Sexual selection and the evolutionary dynamics of the major histocompatibility complex

Abstract

The genes of the major histocompatibility complex (MHC) are a key component of the adaptive immune system and among the most variable loci in the vertebrate genome. Pathogen-mediated natural selection and MHC-based disassortative mating are both thought to structure MHC polymorphism, but their effects have proven difficult to discriminate in natural systems. Using the first model of MHC dynamics incorporating both survival and reproduction, we demonstrate that natural and sexual selection produce distinctive signatures of MHC allelic diversity with critical implications for understanding host-pathogen dynamics. While natural selection produces the Red Queen dynamics characteristic of host-parasite interactions, disassortative mating stabilizes allele frequencies, damping major fluctuations in dominant alleles and protecting functional variants against drift. This subtle difference generates a complex interaction between MHC allelic diversity and population size. In small populations, the stabilizing effects of sexual selection moderate the effects of drift, whereas pathogen-mediated selection accelerates the loss of functionally important genetic diversity. Natural selection enhances MHC allelic variation in larger populations, with the highest levels of diversity generated by the combined action of pathogen-mediated selection and disassortative mating. MHC-based sexual selection may help to explain how functionally important genetic variation can be maintained in populations of conservation concern.

Patterns of MHC‐dependent mate selection in humans and nonhuman primates: a meta‐analysis

“…; Ejsmond et al . ). Proximate mechanisms enabling MHC‐mediated mate choice include odour and visual cues of MHC composition.…”

Pathogen richness and abundance predict patterns of adaptive major histocompatibility complex variation in insular amphibians

“…The major histocompatibility complex (MHC) is one of the most polymorphic regions in the vertebrate genome and plays a critical role in pathogen detection, recognizing and presenting foreign antigens and triggering the adaptive immune response (Kelley, Walter, & Trowsdale, ). It is generally hypothesized that MHC diversity is maintained by pathogen‐mediated balancing selection through mechanisms including heterozygote advantage and negative frequency‐dependent selection, and by sexual selection for MHC‐dissimilar mates (Ejsmond, Radwan, & Wilson, ; Milinski, ; Spurgin & Richardson, ). At the same time, spatial heterogeneity in the distribution of pathogen communities may lead to diversifying selection, generating spatially segregated patterns of MHC variation (Eizaguirre, Lenz, Kalbe, & Milinski, ; Loiseau et al., ; Marsden et al., ).…”

Major histocompatibility complex similarity and sexual selection: different does not always mean attractive

“…The major histocompatibility complex (MHC), a group of highly polymorphic genes responsible for disease resistance and immune function in vertebrates (Bernatchez & Landry 2003), is likely to be involved in determining compatibility between mates (Tregenza & Wedell 2000;Ejsmond et al 2014). In a sexual selection context, MHC-driven female choice can evolve as a means of increasing MHC heterozygosity in the offspring or avoiding inbreeding, with the relative importance of these mechanisms depending on the relative risk and costs of inbreeding and pathogen-related diseases in the population (Reusch et al 2001).…”