Range-wide whole-genome resequencing of the brown bear reveals drivers of intraspecies divergence

Population-genomic studies can shed new light on the effect of past demographic processes on contemporary population structure. We reassessed phylogeographical patterns of a classic model species of postglacial recolonisation, the brown bear (Ursus arctos), using a range-wide resequencing dataset of 128 nuclear genomes. In sharp contrast to the erratic geographical distribution of mtDNA and Y-chromosomal haplotypes, autosomal and X-chromosomal multi-locus datasets indicate that brown bear population structure is largely explained by recent population connectivity. Multispecies coalescent based analyses reveal cases where mtDNA haplotype sharing between distant populations, such as between Iberian and southern Scandinavian bears, likely results from incomplete lineage sorting, not from ancestral population structure (i.e., postglacial recolonisation). However, we also argue, using forward-in-time simulations, that gene flow and recombination can rapidly erase genomic evidence of former population structure (such as an ancestral population in Beringia), while this signal is retained by Y-chromosomal and mtDNA, albeit likely distorted. We further suggest that if gene flow is male-mediated, the information loss proceeds faster in autosomes than in X chromosomes. Our findings emphasise that contemporary autosomal genetic structure may reflect recent population dynamics rather than postglacial recolonisation routes, which could contribute to mtDNA and Y-chromosomal discordances.