Museum specimens of a landlocked pinniped reveal recent loss of genetic diversity and unexpected population connections

Abstract

Aim: The Saimaa ringed seal (Pusa hispida saimensis) is endemic to Lake Saimaa in Finland. The subspecies is thought to have originated when parts of the ringed seal population of the Baltic region were trapped in lakes emerging due to post-glacial bedrock rebound around 9,000 years ago. During the 20th century, the population experienced a drastic human-induced bottleneck. Today encompassing a little over 400 seals with extremely low genetic diversity, it is classified as endangered. Our main aim was to evaluate the role of the 20th century bottleneck in the erosion of genetic diversity in the Saimaa seal population. We also evaluated connections with other ringed seals from the Baltic Sea, Lake Ladoga, North America, Svalbard and the White Sea. Location: Lake Saimaa, Finland, together with the Baltic Sea and the Arctic Ocean. Methods: We sequenced sections of the mitochondrial control region from 60 up to 125 years old museum specimens of the Saimaa ringed seal. The generated dataset was combined with publicly available sequences. We studied how genetic variation has changed through time in this subspecies, and how it is phylogenetically related to other ringed seal populations. Results: We observed temporal fluctuations in haplotype frequencies and loss of haplotypes accompanied by a recent reduction in female effective population size. In apparent contrast with the traditionally held view of the Baltic origin of the population, the Saimaa ringed seal mtDNA variation shows also affinities to North American ringed seals. Main conclusions: Our results suggest that the Saimaa ringed seal has experienced recent genetic drift associated with small population size. The results further suggest that extant Baltic ringed seals do not represent well the ancestral population of the Saimaa ringed seal, which calls for re-evaluation of the deep history of this subspecies.

Fragmented habitat compensates for the adverse effects of genetic bottleneck

“…Our analyses show that Saimaa ringed seals are unique among the studied ringed seal subspecies and contain a high number of private polymorphic sites and fixed nucleotide changes, consistent with the proposed long isolation and population bottleneck in Saimaa (25). Our demographic analyses reveal the severity of this bottleneck, give an approximate timing for the start of isolation and suggest a complex ancestry for the Saimaa population.…”

“…1B) possibly reflects the population deriving some of its ancestry from elsewhere. Similar signals are seen in other aquatic organisms in the Baltic Sea region (22–24), and an origin in an eastern freshwater refugium has been proposed also for Saimaa ringed seals based on their unique mitochondrial haplotypes (25). Finally, conversion of coalescent estimates into years and numbers of individuals requires a good understanding of the genomic mutation rate, and lacking that, our estimates should be considered approximate.…”