Forces shaping major histocompatibility complex evolution in two hyena species

Abstract

Genes of the mammalian major histocompatibility complex (MHC) are central to adaptive immunity. High levels of observed polymorphism at MHC loci have been hypothesized to be maintained by natural selection acting to preserve alleles for pathogen resistance. Here we examined patterns of multilocus MHC diversity in natural populations of 2 closely related carnivore species: spotted hyenas (Crocuta crocuta) and striped hyenas (Hyaena hyaena). We also tested hypotheses suggesting specific selection pressures favoring MHC diversity in these hyena species. We found several lines of evidence consistent with positive selection acting at multiple MHC loci in both species. These included high allelic variation, pervasive gene duplication, transspecies segregation of alleles, and codons evolving under positive selection that disproportionately map to known antigen-binding regions. Despite striking behavioral differences between these 2 hyaenids with respect to their mating systems and social behavior, we found no qualitative species differences in MHC loci, nor did we detect differences in the strength of natural selection. Our findings suggest that ancient shared selection pressures, including a common ancestral pattern of carrion feeding, has influenced MHC diversity more strongly in these hyena species than have selection pressures imposed relatively recently by sociality or sexual selection.