Trans-specific polymorphism and the convergent evolution of supertypes in MHC class II genes in Darters (Etheostoma)

Major Histocompatibility Complex (MHC) genes are one of the most
polymorphic gene groups known in vertebrates. MHC genes also exhibit
allelic variants that are shared among taxa, referred to as trans-specific
polymorphism (TSP). The role that selection plays in maintaining such high
diversity within species, as well as TSP, is an ongoing discussion in
biology. In this study we used deep-sequencing techniques to characterize
MHC class IIb gene diversity in three sympatric species of darters. We
found at least 5 copies of the MHC gene in darters, with 126 genetic
variants encoding 122 unique amino acid sequences. We identified four
supertypes based on the binding properties of proteins encoded by the
sequences. Although each species had a unique pool of variants, many
variants were shared between species pairs and across all three species.
Phylogenetic analysis showed that the variants did not group together
monophyletically based on species identity or on supertype. An expanded
phylogenetic analysis showed that some darter alleles grouped together
with alleles from other percid fishes. Our findings show that TSP occurs
in darters, which suggests that balancing selection is acting at the
genotype level. Supertypes, however, are most likely evolving
convergently, as evidenced by the fact that alleles do not form
monophyletic groups based on supertype. Our research demonstrates that
selection may be acting differently on MHC genes at the genotype and
supertype levels, selecting for the maintenance of high genotypic
diversity while driving the convergent evolution of similar MHC phenotypes
across different species.