Diversity of MHC IIB genes and parasitism in hybrids of evolutionarily divergent cyprinoid species indicate heterosis advantage

Andrea Šimková,Michal Janáč,Mária Seifertová,Lukáš Vetešník,Kristína Civáňová,Lenka Gettová

doi:10.1038/s41598-021-96205-x

Abstract

The genes of the major histocompatibility complex (MHC) are an essential component of the vertebrate immune system and MHC genotypes may determine individual susceptibility to parasite infection. In the wild, selection that favors MHC variability can create situations in which interspecies hybrids experience a survival advantage. In a wild system of two naturally hybridizing leuciscid fish, we assessed MHC IIB genetic variability and its potential relationships to hosts’ ectoparasite communities. High proportions of MHC alleles and parasites were species-specific. Strong positive selection at specific MHC codons was detected in both species and hybrids. MHC allele expression in hybrids was slightly biased towards the maternal species. Controlling for a strong seasonal effect on parasite communities, we found no clear associations between host-specific parasites and MHC alleles or MHC supertypes. Hybrids shared more MHC alleles with the more MHC-diverse parental species, but expressed intermediate numbers of MHC alleles and positively selected sites. Hybrids carried significantly fewer ectoparasites than either parent species, suggesting a hybrid advantage via potential heterosis.

Highlights

The genes of the major histocompatibility complex (MHC) are an essential component of the vertebrate immune system and MHC genotypes may determine individual susceptibility to parasite infection
The authors reported the expression of an intermediate number of MHC IIB alleles in hybrids of the first generation (F1 hybrids), representing their potential advantage; hybrids expressed a higher proportion of MHC genes of more genetically variable species, i.e. native P. toxostoma
Hybridization is a common phenomenon in fish[9,40]; prior to this study, the variability in functional immune genes in naturally distributed fish hybrids coexisting in the same natural habitats with their parental species was only rarely investigated[26]

Summary

Introduction

The genes of the major histocompatibility complex (MHC) are an essential component of the vertebrate immune system and MHC genotypes may determine individual susceptibility to parasite infection. In hybrids of wild living vertebrates, selection may favor the variability of immune genes associated with high resistance to parasites, and potentially interspecies hybrids may through the variability of immune genes exhibit a survival advantage over parents. Concerning wildliving vertebrates, the genetic variation in MHC genes between hybridizing species was studied, and adaptive MHC introgression was documented, especially in newts[23,24,25]. The authors reported the expression of an intermediate number of MHC IIB alleles in hybrids of the first generation (F1 hybrids), representing their potential advantage; hybrids expressed a higher proportion of MHC genes of more genetically variable species, i.e. native P. toxostoma. Paternal effects have been reported for innate immunity[28] This may evoke the question of whether the direction of genetic introgression affects hybrid immunocompetence and susceptibility to parental species-specific parasites

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