Evolution of MHC class I genes in Japanese and Russian raccoon dogs, Nyctereutes procyonoides (Carnivora: Canidae)

Abstract

Major histocompatibility complex (MHC) genes have been widely studied to assess the immunological fitness and evolutionary adaptation of animal populations. Among the Canidae, the raccoon dog’s adventurous nature, omnivorous behavior, and high variability of intracellular pathogens make it ideal to study selection on MHC class I in a non-model canid species. Here, we examined allelic diversity and evolutionary patterns of MHC class I genes in the raccoon dog (Nyctereutes procyonoides). We identified 48 novel MHC class I alleles from 31 raccoon dogs from Japan and Russia. Some alleles were geographically restricted, whereas others were widely distributed across the species’ range. The rate of non-synonymous substitutions was greater than that of synonymous substitutions for both exon 2 and exon 3 encoding α1 and α2 domains, respectively, in the α chain of the MHC class I protein. Positively selected sites at the amino acid level were evident in both the α1 and α2 domains, and a recombination breakpoint was found in exon 3. Bayesian phylogenetic trees showed no evidence of trans-species polymorphism (TSP) with alleles from carnivoran species in other families but did detect TSP between raccoon dogs and the domestic dog, Canis familiaris, indicative of long-term balancing selection in canids. Our results indicate that the extensive allelic diversity of MHC class I in Japanese and Russian raccoon dogs has been influenced and maintained by pathogen-driven positive selection, recombination, and long-term balancing selection.Supplementary InformationThe online version contains supplementary material available at 10.1007/s13364-021-00561-y.