Whole-genome sequencing revealed local genetic differences and multi-layered genetic structure in brown bear (Ursus arctos) populations

Abstract

A multi-layered genetic structure shaped by multiple demographic events across different time periods has been well documented in some species. However, evaluating this pattern remains challenging in many wide-ranging wildlife because genome-wide datasets with broad geographic coverage are still scarce. Brown bears are genetically differentiated among regional populations, but the genomic data are still limited and the demographic events remain incompletely understood. Here, we generated whole-genome resequencing data from brown bears in Asian local populations previously reported to show significant variation and combined these data with ancient samples for population genomic analyses. Our results support previously reported demographic events, such as the early divergence of Central Asian populations. Furthermore, we found genetic differences among Asian brown bear populations, suggesting that population-specific demographic histories occurring at different times have contributed to their unique genetic characteristics. In the Central and West Asian populations, divergence times estimated from autosomal genomes differed by hundreds of thousands of years from those inferred from mitochondrial DNA and Y-chromosomal DNA haplotypes, suggesting that gene flow continued after regional dispersal. In addition, the Y-chromosomal phylogeny and f4 statistics indicated genetic differentiation between the Kazakhstan and Tibetan populations, likely resulting from male-biased introgression into the Tibetan population. Finaly, the Hokkaido and Etorofu (Iturup) populations retained alleles derived from hybridization with polar bears, likely due to the limited impact of post-LGM population expansion. These findings indicate that the genetic variation among brown bear populations is shaped by multiple demographic events occurring at different times, resulting in a multi-layered genetic structure. Significance StatementMulti-layered genetic structure is well known in some species, but remains poorly understood in wild species due to limited genomic data. In this study, we newly sequenced nine brown bears in Asia which included bears that genome data in their area is unreported. By combining these with modern and ancient genomes, we conducted population genomic analyses to characterize local genetic variation and detect hybridization with related species such as the polar bear. We identified (1) substantial divergence time gaps in Central and West Asian populations between autosomal genomes and mitochondrial and Y-chromosomal haplotypes, (2) male-biased introgression into the Tibetan population, and (3) limited impact of recent expansion between island and Eurasian continental populations. These findings suggest that the genetic structure of the populations has been shaped by multiple demographic events at different times, resulting in a multi-layered genetic structure and providing new insights into how wildlife genetic diversity is shaped.