Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population

Abstract

Antagonistic coevolution between hosts and parasites has been proposed as a mechanism maintaining genetic diversity in both host and parasite populations. In particular, the high levels of genetic diversity widely observed at the major histocompatibility complex (MHC) of vertebrate hosts are consistent with the hypothesis of parasite-driven balancing selection acting to maintain MHC genetic diversity. To date, however, empirical evidence in support of this hypothesis, especially from natural populations, has been lacking. A large unmanaged population of Soay sheep (Ovis aries L.) is used to investigate associations between MHC variation, juvenile survival, and parasite resistance. We show in an unmanaged, nonhuman population that allelic variation within the MHC is significantly associated with differences in both juvenile survival and resistance to intestinal nematodes. Certain MHC alleles are associated with low survivorship probabilities and high levels of parasitism or vice versa. We conclude that parasites are likely to play a major role in the maintenance of MHC diversity in this population.

Figure 1

Part of sheep chromosome 20 showing the MHC (indicated by box) and the names and locations of the microsatellite markers used in this study. Genetic distances and nomenclature are taken from Crawford (35). D_IS*, the within cohort component of linkage disequilibrium adjusted for heterozygosity, and significance levels of linkage disequilibrium between neighboring pairs of markers in the St. Kilda Soay sheep population (55) also are shown.