Habitat discontinuity and fidelity to migratory routes shape narwhal genetic structure and diversity

Rapid Arctic warming is reshaping marine ecosystems and altering the evolutionary trajectories of ice-associated species. Narwhals (Monodon monoceros) are Arctic endemics that are thought to be vulnerable to climate change. We present the first nuclear genomic assessment of narwhals across their distribution to evaluate population structure, demographic history, local adaptation, inbreeding and genetic load. Using genomes from 117 individuals, we identified three populations: Canadian Arctic Archipelago/West Greenland, Northeast Greenland/Svalbard and Southeast Greenland. Demographic reconstructions indicated low effective population size over at least 600,000 years, followed by population growth during the last glacial period. Our results suggest that population structure is maintained by habitat discontinuities and fidelity to migration routes. The latter may promote local adaptation, as genes related to long-term memory were found in regions putatively under selection in Canadian Arctic Archipelago/West Greenland narwhals, which undertake the longest migrations. Genome-wide diversity was uniformly low across populations. Inbreeding levels were inversely related to estimated population sizes. The small and rapidly declining Southeast Greenland population exhibited elevated recent inbreeding. Deleterious mutations were primarily masked in heterozygous genotypes, raising concerns for this population. Together, our results demonstrate that past climate, habitat discontinuities and migration fidelity jointly structure narwhal populations.