Sex-dependent influence of major histocompatibility complex diversity on fitness in a social mammal

Abstract

Parasite infections affect males and females differently across a wide range of species, often due to differences in immune responses. Generally, females tend to have stronger immune defenses and lower parasite loads than males. The major histocompatibility complex (MHC) plays a crucial role in the adaptive immune response, and extensive research has explored how variation in this region influences infection and fitness outcomes. However, studies of sex-specific relationships between MHC variation and infection are scarce, perhaps because MHC genes are located on the autosomes, which are shared by both sexes. Here, we provide evidence of sexually antagonistic selection in a wild, group-living mammal--the banded mongoose. Using genetic and life history data collected from over 300 individuals across 25 years, we found that particularly MHC class I (MHC-I) but also MHC class II (MHC-II) diversity influence lifetime reproductive success differently in males and females. Specifically, higher MHC diversity is linked to increased fitness in males but decreased fitness in females. Furthermore, MHC diversity did not differ between the sexes, indicating an unresolved genetic sexual conflict. Our findings demonstrate that sexually antagonistic selection acts on the MHC and may operate across both MHC classes but differently. This study contributes to the growing body of evidence that sex is a significant factor in shaping host immunity and fitness.