Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.)

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.Maintenance of genetic diversity at the major histocompatibility complex (MHC) of vertebrates has become a paradigm for the manner in which genetic diversity may be maintained in natural populations (1). The MHC consists of a group of closely linked genes involved in antigen presentation to the vertebrate immune system (2) and is remarkable in that extremely high levels of heterozygosity are commonly observed at certain genes contained within the complex (1, 3).Several lines of evidence indicate that the high allelic diversity observed at the MHC is maintained through some form of selective force. First, where genealogies of MHC allele sequences have been constructed from a number of species [for example, primates (4) and felines (5)] it is observed that the divergence of allelic MHC lineages predates the speciation event giving rise to separate taxa. This suggests the action of some form of balancing selection over long periods of evolutionary time. Second, comparisons of allelic sequences present within mice and human populations indicate that the rate of nonsynonymous (coding) substitution exceeds the rate of synonymous (noncoding) substitution at the antigen presenting site, thus favoring new MHC variants and increasing diversity (6-8). Finally, in human populations the large numbers of alleles present at MHC loci show a relatively even distribution, leading to higher levels of heterozygosity than may be explained under neutral theory (9) and suggesting the action of recent balancing selection. So far, however, most studies of MHC polymorphism have been confined to human or semicaptive mouse populations, and there is a paucity of population-based studies within natural populations of other vertebrates.Despite strong evidence for balancing selection at the MHC, the mechanisms behind maintenance of MHC polymorphism are still unclear. Two broad categories of selective mechanisms have been proposed. Reproductive...

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“…Thus, replicating results in a second family where the polymorphism is not segregating is not possible. Polymorphisms may not be segregating in families due to low allele frequencies in the breed, or because the polymorphism is (Schwaiger et al, 1995 ;Outteridge et al, 1996;Paterson et al, 1998 ;Coltman et al, 2001 ;Patterson et al, 2001;Davies et al, 2006). However, this study found no validated SNP in these regions.…”

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“…Acvedo-Whitehouse et al 2003) and parasites (e.g. Paterson et al 1998). Therefore, genetically impoverished populations are expected to be more vulnerable to both lowered reproduction and increased mortality.…”

MHC influences infection with parasites and winter survival in the root vole Microtus oeconomus

“…Nevertheless, survival-related MHC alleles have been observed in the Seychelles warbler (Brouwer et al 2010), Soay sheep (Paterson et al 1998), and brushtail possum (Banks et al 2010). Additionally, several other studies have documented this relationship in the context of parasitic infections.…”

“…Additionally, several other studies have documented this relationship in the context of parasitic infections. For example, a higher survival rate of heterozygotes has been observed in red junglefowl during an outbreak of coccidiosis (Worley et al 2010), and a study of the Soay sheep revealed lower mortality in juveniles possessing MHC alleles associated with resistance against helminths (Paterson et al 1998). Among fish species, MHC genotype influenced the survival of embryos that had been exposed to bacterial infection (Wedekind et al 2004), and individuals with homozygous MHC genotypes survived better when infected with flukes than did heterozygotes (Hedrick et al 2001).…”