Tracing the Drivers of Range-Wide Bowhead Whale Genomic Structure and Diversity

In a rapidly warming Arctic, genetic variation might serve to buffer organisms against the effects of environmental change, such as sea ice loss and ocean warming. Yet, this concept remains largely unexplored because comprehensive genome-wide studies across the full ranges of Arctic marine taxa are rare. Bowhead whales (Balaena mysticetus) have a strong association with sea ice and polar water masses, a long history of human exploitation, and a circumpolar distribution, making them a valuable model for evaluating how past environmental and anthropogenic factors have shaped contemporary population variation. We analysed both nuclear and mitochondrial genomes from bowhead whales sampled across the species' range, encompassing all four recognised stocks. Firstly, our results indicate the existence of three genetic groupings instead of four: (1) Okhotsk Sea; (2) East Greenland-Svalbard-Barents Sea; and (3) a population containing two recognised stocks-the Bering-Chukchi-Beaufort and East Canada-West Greenland. We utilised high-resolution ecological niche modelling and bowhead whale movement data to reconstruct inter-stock habitat connectivity over the last 11,700 years, finding that this explains our identified genetic groupings. Bowhead whale populations exhibit little-to-no evidence of recent inbreeding and retain high genetic diversity relative to other mammalian species despite centuries of intensive commercial whaling. The most vulnerable population is that in the Okhotsk Sea, which has the lowest genetic diversity, most inbreeding, and the highest realised genetic load. Collectively, our findings elucidate the recent history and dynamics of bowhead whales, offering valuable baseline data and context on present-day genetic structure and diversity to support effective conservation and management strategies.