Complex genomic ancestry in southern regions and drivers of continental-level genetic diversity in the wolves of Asia

Gray wolves ( Canis lupus ) in Asia encompass most of the species’ global genetic diversity and many endangered populations. However, a clear understanding of the evolutionary history of wolves from many parts of Asia, especially southern regions, is lacking. We used 98 whole genomes of wolves sampled across Eurasia to better resolve their evolutionary history by investigating phylogenetic and gene flow histories across the genome, and to characterize their demographic history and genetic diversity. The strongest barriers to gene flow coincided with boundaries separating the three major extant wolf lineages - Indian, Tibetan, and Holarctic. Wolves in the central Asian mountain ranges belonged to the Holarctic lineage, and despite their geographic adjacency only share minimal ancestry with the Tibetan lineage. In contrast, wolves from eastern Asia share population-wide ancestry with the Tibetan lineage, which may reflect an unsampled lineage similar, but not exactly to, the modern-day Tibetan lineage. Wolves from southwestern Asia also share population-wide ancestry with the Indian lineage, likely due to old (>6kya) admixture events. Long-term historical declines over the last 100,000 years, geographic isolation, and recent inbreeding have resulted in the Indian and Tibetan wolves having some of the lowest levels of genetic diversity and highest realized genetic loads. In contrast, adjacent populations exhibit some of the highest genetic diversity, due in part to admixture along contact zones. Our study illustrates how using multiple approaches that consider heterogenous signals across the genome can more fully resolve the historical and contemporary processes that have led to present-day species’ diversity.