Selection, drift, and introgression shape MHC polymorphism in lizards.

ABSTRACT

The major histocompatibility complex (MHC) has long served as a model for the evolution of adaptive genetic diversity in wild populations. Pathogen-mediated selection is thought to be a main driver of MHC diversity, but it remains elusive to what degree selection shapes MHC diversity in complex biogeographical scenarios where other evolutionary processes (e.g. genetic drift and introgression) may also be acting. Here we focus on two closely related green lizard species, Lacerta trilineata and L. viridis, to address the evolutionary forces acting on MHC diversity in populations with different biogeographic structure. We characterized MHC class I exon 2 and exon 3, and neutral diversity (microsatellites), to study the relative importance of selection, drift, and introgression in shaping MHC diversity. As expected, positive selection was a significant force shaping the high diversity of MHC genes in both species. Moreover, introgression significantly increased MHC diversity in mainland populations, with a primary direction of gene flow from L. viridis to L. trilineata. Finally, we found significantly fewer MHC alleles in island populations, but maintained MHC sequence and functional diversity, suggesting that positive selection counteracted the effect of drift. Overall, our data support that different evolutionary processes govern MHC diversity in different biogeographical scenarios positive selection occurs broadly while introgression acts in sympatry and drift when the population sizes decrease.