High levels of inbreeding with spatial and host-associated structure in lice of an endangered freshwater seal

Abstract

Host-specialist parasites of endangered large vertebrates are in many cases more endangered than their hosts. In particular, low host population densities and reduced among-host transmission rates are expected to lead to inbreeding within parasite infrapopulations living on single host individuals. Furthermore, spatial population structures of directly-transmitted parasites should be concordant with those of their hosts. Using population genomic approaches, we investigated inbreeding and population structure in a host-specialist seal louse (Echinophthirius horridus) infesting the Saimaa ringed seal (Phoca hispida saimensis), which is endemic to Lake Saimaa in Finland, and is one of the most endangered pinnipeds in the world. We conducted genome resequencing of pairs of lice collected from 18 individual Saimaa ringed seals throughout the Lake Saimaa complex. Our analyses showed high genetic similarity and inbreeding between lice inhabiting the same individual seal host, indicating low among-host transmission rates. Across the lake, genetic differentiation among individual lice was correlated with their geographic distance, and assignment analyses revealed a marked break in the genetic variation of the lice in the middle of the lake, indicating substantial population structure. These findings indicate that movements of Saimaa ringed seals across the main breeding areas of the fragmented Lake Saimaa complex may in fact be more restricted than suggested by previous population-genetic analyses of the seals themselves.

Keywords: Saimaa ringed seal; conservation genomics; genome resequencing; host-parasite interactions; seal louse.

FIGURE 1

(a) Echinophthirius horridus seal louse male (top) and female (bottom) from Lake Saimaa (for both, ventral view on left and dorsal on right). (b) Seal lice on the muzzle of a dead Saimaa ringed seal; the white arrow shows one of three individuals. (c) Saimaa ringed seal female nursing a weaning‐age pup

FIGURE 2

(a) Map Lake Saimaa, with collection sites of seals and their paired lice shown by coloured dots that are labelled with the seal individual numbers. The main basins of the Lake Saimaa complex are separated by broken lines, with area names indicated on the side. The location of the town Savonlinna at the Kyrönsalmi strait is indicated by a red circle. (b) PCoA ordination plot of seal lice based on their genetic similarity. Lice from the same seal are coloured similarly and connected by lines, and dot colours and shadings correspond to those used in (a). Dot shading indicates the main lake area (see legend). Note that lice from northern Saimaa and Haukivesi tend to be located on the right‐hand side of the ordination, while lice from the two southernmost areas are to the left. (c) Relationship between genetic distance and ln geographic distance between individual seal lice in the full data set. (d) Admixture plot for individual seal lice at K = 2. Section heights within bars show the proportion of ancestry attributed to “northern” (blue) and “southern” (orange) ancestry. Louse individuals are denoted below the plot and ordered from the south to north in the left to right direction, the main lake areas are indicated above the plot, and the locations of the borders between them (see a) are indicated by inverted triangles. The location of the town Savonlinna at the Kyrönsalmi strait is indicated by a red circle above the triangle

FIGURE 3

Correlation between sample‐specific estimates of mean θ (an indicator of heterozygosity and effective population size) of lice collected from the same seal individuals (i.e., same infrapopulation). Dot colours correspond to those used in Figure 2a, labels indicate the seal individual from which the lice were collected, and dot shading shows the lake area (see legend). The red line represents the correlation from a reduced major axis regression, and grey lines represent the confidence limits of the slope