The origins and diversification of Holarctic brown bear populations inferred from genomes of past and present populations

Abstract

The brown bear is one of the few surviving megafauna species that made it through the Late Quaternary megafaunal extinctions. It is widely distributed and has become a model organism for studying biogeographic patterns across Eurasia and North America. However, to date, most studies have focused on the mitochondrial genome with nuclear genomes only being used for evolutionary studies within the Ursusidae family or local population studies. Here we present novel genomic data from two Late Pleistocene brown bears from Japan and Siberia, and combine them with modern and ancient published genomes from across the Holarctic range, to investigate the species' genomic evolutionary history. We uncovered four differentiated populations corresponding to Europe, Siberia, Japan, and North America which all diverged ~100 kya. Palaeogenomic data reveals population continuity in all populations apart from in Europe where Late Pleistocene European individuals cluster with Siberia rather than contemporary/mid-late Holocene European individuals. We propose a replacement around the Pleistocene-Holocene transition in Europe, supported by results of a recent population expansion in modern European individuals. Population continuity in Japan and North America contrasts mitochondrial suggestions of multiple migration events. However, the rapid population diversification and increased likelihood of gene flow and incomplete lineage may have biased mitochondrial results. Demographic results show similar effective population declines in all populations ~50 kya which we suggest is due to the geographic dispersal of the newly diversified populations and a decrease of gene flow between populations.