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

Abstract

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 postglacial bedrock rebound around 9000 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. 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 from the Baltic Sea, Lake Ladoga, North America, Svalbard, and the White Sea. 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 also shows affinities to North American ringed seals. 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 seal is not representative of the ancestral population of the Saimaa ringed seal, which calls for re-evaluation of the deep history of this subspecies.

Keywords: Saimaa ringed seal; freshwater pinniped; genetic diversity; genetic drift; mitochondrial DNA; museum specimens.

FIGURE 1

Maps showing the areas from which (a) marine and (b) freshwater ringed seals were sampled for this study (note that a permanent population is not present in Lake Pielinen).

FIGURE 2

Haplotype network of ringed seals in the Baltic Sea and lakes Saimaa, Pielinen, and Ladoga. The sizes of the circles correspond to the number of sampled individuals with the haplotype, section colors denote sampling site and collection period within Lake Saimaa (see map and legend in inset). Small white circles denote unobserved haplotypes. Note that haplotype H14 is present in a single individual that has a 64‐bp deletion (each bp in the deletion is counted as one change) as well as unique substitutions.

FIGURE 3

Haplotype network of Saimaa ringed seals during five different time intervals spanning periods from 1894 to the present. In each network, circle size is proportional to the number of samples representing each haplotype, and sector colors denote the proportion of samples belonging to each of the sampling areas indicated in the map to the right of the networks.

FIGURE 4

Haplotype frequency differences between the modern population and earlier temporal groups (TG1–TG4). Dark gray bars depict the expected distribution of the number of observations per haplotype in each temporal group based on 100,000 rounds of resampling from the modern distribution (TG5, N = 128). Red bars indicate the observed numbers within each temporal group, and red font denotes haplotypes with a nominally significant frequency difference as compared the modern population (i.e., with an observed number of occurrences outside 95% of the simulated probability mass).

FIGURE 5

Bayesian skyline plot depicting the estimated historical effective population size of Saimaa ringed seal females on a logarithmic scale. Calendar years are shown on the X‐axis. The thick line shows the median and the shaded area represents the 95% highest posterior density interval.

FIGURE 6

Bayesian phylogenetic tree of 211 unique mitochondrial control‐region haplotypes found in freshwater, Baltic, and Arctic ringed seal populations. Symbols and colors at the tips of the tree indicate the areas where each haplotype is present (see inset map and legend). Numbers above branches are posterior probabilities; only values over 0.50 are shown. The location of the Saimaa ringed seal individual with a 64‐bp deletion (haplotype H14) is indicated by an arrow.