Genetic and evolutionary divergence of harbour seals (Phoca vitulina) in Iliamna Lake, Alaska

Abstract

Freshwater populations of typically marine species present unique opportunities to investigate biodiversity, evolutionary divergence, and the adaptive potential and niche width of species. A few pinniped species have populations that reside solely in freshwater. The harbour seals inhabiting Iliamna Lake, Alaska constitute one such population. Their remoteness, however, has long hindered scientific inquiry. We used DNA from seal scat and tissue samples provided by Indigenous hunters to screen for mitochondrial DNA and microsatellite variation within Iliamna Lake and eight regions across the Pacific Ocean. The Iliamna seals (i) were substantially and significantly discrete from all other populations ( [Formula: see text]F _st-mtDNA = 0.544, [Formula: see text]Φ _{st - mtDNA} = 0.541, [Formula: see text]F _{st-microsatellites} = 0.308), (ii) formed a discrete genetic cluster separate from all marine populations (modal ∆k = 2, PC1 = 14.8%), had (iii) less genetic diversity (Hd, π, H _exp), and (iv) higher inbreeding (F) than marine populations. These findings are both striking and unexpected revealing that Iliamna seals have likely been on a separate evolutionary trajectory for some time and may represent a unique evolutionary legacy for the species. Attention must now be given to the selective processes driving evolutionary divergence from harbour seals in marine habitats and to ensuring the future of the Iliamna seal.

Keywords: Iliamna Lake; Phoca vitulina; divergences; evolution; genetics; seals.

Figure 1.

(a) Locations for eight harbour seal regions across the North Pacific range (green) and Iliamna Lake (blue). (b) Location of Iliamna Lake connected to Bristol Bay via the Kvichak River with sampling locations denoted by blue symbols. (c) Box-and-whisker plots (central tendency and variance) of genetic diversity, differentiation and inbreeding (see text for details). Iliamna seals are denoted by blue circles.

Figure 2.

Patterns of genetic diversity and differentiation in Pacific harbour seals from eight marine regions (green) and Iliamna Lake (blue). (a) Patterns of mtDNA (haplotype) diversity within populations. (b) Patterns of nDNA (microsatellite) diversity and inbreeding within populations. (c) Summary plots of the model-based cluster analysis from structure for k = 2 and k = 3 population clusters. Both plots represent analyses where admixture was not allowed and sampling locations were not provided as prior information. All parameter settings yielded very similar results. Each of the 227 genotyped individuals is represented by a vertical bar with estimated membership of each cluster denoted by different colours. The order of the nine seal populations in each panel in A and B follow that of the plots in C. nd denotes no data.

Figure 3.

(a) Minimum spanning network of harbour seal mtDNA haplotypes from Iliamna lake and eight regions across the Pacific Ocean. For ease of viewing, the haplotypes found in Ilimana Lake are highlighted in blue and those in Bristol Bay in yellow. Samples from the geographical extremes are highlighted in shades of green (Japan and Russia) and in burgundy (California), while all others are in shades of grey. Disc size corresponds to overall haplotype frequency. (b) Principal component analysis on Pacific harbour seal genotypes from Iliamna Lake and eight marine regions. Individuals from a particular locale are represented by dots of the same colour and are connected to the locale’s labelled centroid. Confidence ellipses are included.