Yaks are a unique livestock species in the plateau region, displaying high-altitude adaptation to extreme and harsh environments, including cold and hypoxia (Wiener et al., 2003; Aguiar et al., 2018; Qi et al., 2019). They hold significant importance in local animal husbandry, providing meat, milk, wool, labor, fuel, and other essential resources to the local herdsmen (Wiener et al., 2003). Additionally, yaks serve as a valuable gene bank for genetic studies (Qiu et al., 2012).

The exploration of population genetic structure of yak has become a prominent field in domestic animal. Studies have been conducted on the genetic diversity of yaks using microsatellites and mitochondrial DNA (Qiu et al., 2015; Wang et al., 2021; Hameed et al., 2022; Ma et al., 2022). Moreover, the assembly and publication of the first yak reference genome in 2012, followed by subsequent improvements, have resulted in a highly complete and accurate yak reference genome at the chromosome level (Qiu et al., 2012; Ji et al., 2021; Zhang et al., 2021). This achievement has laid a robust foundation for investigating genetic variation at the whole-genome level in yaks, leading to the widespread use of whole-genome resequencing technology. This technology has enabled analyses of genetic variation in yaks, covering aspects such as their origin, domestication (Medugorac et al., 2017; Chai et al., 2020; Meng et al., 2022), genetic diversity and structure (Wang et al., 2014; Zhang et al., 2016; Lan et al., 2018; Wang et al., 2019; Li et al., 2022), high-altitude adaptation (Qiu et al., 2012; Qiu et al., 2015; Guang Xin et al., 2019b; Lan et al., 2021; Gao et al., 2022) and selection pressures (Lan et al., 2018; Xie et al., 2018; Guang Xin et al., 2019a; Li et al., 2022).

Southwestern China, specifically Sichuan Province’s Garze Tibetan Autonomous Prefecture, Aba Tibetan and Qiang Autonomous Prefecture, and Yunnan Province’s Diqing Tibetan Autonomous Prefecture, serves as the primary production area for yaks (Lan et al., 2018). In this region, several yak breeds, including Jiulong yak, Maiwa yak, Muli yak, Jinchuan yak, Changtai yak, and Zhongdian yak, have been officially recognized as excellent indigenous breeds by the government (Lan et al., 2021). Each of these yak breeds possesses unique characteristics and outstanding traits. For example, the Jinchuan yak stands out with approximately 52% of individuals having 15 thoracic vertebrae and 15 pairs of ribs, one more thoracic vertebra and one more pair of ribs than other yak breeds (Lan et al., 2018). Additionally, multi-ribbed Jinchuan yaks demonstrate higher meat and milk production, as well as superior reproductive performance compared to other breeds (Mipam et al., 2012). Maiwa yaks, on the other hand, produce milk with a protein content 40%–60% higher than that of native bovine milk (Chen et al., 2021). Protecting, developing, and utilizing the genetic resources of yak populations in this region holds great significance for the advancement of China’s yak industry. However, comprehensive studies on genetic variation detection, and selection signal analysis at the whole-genome level for multiple yak breeds in this region remain unreported.

To address the genetic gap, this study detected genetic variation, elucidate the genetic diversity, explore population genetic structure and genome-wide selection using six yak populations including four from Sichuan (Maiwa yak, Muli yak, Jinchuan yak, and Changtai yak), one from Yunnan (Zhongdian yak), and a collection of Tibetan yak populations. Our findings provide a scientific and theoretical basis for the protection, development, and genetic improvement of yak genetic resources in Tibet and southwestern China.

Genetic diversity reflects the adaptability of a population to its environment and its evolutionary history. It holds significant value for the protection and further utilization of animal genetic resources. In this study, we observed that the nucleotide diversity of Tibetan yak is low, likely due to their isolated geographical location, leading to limited genetic interchange with other populations. Chai et al. (2020) classeified 91 domestic yaks from 31 populations into three groups based on their phylogenetic relationships.They noted that the nucleotide diversity and genetic diversity of the yak population in the central Tibetan region were both low, aligning with our study results.

The observed heterozygosity (Ho) of Muli yak, Jinchuan yak, and Changtai yak was higher than the expected heterozygosity, and the inbreeding coefficient was generally lower. This suggests that these populations abundant exhibit genetic diversity and a low degree of inbreeding. This may be attributed to the large-scale purebred breeding and hybrid improvement efforts carried out on yaks in Sichuan in recent years. As a result of this work, several yak varieties have been developed for breeding populations and core breeding groups. On the other hand, the observed heterozygosity of Tibetan yak was low, while the inbreeding coefficient was high. This suggests a lack of genetic diversity, possibly due to the traditional feeding practices in the region that have led to significant inbreeding and a decline in reproductive performance. The LD decay analysis results indicated that Muli yak, Jinchuan yak, and Changtai yak have experienced more intense artificial selection in recent years, as evidenced by their slower LD decay rate. as evidenced by their slower LD decay rate. In contrast, Tibetan yak exhibited a faster LD decay compared to other populations, indicating less human intervention. This aligns with previous LD decay analysis results for Jinchuan yak and Tibetan yak (Wang et al., 2020).

