Cattle Genomics: Aurochs Admixture in East Asia

The genetic origins and dispersal of domesticated cattle, in common with other livestock species, is getting increasingly complex the closer we look [1, 2]. This trend has accelerated over the last decade, particularly through comparative analyses of whole-genome sequence (WGS) data sets (paleogenomes) generated using ancient DNA (aDNA) from the extinct wild aurochs (Bos primigenius), the progenitor of modern cattle populations [3-7]. These and other high-resolution population genomics studies of domestic cattle have led to a reappraisal of simple models for understanding cattle genetic origins, domestication, and diversity, which developed from the first surveys of maternally inherited mitochondrial DNA (mtDNA) in modern and ancient cattle [8-10]. In a similar fashion to our more nuanced understanding of recent human evolution and the evidence for gene flow from archaic hominins [11], it is now clear that nuclear genomic introgression from wild aurochsen populations during the Holocene has had a significant impact on the ancestry of modern cattle breeds. The rich landscape of cattle genetic and phenotypic diversity across the globe does not derive solely from the small number of domestication centres in Southwest Asia that gave rise to modern humpless taurine (Bos taurus), humped indicine (Bos indicus), and B. taurus × B. indicus hybrid populations.

Recently published work from Jiawen Hou and her colleagues provides important new insights into the biogeography of B. primigenius and adds to the growing body of evidence for aurochs admixture in East Asian cattle [12]. Bovine archeological material representing 59 specimens collected from the Songnen Plain in Northeast China and from the Qinghai–Tibet Plateau (QTP), was used to generate paleogenomic data for 16 different aurochsen, which were radiocarbon dated to between 3.7 and 37.0 kya (thousand years ago). These data sets were integrated with previously published paleogenomes from 74 ancient wild and domestic cattle [6, 7, 13] plus WGS data from almost 200 modern cattle (taurine, indicine, and hybrid) and related species. Mitochondrial genomic diversity and phylogeography was also examined using more than 200 mitogenomes from ancient and modern cattle and several outgroup species.

Comparative phylogenetic analysis of the East Asian aurochs mitogenomes revealed that the mtDNA haplotypes possessed by all 16 Songnen Plain and QTP aurochsen are representative of the “C” haplogroup, which is an outgroup (with the K haplogroup) to all non-indicine B. primigenius haplogroups (P, Q, R, and T), splitting from these other mtDNA lineages approximately 150 kya. Hou et al. propose that this observation, coupled with a comparable nuclear genomic divergence, provides support for the taxonomic classification of the East Asian aurochs as a subspecies of B. primigenius: B. p. sinensis, which fits into an expanded taxonomy encompassing West Eurasian aurochs, B. p. primigenius; North African aurochs, B. p. opisthonomus; and South Asian aurochs, B. p. namadicus—the likely progenitor of B. indicus domestic cattle. It is important to note, however, that this taxonomy is largely based on fossil evidence and is likely to be substantially revised as paleogenomic data for aurochs are assembled from across these regions.

Although the WGS data generated from the 16 East Asian aurochs specimens provided relatively modest genome coverage ranging from less than 0.01 × to 1.57 ×, consensus data sets of at least two million single-nucleotide polymorphisms (SNPs) were available for most of the high-resolution population genomics analyses focused on the nuclear genome. The most notable result from this work was the observation that the East Asian aurochs has contributed to the genomic ancestry of domestic cattle populations in the region, mirroring observations in other parts of Eurasia that, taken together, provide a new perspective on post-domestication interactions between wild aurochs and human-managed cattle [5-7]. For example, East Asian aurochs from the Holocene showed genetic affinities with ancient domestic cattle, contributing approximately 7% genomic ancestry with animals dated to 3.9 kya from the late Neolithic Shimao site in Shaanxi Province. This result supports the hypothesis that gene flow between domestic and wild populations happened in northern China by 4 kya [3, 13, 14]. Additional analyses of gene flow and admixture, which also encompassed an earlier study of three Bos individuals excavated on the QTP and dated to the middle of the fourth millennium BP [3], provided multiple lines of statistical evidence for substantial aurochs ancestry in modern QTP cattle breeds (Changdu, Dingjie, Diqing, and Yushu). This was demonstrated through complementary approaches including tests of shared genetic drift, phylogenetic network analysis, formal tests of admixture, and model-based ancestry estimation. Together, these analyses indicate that introgression from East Asian aurochs began soon after domestic cattle migrated eastward from Southwest Asia. Figure 1 provides a simplified illustration of current knowledge of aurochs taxonomy and nuclear and mitochondrial genomic diversity in aurochs populations across Europe, North Africa, and Asia during the early Holocene [3, 4, 7, 12].

The extent and dynamics of the admixture processes between East Asian aurochsen and domestic cattle on the QTP and elsewhere in East Asia will become better understood as paleogenomic data from wild and domestic cattle accumulates during the coming years. Models of introgression that involve sex-biased gene flow (e.g., predominantly male-mediated aurochs input) can be tested using Y chromosome haplotypes and, at a more fine-grained level, using comparative analyses of X and autosome chromosomal ancestry [15]. In addition, preliminary analyses of introgressed SNP alleles performed by Hou and colleagues identified East Asian aurochs gene variants associated with immunobiology, neurobiology and metabolism. However, these functional population genomics studies of aurochs admixture can ultimately be extended to parallel work in other livestock and companion animal species that has uncovered introgressed genes and genomic regulatory elements (GREs) from wild congeners that impacts many important traits, including resistance to infectious disease and adaptation to specific environmental conditions such as high altitude and low oxygen levels [16-20]. Understanding the roles of introgressed aurochs gene and GRE variants in the genomic architecture of these adaptive traits in domestic cattle will be important for future breeding programs that leverage genomic selection and gene editing [21].

James A. Ward: writing–original draft, writing–review and editing, conceptualization, visualization. David E. MacHugh: conceptualization, writing–original draft, funding acquisition, visualization, writing–review and editing, project administration, resources, supervision.

The authors declare no conflicts of interest.