qinghai-Tibetan Plateau (QTP), the yak (Bos grunniens) provides the most important resources (e.g. food, hides, dung fuel and transport power) for local people. The present domestic yaks are descended from wild yaks. Currently there are around 15,000 wild yaks roaming on the Plateau. These wild individuals provide unique opportunities, unavailable for most other domestic animals, to elucidate the domestication process of domestic yaks, and to investigate the selective constraints on domestic yaks after domestication. Furthermore, as the yaks thrive in the harsh environment on the QTP, it is interesting to trace the genetic signatures for such a high-altitude adaptation.
All available D-loop sequences for 405 domesticated yaks and 47 wild yaks were examined, including new sequences from 96 domestic and 34 wild yaks. We further sequenced the complete mitochondrial genomes of 48 domesticated and 21 wild yaks. Meanwhile, three complete mitochondrial sequences of domestic yaks were downloaded from Genbank. Phylogeographic analyses were performed using the mitochondrial D-loop and the total genome datasets. The genetic diversity of wild yaks is higher than that of domestic ones. We recovered a total of 123 haplotypes based on the D-loop sequences in wild and domestic yaks. Phylogenetic analyses of this dataset and the mitochondrial genome data suggested three well-supported and divergent lineages. Two lineages with six D-loop haplogroups were recovered for all morphological breeds of domestic yaks across their distributions in the QTP, while one more lineage and more endemic haplogroups or haplotypes were found for wild yaks. Analysis of molecular variance (AMOVA) of the D-loop haplotypes suggested that within domestic yaks, most of the total variances (93.91%) were attributed within populations and 5.46% among populations, with a very small percentage (0.64%) among regions. These results reflected that the phylogeographic structure was weak among domestic populations. Based on the mitochondrial genome data, the divergences of the three lineages were estimated to have occurred around 420,000 and 580,000 years ago, consistent with the geological records of two large glaciation events experienced in the QTP. Three differentiated lineages of yaks probably evolved allopatrically in different regions during the Pleistocene glaciation events, then reunited into a single gene pool during post-glacial population expansion and migrations before the start of the domestication of yaks in the Holocene. Domestication from this gene pool led to the presence of two divergent lineages within domestic yaks, although a third remote lineage remained undomesticated.
Wild yaks roam the central QTP and move very rapidly because they have to seek food and mates, and also escape from hunters; therefore, they have to maintain high metabolic efficiency. However, the living conditions of domestic yaks have changed dramatically after domestication. Domestic yaks do not require such high efficiency because of their limited activity. Hence, domestication may have caused the relaxation of selective constraints on the yak mitochondrial genome because mitochondrial mutations are extremely sensitive to energy-related selective pressures. We have tested this hypothesis by analyzing the mitochondrial genomes of 51 domestic yaks and 21 wild yaks. The results show that the ratio of nonsynonymous/synonymous substitutions in mitochondrial protein-coding genes is significantly higher in domestic yak lineages than those of wild yaks. This genetic difference suggests that the relaxation of selective constraints following the domestication in addition to bottlenecks has allowed faster accumulation of non-silent substitutions in the yak mitochondrial genome, despite its short domestication history. If this change also affected other parts of the yak genome, it could have facilitated the generation of novel functional genetic diversity. This diversity could thus have contributed raw material upon which artificial selection could act in attempts to breed more phenotypic varieties, as in other domesticated animals.
In addition, the yaks have well adapted to the high altitude conditions, such as: hypoxia, low temperature and high solar radiation. It is a good model to study the adaptation of animals to the high altitudes. In order to trace such genetic signatures in yaks, we compared the mitochondrial sequences of 17 wild yaks and 34 bison. Our analyses indicate that in the yak lineage there is a remarkable increase in threonine (Thr) residues in the transmembrane regions of mitochondrial proteins. Because crucial roles of Thr in membrane proteins have been proposed to be the formation of hydrogen bonds enhancing helix-helix interactions, the Thr increase detected in yaks might be adaptive by serving to reinforce stability of mitochondrial proteins in the inner membrane. This Thr increase may enhance the efficiency of oxygen utilization and oxidative phosphorylation.
引文
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