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

A multi-layered genetic structure reflecting multiple demographic events across different time periods has been well documented particularly in modern humans. However, it is still unknown in wild species because of a lack of comprehensive genome-wide data on a global scale. The brown bear exhibits a clear discrepancy between mitogenome- and nuclear genomebased phylogenetic trees. A previous study suggested that this discrepancy was caused by incomplete lineage sorting of the mitochondrial DNA lineages or recent expansion erasing the former genetic structure of the nuclear genome; however, neither scenario fully explained the discrepancy because genetic variation was observed across their habitat at different times. We performed whole-genome resequencing on brown bears from local populations around or on the Eurasian continent. The ancestral genetic characteristics have persisted in Western Asia and Central Asia where minor mitochondrial haplotypes have been reported, whereas individuals from these areas shared few alleles with individuals speculated to possess many alleles from recent dispersal, which suggested that the recent ancestors of these populations had not experienced complete isolation from other populations. The Hokkaido and Etorofu (Iturup) Island populations obtained many alleles via gene flow from the polar bear; this finding was similar to that of a North American brown bear population previously reported hybridization with polar bears. This phenomenon may be attributed to less influence of recent expansion on island populations compared with that of continental populations. These results support our hypothesis and indicate that brown bears have a multi-layered genetic structure influenced by migration events at different times.