Widespread Adaptive Introgression of Major Histocompatibility Complex Genes across Vertebrate Hybrid Zones

Abstract

Interspecific introgression is a potentially important source of novel variation of adaptive significance. Although multiple cases of adaptive introgression are well documented, broader generalizations about its targets and mechanisms are lacking. Multi-allelic balancing selection, particularly when acting through rare allele advantage, is an evolutionary mechanism expected to favor adaptive introgression. This is because introgressed alleles are likely to confer an immediate selective advantage, facilitating their establishment in the recipient species even in the face of strong genomic barriers to introgression. Vertebrate Major Histocompatibility Complex (MHC) genes are well-established targets of long-term multi-allelic balancing selection, so widespread adaptive MHC introgression is expected. Here we evaluate this hypothesis using data from 29 hybrid zones formed by fish, amphibians, squamates, turtles, birds and mammals at advanced stages of speciation. The key prediction of more extensive MHC introgression compared to genome-wide introgression was tested with three complementary statistical approaches. We found evidence for widespread adaptive introgression of MHC genes, providing a link between the process of adaptive introgression and an underlying mechanism. Our work identifies MHC introgression as a general mechanism by which species can acquire novel, and possibly regain previously lost, variation that may enhance defense against pathogens and increase adaptive potential.