In previous studies, Lan et al. (2018) investigated the population genetic structure of Jinchuan yaks at the whole-genome level. The results from phylogenetic tree and PCA analysis both indicated that Jinchuan yaks form an independent branch within the domestic yak population and are distantly related to Zhongdian yak, Tibetan yak, and Qinghai yak. Additionally, the ancestral component analysis results revealed that when K = 3, the Jinchuan yak population was separated from the rest of the domestic yak population. In the present study, the ancestral component analysis, PCA analysis, and F _ST statistics results of the six yak populations all pointed towards Muli yak exhibiting a relatively independent population genetic structure and distant relationship with other yak populations. Most of the Maiwa yak showed a high degree of hybridization, characterized by the smallest average differentiation index and a complex genetic background. This genetic variation is likely influenced by the diverse geographical environment of the two primary yak breeding regions. Muli yak and Maiwa yak are classified as the “Hengduan Mountains type” and “Qinghai-Tibet Plateau type,” respectively, based on their ecological characteristics. Muli yak predominantly inhabits mountain valleys, leading to grassland fragmentation and restricted gene flow, resulting in isolated breeding populations with. artificial selection. Conversely, Maiwa yak is primarily found in high-altitude terrains with espansive grasslands, where primitive year-round grazing is common, leading to a lower degree of artificial selection. It is speculated that the Maiwa yak population in this study may have originated from two distinct large populations due to the establishment of a core breeding group for Maiwa yak and the implementation of various effective breeding practices. One population may have introduced Jinchuan and Changtai yak bloodlines, while the other population retained a relatively pure genetic lineage without external influences.

The identification of selective signatures in a population is crucial for understanding its evolutionary history and economic traits. A total of 187 candidate positively selected genes were identified in the Maiwa yak population, and their potential effects on relevant important traits were discussed. For example, the CLDN1 gene, a component of endothelial tight junctions, has been demonstrated to decrease intestinal permeability and improve immune adaptability in calves through the upregulation of its expression (Ghaffari et al., 2021). It also plays an effective role in repairing the rumen epithelial barrier of slow-growing yaks (Hu et al., 2019). Thus, the CLDN1 gene may be associated with the stronger gastrointestinal immune function of Maiwa yaks, enabling them to adapt to the challenging high-altitude wetland grassland environment. The GNB4 gene can control cattle growth by influencing the expression of growth-related hormones in the pituitary gland (Lu et al., 2020). The HMGA2 gene, a transcription factor of insulin-like growth factor gene 2 (IGF2), plays a significant role in the growth trait of navel length in beef cattle (Aguiar et al., 2018). Similarly, the TRPS1 gene is significantly associated with the increase in both cattle body weight and eye muscle area (Lee et al., 2011). Therefore, the GNB4, HMGA2, and TRPS1 genes are likely to be closely associated with the growth and development of Maiwa yak.

This study also identified several genes that are specifically associated with reproduction. For instance, PI4KB is responsible for regulating actin aggregation during sperm capacitation (Etkovitz et al., 2007). DYNC1I1 participates in transporting molecules and organelles during oocyte maturation and is the most prevalent transport system in cells (Racedo et al., 2008). GRIP1 has been validated as a marker for detecting cow estrus (Hlaing et al., 2001; Lee et al., 2017). CARPT is a novel regulatory factor for ovarian function during follicular wave emergence in cows and is thought to play a potential role in dominant follicle selection during the follicular wave period in single-ovulating species as an “ovulation quota gatekeeper” (Mihm et al., 2000; Lv et al., 2009; Smith et al., 2010). These genes may have an impact on maintaining a stable reproductive pattern of Maiwa yak in the harsh high-altitude environments.

The challenging high-altitude environment and extensive productionpractices have resulted in the strong selection of genes associated with immunity and adaptation to hypoxia in the genome of Maiwa yak. For example, the reduction of the CD200 gene has a significantly affects on the quantity of pulmonary epithelial cells in radiation conditions (Beach et al., 2023). This finding might elucidate the relevant mechanism that enables the Maiwa yak to adapt to high-altitude with intense radiation and maintain lung function without harm. The IL1RAP gene has been identified as a central gene encoding the interleukin-1 receptor accessory protein, which plays a significant role in the immune system (Dos Santos Silva et al., 2019). Furthermore, three genes, NDUFB6, PRKN, and MRPS9, are closely linked to mitochondrial structure and normal function (Buggiotti et al., 2021; Fang et al., 2022; Zhang et al., 2022). Their influence on respiratory and energy metabolism efficiency may be be associated with Maiwa yak’s adaptation to high-altitude hypoxic environments.

In addition, this study identified lactation-related genes SNX13 and CPM among the selected genes of Maiwa yak. The SNX13 gene is highly correlated with milk production traits in cows, while the CPM gene has a significant effect on the fatty acid content in cow milk (Rincón et al., 2009; Shi et al., 2020). The SUCLG2 gene has been identified as a candidate biomarker for beef tenderness in cattle (Li and Li, 2021).

Three keratin family genes, KRT24, KRT25, and KRT26, have been identified. The KRT24 gene play a crucial role in hair growth and follicle development in yaks (Bao et al., 2022). The long and dense wool of Maiwa yak helps them retain heat and withstand cold weather at high altitudes. It is worth noting that a pigment deposition-related gene, Additionally, an OCA2 gene related to pigment deposition has been identified, potentially influencing black pigment deposition in Maiwa yak’s wool (Grønskov et al., 2007; Caduff et al., 2017; Ballan et al., 2022).

In conclusion, this study systematically investigates the genetic diversity, population genetic structure, kinship relationships, genetic differentiation, and gene selection of several yak breeds (populations) in Tibet and southwestern China at the whole-genome level. Overall, all six populations exhibit rich genetic diversity. Muli yak shows higher differentiation from other yak populations and forms an independent cluster. The Maiwa yak population demonstrates a complex genetic structure. The candidate genes identified for Maiwa yak are associated with various functions such as growth, reproduction, immunity, lactation, hypoxia adaptation, hair development, meat quality, digestion and absorption, and pigment deposition. These findings provide a scientific and theoretical foundation for the exploration and conservation of yak genetic resources in this region, as well as for the selection and breeding of yak breeds.