A rare MHC haplotype confers selective advantage in a free-living ruminant

Genes within the major histocompatibility complex (MHC) are the most variable identified in vertebrates. Pathogen-mediated selection (PMS) is believed to be the main force maintaining diversity at MHC class I and II genes, but it has proven hard to demonstrate the exact PMS regime that is acting in natural populations. Demonstrating contemporary selection on MHC alleles is not trivial, and previous work has been constrained by limited genetic tools, low sample sizes and short time scales and has sometimes involved anticonservative statistical approaches. Here, we use appropriate statistical approaches to examine associations between MHC variation and several fitness measurements including total fitness (lifetime breeding success) and five fitness components, in 3400 wild Soay sheep (Ovis aries) monitored over their lifetimes between 1989 and 2012. We found haplotypes C and D were associated with decreased and increased male total fitness respectively. In terms of fitness components, juvenile survival was positively associated with haplotype divergence. Of the eight MHC haplotypes (A-H), haplotypes C and F were associated with decreased adult male breeding success and decreased adult female life span respectively. Consistent with the increased male total fitness, haplotype D, which is the rarest, has increased in frequency throughout the study period. Our results suggest that contemporary balancing selection is acting on MHC class II genes in Soay sheep and that different selection mechanisms are acting between juveniles and adults.