Population genomics of the inbred Scandinavian wolf

Abstract

The Scandinavian wolf population represents one of the genetically most well-characterized examples of a severely bottlenecked natural population (with only two founders), and of how the addition of new genetic material (one immigrant) can at least temporarily provide a 'genetic rescue'. However, inbreeding depression has been observed in this population and in the absence of additional immigrants, its long-term viability is questioned. To study the effects of inbreeding and selection on genomic diversity, we performed a genomic scan with approximately 250 microsatellite markers distributed across all autosomes and the X chromosome. We found linkage disequilibrium (LD) that extended up to distances of 50 Mb, exceeding that of most outbreeding species studied thus far. LD was particularly pronounced on the X chromosome. Overall levels of observed genomic heterozygosity did not deviate significantly from simulations based on known population history, giving no support for a general selection for heterozygotes. However, we found evidence supporting balancing selection at a number of loci and also evidence suggesting directional selection at other loci. For markers on chromosome 23, the signal of selection was particularly strong, indicating that purifying selection against deleterious alleles may have occurred even in this very small population. These data suggest that population genomics allows the exploration of the effects of neutral and non-neutral evolution on a finer scale than what has previously been possible.

Figure 1

Distribution of D′ for pairs of unlinked loci on different chromosomes. Approximately 1 % (231) of the pairs of loci has a D′ value of 1. However, when LD for these pairs is estimated by χ²′, they have a distribution similar to that of χ²′ for all pair-wise loci, indicating that these high D′ values are artifacts.

Figure 2

The relationship between LD (D′) and physical distance (Mb) between loci residing on the same chromosome. Mean D′ is given in 1 Mb intervals for autosomes (filled circles) and the X chromosome (open circles).

Figure 3

Observed microsatellite heterozygosity for cohorts within the Scandinavian wolf population. Filled circles are animals descending from the initial two founders while open circles are animals with some ancestry also from a third immigrant that first reproduced in 1991. Separate regression lines for the two data sets are given.

Figure 4

Observed and simulated average heterozygosity for cohorts within the Scandinavian wolf population. Open circles are average heterozygosities per birth year for wolves in the data set. Filled circles are simulated average heterozygosity.

Figure 5

Inbreeding coefficients from Bensch et al. (2006) shown in open circles vs. our simulations shown in filled circles. Error bars show +/- one standard error for simulated values.

Figure 6

F_ST for all markers estimated in the comparison of Scandinavian and Russian wolves. Markers from different chromosomes are given in alternating colors. * denotes loci with F_ST values outside of 95 % confidence intervals from simulated F_ST values.

Figure 6

F_ST for all markers estimated in the comparison of Scandinavian and Russian wolves. Markers from different chromosomes are given in alternating colors. * denotes loci with F_ST values outside of 95 % confidence intervals from simulated F_ST values.