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Causes and Consequences of Fine-Scale Population Structure in a Critically Endangered Freshwater Seal

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Causes and Consequences of Fine-Scale Population Structure in a Critically Endangered Freshwater Seal

Mia Valtonen et al. BMC Ecol.

Abstract

Background: Small, genetically uniform populations may face an elevated risk of extinction due to reduced environmental adaptability and individual fitness. Fragmentation can intensify these genetic adversities and, therefore, dispersal and gene flow among subpopulations within an isolated population is often essential for maintaining its viability. Using microsatellite and mtDNA data, we examined genetic diversity, spatial differentiation, interregional gene flow, and effective population sizes in the critically endangered Saimaa ringed seal (Phoca hispida saimensis), which is endemic to the large but highly fragmented Lake Saimaa in southeastern Finland.

Results: Microsatellite diversity within the subspecies (HE = 0.36) ranks among the lowest thus far recorded within the order Pinnipedia, with signs of ongoing loss of individual heterozygosity, reflecting very low effective subpopulation sizes. Bayesian assignment analyses of the microsatellite data revealed clear genetic differentiation among the main breeding areas, but interregional structuring was substantially weaker in biparentally inherited microsatellites (FST = 0.107) than in maternally inherited mtDNA (FST = 0.444), indicating a sevenfold difference in the gene flow mediated by males versus females.

Conclusions: Genetic structuring in the population appears to arise from the joint effects of multiple factors, including small effective subpopulation sizes, a fragmented lacustrine habitat, and behavioural dispersal limitation. The fine-scale differentiation found in the landlocked Saimaa ringed seal is especially surprising when contrasted with marine ringed seals, which often exhibit near-panmixia among subpopulations separated by hundreds or even thousands of kilometres. Our results demonstrate that population structures of endangered animals cannot be predicted based on data on even closely related species or subspecies.

Figures

Figure 1
Figure 1
Location of Lake Saimaa in Finland (A) and collection sites of the ringed seal specimens (B – D). Initial (B) and updated (C, D) regional division used in this study. Different colours imply different mtDNA haplotypes (B), and different clusters identified by Structure (C) and TESS (D) (see Figure  5A,C).
Figure 2
Figure 2
Observed heterozygosity of Saimaa ringed seal individuals in relation to their year of birth.
Figure 3
Figure 3
Factorial correspondence analysis (FCA) plot of ringed seals from different regions of Lake Saimaa. Individuals are marked with different symbols based on (A) the initial division to four main regions and (B) on the updated division to five regions (see legends).
Figure 4
Figure 4
Average kinship coefficient plotted against logarithmic distance between Saimaa ringed seal individual pairs. The plots are based on (A) 17 microsatellite loci, and (B) mtDNA haplotypes (Loiselle) and genetic distance between haplotypes (Nij). Distance classes differing significantly from the mean kinship of the population are marked with asterisks: ***P < 0.001; *P < 0.05.
Figure 5
Figure 5
Assignment of individual Saimaa ringed seals into population clusters based on microsatellite data. Results are shown as indicated by Structure (A) for K= 2 and (B)K= 4, and (C) by TESS for K= 4. Each bar represents a single individual, and the height of each bar represents the relative probability of it belonging to a given cluster. Individuals are grouped by the four main sampling areas, inverted triangles above the plots denote individuals that originate from the Kolovesi part of the Haukivesi area. Cluster colours in (A) and (C) correspond to the colours used in Figure  1C,D. The arrow below the plot in (C) indicates an individual that was excluded from the analysis in TESS due to lacking detailed location information.

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