Polar bears (PBs) are superbly adapted to the extreme Arctic environment and have become emblematic of the threat to biodiversity from global climate change. Their divergence from the lower-latitude brown bear provides a textbook example of rapid evolution of distinct phenotypes. However, limited mitochondrial and nuclear DNA evidence conflicts in the timing of PB origin as well as placement of the species within versus sister to the brown bear lineage. We gathered extensive genomic sequence data from contemporary polar, brown, and American black bear samples, in addition to a 130,000-to 110,000-y old PB, to examine this problem from a genome-wide perspective. Nuclear DNA markers reflect a species tree consistent with expectation, showing polar and brown bears to be sister species. However, for the enigmatic brown bears native to Alaska's Alexander Archipelago, we estimate that not only their mitochondrial genome, but also 5-10% of their nuclear genome, is most closely related to PBs, indicating ancient admixture between the two species. Explicit admixture analyses are consistent with ancient splits among PBs, brown bears and black bears that were later followed by occasional admixture. We also provide paleodemographic estimates that suggest bear evolution has tracked key climate events, and that PB in particular experienced a prolonged and dramatic decline in its effective population size during the last ca. 500,000 years. We demonstrate that brown bears and PBs have had sufficiently independent evolutionary histories over the last 4-5 million years to leave imprints in the PB nuclear genome that likely are associated with ecological adaptation to the Arctic environment.demographic history | hybridization | mammalian genomics | phylogenetics G enome-scale studies of speciation and admixture have become essential tools in evolutionary analyses of recently diverged lineages. For example, paradigm-shifting genomic research on archaic and anatomically modern humans has identified critical gene flow events during hominin history (1, 2). However, aside from several analyses of domesticated species and their wild relatives (e.g., ref.3), studies that use whole-genome sequencing to investigate admixture in wildlife populations are only now beginning to emerge.The bear family (Ursidae, Mammalia) represents an excellent, largely untapped model for investigating complex speciation and rapid evolution of distinct phenotypes. Although polar bears (PBs; Ursus maritimus) and brown bears (Ursus arctos) are considered separate species, analyses of fossil evidence and mitochondrial sequence data have indicated a recent divergence of PBs from within brown bears (surveyed in ref. 4). For example, phylogenetic analyses of complete mitochondrial genomes, including from a unique 130,000-to 110,000-y-old PB jawbone from Svalbard, Norway, confirmed a particularly close relationship between PB and a genetically isolated population of brown bears from the Admiralty, Baranof, and Chichagof islands in Alaska's Alexander Archipelago (hereaf...

No abstract

The authors note that, due to a printer's error, on page 5054, right column, second paragraph, eighth line, "Within this clade, we estimated the mean age of the split between the ABC bears and the polar bears to be 152 ky, and the mean age for all polar bears as 134 ky, near the end of the Eemian interglacial period and completely in line with the stratigraphically determined age of the Poolepynten subfossil (11)," should instead appear as "Within this clade, we estimated the mean age of the split between the ABC bears and the polar bears to be 152 ky, and the mean age for all polar bears as 134 ky, near the beginning of the Eemian interglacial period and completely in line with the stratigraphically determined age of the Poolepynten subfossil (11)." This error does not affect the conclusions of the article. This error has been corrected online and in print.www.pnas.org/cgi

We provide an expansive analysis of polar bear (Ursus maritimus) circumpolar genetic variation during the last two decades of decline in their sea-ice habitat. We sought to evaluate whether their genetic diversity and structure have changed over this period of habitat decline, how their current genetic patterns compare with past patterns, and how genetic demography changed with ancient fluctuations in climate. Characterizing their circumpolar genetic structure using microsatellite data, we defined four clusters that largely correspond to current ecological and oceanographic factors: Eastern Polar Basin, Western Polar Basin, Canadian Archipelago and Southern Canada. We document evidence for recent (ca. last 1–3 generations) directional gene flow from Southern Canada and the Eastern Polar Basin towards the Canadian Archipelago, an area hypothesized to be a future refugium for polar bears as climate-induced habitat decline continues. Our data provide empirical evidence in support of this hypothesis. The direction of current gene flow differs from earlier patterns of gene flow in the Holocene. From analyses of mitochondrial DNA, the Canadian Archipelago cluster and the Barents Sea subpopulation within the Eastern Polar Basin cluster did not show signals of population expansion, suggesting these areas may have served also as past interglacial refugia. Mismatch analyses of mitochondrial DNA data from polar and the paraphyletic brown bear (U. arctos) uncovered offset signals in timing of population expansion between the two species, that are attributed to differential demographic responses to past climate cycling. Mitogenomic structure of polar bears was shallow and developed recently, in contrast to the multiple clades of brown bears. We found no genetic signatures of recent hybridization between the species in our large, circumpolar sample, suggesting that recently observed hybrids represent localized events. Documenting changes in subpopulation connectivity will allow polar nations to proactively adjust conservation actions to continuing decline in sea-ice habitat.

Genetic and paleontological evidence are combining to provide a new and surprising picture of mammalian biogeography in southeastern Alaska. Prior to our study, the brown and black bears of the Alexander Archipelago were considered postglacial immigrants that never had overlapping ranges. Vertebrate fossils from caves on Prince of Wales Island now demonstrate that brown and black bears coexisted there (and even inhabited the same caves) both before and after the last glaciation. Differences in mtDNA sequences suggest that living brown bears of the Alexander Archipelago comprise a distinct clade and are more closely related to polar bears than to their mainland conspecifics. We conclude that brown bears, and perhaps other large mammals, have continuously inhabited the archipelago for at least 40,000 yr and that habitable refugia were therefore available throughout the last glaciation.