Genomics reveal population structure, evolutionary history, and signatures of selection in the northern bottlenose whale, Hyperoodon ampullatus

Abstract

Information on wildlife population structure, demographic history, and adaptations are fundamental to understanding species evolution and informing conservation strategies. To study this ecological context for a cetacean of conservation concern, we conducted the first genomic assessment of the northern bottlenose whale, Hyperoodon ampullatus, using whole-genome resequencing data (n = 37) from five regions across the North Atlantic Ocean. We found a range-wide pattern of isolation-by-distance with a genetic subdivision distinguishing three subgroups: the Scotian Shelf, western North Atlantic, and Jan Mayen regions. Signals of elevated levels of inbreeding in the Endangered Scotian Shelf population indicate this population may be more vulnerable than the other two subgroups. In addition to signatures of inbreeding, evidence of local adaptation in the Scotian Shelf was detected across the genome. We found a long-term decline in effective population size for the species, which poses risks to their genetic diversity and may be exacerbated by the isolating effects of population subdivision. Protecting important habitat and migratory corridors should be prioritized to rebuild population sizes that were diminished by commercial whaling, strengthen gene flow, and ensure animals can move across regions in response to environmental changes.

Keywords: cetacean; conservation; genetic diversity; genomics; whale.

FIGURE 1

Map of northern bottlenose whale sample sites across the North Atlantic Ocean, collected between 2003–2019. Dark blue, Jan Mayen; light blue, Canadian Arctic; yellow, Labrador; orange, Newfoundland; red, Scotian shelf. White lines represent shortest distances between sites in water depths of 500 m or greater.

FIGURE 2

Regional clustering seen from northern bottlenose whale population analyses. (a) Principal components analysis (PCA) with first two principal axes and (b) PCA with third and fourth principal axes, where proportion of variance explained by each principal component is listed in parentheses, and (c) admixture results from sNMF analyses using K = 2 and K = 3 clusters. JM, Jan Mayen; CA, Canadian Arctic; LB, Labrador; NF, Newfoundland; SS, Scotian shelf. 995,508 SNPs were used in PCA, and 544,733 SNPs were used in sNMF analyses.

FIGURE 3

Correlations of pairwise F _ST from 995,508 SNPs with (a) distance and (b) latitude between northern bottlenose whale sampling locations (JM, Jan Mayen; CA, Canadian Arctic; LB, Labrador; NF, Newfoundland; SS, Scotian shelf). Linear regression standard error is coloured in grey. Mantel test correlation and p‐value are displayed top left.

FIGURE 4

Demographic history of the northern bottlenose whale from 1,985,379 SNPs estimated as (a) one population and (b) three subgroups (JM, Jan Mayen; WNA, western North Atlantic; SS, Scotian shelf). Notable time periods are coloured in grey and marked by Roman numerals representing (i) the start of whaling in the North Atlantic, with dark grey bar representing large‐scale whaling in 19th–20th centuries, and (ii) last glacial period (11.7–115 kya) with dark grey bar representing last glacial maximum (19–26.5 kya). Plots were scaled with a mutation rate of 1.53 × 10⁻⁸ and generation time of 17.8 years.

FIGURE 5

XP‐EHH in the northern bottlenose whale from 1,264,382 SNPs between (a) Scotian shelf and northern regions including Jan Mayen and western North Atlantic. The northern group was divided into subgroups for comparisons with Scotian shelf using (b) Jan Mayen only, and (c) western North Atlantic as one group. Candidate regions under selection are coloured blue in northern groups, and red in Scotian shelf, including genes within 20 kb windows of candidate regions.