Circumpolar phylogeography and demographic history of beluga whales reflect past climatic fluctuations.

Several Arctic marine mammal species are predicted to be negatively impacted by rapid sea ice loss associated with ongoing ocean warming. However, consequences for Arctic whales remain uncertain. To investigate how Arctic whales responded to past climatic fluctuations, we analyzed 206 mitochondrial genomes from beluga whales (Delphinapterus leucas) sampled across their circumpolar range, and four nuclear genomes, covering both the Atlantic and the Pacific Arctic region. We find four well-differentiated mitochondrial lineages, which were established before the onset of the last glacial expansion ~110 thousand years ago. Our findings suggest these lineages diverged in allopatry, reflecting isolation of populations during glacial periods, when the Arctic sea-shelf was covered by multi-year sea ice. Subsequent population expansion and secondary contact between the Atlantic and Pacific Oceans has shaped the current geographic distribution of lineages, and likely facilitated mitochondrial introgression. Our demographic reconstructions based on both mitochondrial and nuclear genomes show markedly lower population sizes during the Last Glacial Maximum (LGM) compared to the preceding Eemian and current Holocene interglacial periods. Habitat modelling similarly reveals less suitable habitat during the LGM (glacial) than at present (interglacial). Together, our findings suggest an association between climate, population size and available habitat in belugas. Forecasts for year 2100 show that beluga habitat will decrease and shift northwards as oceans continue to warm, putatively leading to population declines in some beluga populations. Finally, we identify vulnerable populations which, if extirpated as a consequence of ocean warming, would lead to a substantial decline of species-wide haplotype diversity.