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.

Group structure and kinship in beluga whale societies.

Evolutionary explanations for mammalian sociality typically center on inclusive-fitness benefits of associating and cooperating with close kin, or close maternal kin as in some whale societies, including killer and sperm whales. Their matrilineal structure has strongly influenced the thinking about social structure in less well-studied cetaceans, including beluga whales. In a cross-sectional study of group structure and kinship we found that belugas formed a limited number of distinct group types, consistently observed across populations and habitats. Certain behaviours were associated with group type, but group membership was often dynamic. MtDNA-microsatellite profiling combined with relatedness and network analysis revealed, contrary to predictions, that most social groupings were not predominantly organized around close maternal relatives. They comprised both kin and non-kin, many group members were paternal rather than maternal relatives, and unrelated adult males often traveled together. The evolutionary mechanisms that shape beluga societies are likely complex; fitness benefits may be achieved through reciprocity, mutualism and kin selection. At the largest scales these societies are communities comprising all ages and both sexes where multiple social learning pathways involving kin and non-kin can foster the emergence of cultures. We explore the implications of these findings for species management and the evolution of menopause.

Migratory culture, population structure and stock identity in North Pacific beluga whales (Delphinapterus leucas).

The annual return of beluga whales, Delphinapterus leucas, to traditional seasonal locations across the Arctic may involve migratory culture, while the convergence of discrete summering aggregations on common wintering grounds may facilitate outbreeding. Natal philopatry and cultural inheritance, however, has been difficult to assess as earlier studies were of too short a duration, while genetic analyses of breeding patterns, especially across the beluga's Pacific range, have been hampered by inadequate sampling and sparse information on wintering areas. Using a much expanded sample and genetic marker set comprising 1,647 whales, spanning more than two decades and encompassing all major coastal summering aggregations in the Pacific Ocean, we found evolutionary-level divergence among three geographic regions: the Gulf of Alaska, the Bering-Chukchi-Beaufort Seas, and the Sea of Okhotsk (Φst = 0.11-0.32, Rst = 0.09-0.13), and likely demographic independence of (Fst-mtDNA = 0.02-0.66), and in many cases limited gene flow (Fst-nDNA = 0.0-0.02; K = 5-6) among, summering groups within regions. Assignment tests identified few immigrants within summering aggregations, linked migrating groups to specific summering areas, and found that some migratory corridors comprise whales from multiple subpopulations (PBAYES = 0.31:0.69). Further, dispersal is male-biased and substantial numbers of closely related whales congregate together at coastal summering areas. Stable patterns of heterogeneity between areas and consistently high proportions (~20%) of close kin (including parent-offspring) sampled up to 20 years apart within areas (G = 0.2-2.9, p>0.5) is the first direct evidence of natal philopatry to migration destinations in belugas. Using recent satellite telemetry findings on belugas we found that the spatial proximity of winter ranges has a greater influence on the degree of both individual and genetic exchange than summer ranges (rwinter-Fst-mtDNA = 0.9, rsummer-Fst-nDNA = 0.1). These findings indicate widespread natal philopatry to summering aggregation and entire migratory circuits, and provide compelling evidence that migratory culture and kinship helps maintain demographically discrete beluga stocks that can overlap in time and space.

Arctic marine mammal population status, sea ice habitat loss, and conservation recommendations for the 21st century.

Arctic marine mammals (AMMs) are icons of climate change, largely because of their close association with sea ice. However, neither a circumpolar assessment of AMM status nor a standardized metric of sea ice habitat change is available. We summarized available data on abundance and trend for each AMM species and recognized subpopulation. We also examined species diversity, the extent of human use, and temporal trends in sea ice habitat for 12 regions of the Arctic by calculating the dates of spring sea ice retreat and fall sea ice advance from satellite data (1979-2013). Estimates of AMM abundance varied greatly in quality, and few studies were long enough for trend analysis. Of the AMM subpopulations, 78% (61 of 78) are legally harvested for subsistence purposes. Changes in sea ice phenology have been profound. In all regions except the Bering Sea, the duration of the summer (i.e., reduced ice) period increased by 5-10 weeks and by >20 weeks in the Barents Sea between 1979 and 2013. In light of generally poor data, the importance of human use, and forecasted environmental changes in the 21st century, we recommend the following for effective AMM conservation: maintain and improve comanagement by local, federal, and international partners; recognize spatial and temporal variability in AMM subpopulation response to climate change; implement monitoring programs with clear goals; mitigate cumulative impacts of increased human activity; and recognize the limits of current protected species legislation.