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 analysed 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 found four well-differentiated mitochondrial lineages, which were established before the onset of the last glacial expansion ~110 thousand years ago. Our findings suggested these lineages diverged in allopatry, reflecting isolation of populations during glacial periods when the Arctic sea-shelf was covered by multiyear sea ice. Subsequent population expansion and secondary contact between the Atlantic and Pacific Oceans shaped the current geographic distribution of lineages, and may have facilitated mitochondrial introgression. Our demographic reconstructions based on both mitochondrial and nuclear genomes showed markedly lower population sizes during the Last Glacial Maximum (LGM) compared to the preceding Eemian and current Holocene interglacial periods. Habitat modelling similarly revealed less suitable habitat during the LGM (glacial) than at present (interglacial). Together, our findings suggested the association between climate, population size, and available habitat in belugas. Forecasts for year 2100 showed that beluga habitat will decrease and shift northwards as oceans continue to warm, putatively leading to population declines in some beluga populations. Finally, we identified vulnerable populations which, if extirpated as a consequence of ocean warming, will lead to a substantial decline of species-wide haplotype diversity.

Colonizing the Wild West: Low Diversity of Complete Mitochondrial Genomes in Western North Pacific Killer Whales Suggests a Founder Effect.

In the North Pacific, fish-eating R-type "resident" and mammal-eating T-type "transient" killer whales do not interbreed and differ in ecology and behavior. Full-length mitochondrial genomes (about 16.4 kbp) were sequenced and assembled for 12 R-type and 14 T-type killer whale samples from different areas of the western North Pacific. All R-type individuals had the same haplotype, previously described for R-type killer whales from both eastern and western North Pacific. However, haplotype diversity of R-type killer whales was much lower in the western North Pacific than in the Aleutian Islands and the eastern North Pacific. T-type whales had 3 different haplotypes, including one previously undescribed. Haplotype diversity of T-type killer whales in the Okhotsk Sea was also much lower than in the Aleutian Islands and the eastern North Pacific. The highest haplotype diversity for both R- and T-type killer whales was observed in the Aleutian Islands. We discuss how the environmental conditions during the last glacial period might have shaped the history of killer whale populations in the North Pacific. Our results suggest the recent colonization or re-colonization of the western North Pacific by small groups of killer whales originating from the central or eastern North Pacific, possibly due to favorable environmental changes after the Last Glacial Maximum.

High genomic diversity in the endangered East Greenland Svalbard Barents Sea stock of bowhead whales (Balaena mysticetus).

The East Greenland-Svalbard-Barents Sea (EGSB) bowhead whale stock (Balaena mysticetus) was hunted to near extinction and remains Endangered on the International Union of Conservation of Nature Red List. The intense, temporally extensive hunting pressure may have left the population vulnerable to other perturbations, such as environmental change. However, the lack of genomic baseline data renders it difficult to evaluate the impacts of various potential stressors on this stock. Twelve EGSB bowhead whales sampled in 2017/2018 were re-sequenced and mapped to a previously published draft genome. All individuals were unrelated and void of significant signs of inbreeding, with similar observed and expected homo- and heterozygosity levels. Despite the small population size, mean autosome-wide heterozygosity was 0.00102, which is higher than that of most mammals for which comparable estimates are calculated using the same parameters, and three times higher than a conspecific individual from the Eastern-Canada-West-Greenland bowhead whale stock. Demographic history analyses indicated a continual decrease of Ne from ca. 1.5 million to ca. 250,000 years ago, followed by a slight increase until ca. 100,000 years ago, followed by a rapid decrease in Ne between 50,000 and 10,000 years ago. These estimates are lower than previously suggested based on mitochondrial DNA, but suggested demographic patterns over time are similar.