Parasite-Mediated Selection against Inbred Soay Sheep in a Free-Living, Island Population

Abstract

Parasites are thought to provide a selective force capable of promoting genetic variation in natural populations. One rarely considered pathway for this action is via parasite-mediated selection against inbreeding. If parasites impose a fitness cost on their host and the offspring of close relatives have greater susceptibility to parasites due to the increased homozygosity that results from inbreeding, then parasite-mediated mortality may select against inbred individuals. This hypothesis has not yet been tested within a natural vertebrate population. Here we show that relatively inbred Soay sheep (Ovis aries), as assessed by microsatellite heterozygosity, are more susceptible to parasitism by gastrointestinal nematodes, with interactions indicating greatest susceptibility among adult sheep at high population density. During periods of high overwinter mortality on the island of Hirta, St. Kilda, Scotland, highly parasitised individuals were less likely to survive. More inbred individuals were also less likely to survive, which is due to their increased susceptibility to parasitism, because survival was random with respect to inbreeding among sheep that were experimentally cleared of their gastrointestinal parasite burden by anthelminthic treatment. As a consequence of this selection, average microsatellite heterozygosity increases with age in St. Kildan Soay sheep. We suggest that parasitemediated selection acts to maintain genetic variation in this small island population by removing less heterozygous individuals.

Inbreeding, heterozygosity and fitness in a reintroduced population of endangered African wild dogs (Lycaon pictus)

“…Of the 181 wild dogs assigned f values, 85 (from eight packs) also were genotyped to include corresponding molecular metrics. Standardized multilocus heterozygosity (stMLH) was calculated based on the proportion of loci genotyped for a given individual that was heterozygous divided by mean heterozygosity in the population at the same loci (Coltman et al 1999;Slate et al 2004). IR reflects the relatedness of the parents of an individual by determining the degree of allele-sharing relative to random expectations across all loci (Amos et al 2001).…”

“…Molecular metric assessments have led to HFC discoveries involving fitness traits such as fecundity (Amos et al 2001), immunocompetence (Coltman et al 1999), recruitment (Jensen et al 2007) and survival (DaSilva et al 2006). Although small populations of endangered species are most vulnerable to inbreeding and fitness reduction (Fitzpatrick and Evans 2009), most HFC studies have focused on large populations of common species (see Grueber et al 2008 for review).…”

“…Molecular metrics are commonly used as a surrogate for pedigree inbreeding coefficients (f), because the latter can be logistically difficult to obtain within natural populations. The most frequently used molecular metrics of heterozygosity in HFCs analyses include standardized multilocus heterozygosity (stMLH; Coltman et al 1999), internal relatedness (IR; Amos et al 2001) and standardized mean d 2 (Coulson et al 1998). However, it has been suggested that the correlation between molecular heterozygosity and pedigree inbreeding coefficients is too weak to be of biological significance (Coltman and Slate 2003;Balloux et al 2004;Slate et al 2004;Hansson and Westerberg 2008).…”

Condition, innate immunity and disease mortality of inbred crows

“…Inbred individuals might be less resistant to disease if they are unable to recognize as wide a breadth of pathogens and parasites as relatively outbred individuals, or if disease-causing agents are part of an environment that selects against individuals expressing deleterious recessive alleles (Coltman et al 1999). Empirical evidence for disease costs of inbreeding has been documented in captive settings (e.g.…”

“…Empirical evidence for disease costs of inbreeding has been documented in captive settings (e.g. Spielman et al 2004;Hawley et al 2005;Ross-Gillespie et al 2007;Charpentier et al 2008;Ilmonen et al 2008) as well as in an array of free-living taxa, including California sea lions (Zalophus californianus; Acevedo- Whitehouse et al 2003), Mediterranean striped dolphins (Stenella coeruleoalba; Valsecchi et al 2004), Galapagos hawks (Buteo galapagoensis; Whiteman et al 2006), Soay sheep (Ovis aries; Coltman et al 1999), harbour seals (Phoca vitulina; Rijks et al 2008) and American crows (Corvus brachyrhynchos; Townsend et al 2009a). In some studies, however, the relationship between inbreeding and disease is unclear (e.g.…”