Yak Domestication And Adaptation: Evidence From Mitochondrial Genome

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.