Diversifying selection and climatic effects on major histocompatibility complex class II gene diversity in the...

Heterogeneous pathogenic stress can shape major histocompatibility complex (MHC) diversity by influencing the functional plasticity of the immune response. Therefore, MHC diversity could reflect environmental stress, demonstrating its importance in uncovering the mechanisms of adaptive genetic variation. In this study, we combined neutral microsatellite loci, an immune-related MHC II-DRB locus, and climatic factors to unravel the mechanisms affecting the diversity and genetic differentiation of MHC genes in the greater horseshoe bat (Rhinolophus ferrumequinum), a species with a wide geographical distribution that has three distinct genetic lineages in China. First, increased genetic differentiation at the MHC locus among populations compared using microsatellites indicated diversifying selection. Second, the genetic differentiation of MHC and microsatellites were significantly correlated, suggesting that demographic processes exist. However, MHC genetic differentiation was significantly correlated with geographical distance among populations, even after controlling for the neutral markers, suggesting a major effect of selection. Third, although the MHC genetic differentiation was larger than that for microsatellites, there was no significant difference in the genetic differentiation between the two markers among genetic lineages, indicating the effect of balancing selection. Fourth, combined with climatic factors, MHC diversity and supertypes showed significant correlations with temperature and precipitation, but not with the phylogeographic structure of R. ferrumequinum, suggesting an effect of local adaptation driven by climate on MHC diversity. Moreover, the number of MHC supertypes varied between populations and lineages, suggesting regional characteristics and support for local adaptation. Taken together, the results of our study provide insights into the adaptive evolutionary driving forces at different geographic scales in R. ferrumequinum. In addition, climate factors may have played a vital role in driving adaptive evolution in this species.