MHC evolution in three salmonid species: a comparison between class II alpha and beta genes

Abstract

The genes of the major histocompatibility complex (MHC) are amongst the most variable in vertebrates and represent some of the best candidates to study processes of adaptive evolution. However, despite the number of studies available, most of the information on the structure and function of these genes come from studies in mammals and birds in which the MHC class I and II genes are tightly linked and class II alpha exhibits low variability in many cases. Teleost fishes are among the most primitive vertebrates with MHC and represent good organisms for the study of MHC evolution because their class I and class II loci are not physically linked, allowing for independent evolution of both classes of genes. We have compared the diversity and molecular mechanisms of evolution of classical MH class II alpha and class II beta loci in farm populations of three salmonid species: Oncorhynchus kisutch, Oncorhynchus mykiss and Salmo salar. We found single classical class II loci and high polymorphism at both class II alpha and beta genes in the three species. Mechanisms of evolution were common for both class II genes, with recombination and point mutation involved in generating diversity and positive selection acting on the peptide-binding residues. These results suggest that the maintenance of variability at the class IIalpha gene could be a mechanism to increase diversity in the MHC class II in salmonids in order to compensate for the expression of one single classical locus and to respond to a wider array of parasites.

Characterization of MHC class II genes in the critically endangered European eel (Anguilla anguilla)

“…Nonetheless, MHC IIA diversity similar to that of MHC IIB has been described for the salmonid DAA and the mammalian DQA loci (Reche and Reinherz 2003;Gomez et al 2010;Sin et al 2012). Whether this pattern holds true on a larger scale for the European eel MHC remains to be determined.…”

“…Nonetheless, positive selection seems to be important at sites that are potentially in direct contact with self and parasite-derived antigens. And third, it might be a peculiarity of basal teleosts since certain Oncorhynchus species were also lacking a clear signal of positive selection for MHC IIB (Aguilar and Garza 2007;Gomez et al 2010). Furthermore, MHC IIA of O. mykiss was shown to be under strong positive selection (Liu et al 2013).…”

Selection and genetic drift in captive versus wild populations: an assessment of neutral and adaptive (MHC-linked) genetic variation in wild and hatchery brown trout (Salmo trutta) populations

“…Tree topologies were calculated by the Maximum Likelihood algorithm implemented in MEGA 5.2 whereby the best fitting substitution model was evaluated with jModeltest 2.1.4 (Darriba et al 2012) for each dataset separately. A Wilcoxon signedrank test was used to test for differing dN/dS ratios between antigen-binding sites (ABS) and non-ABS, as defined by the human model (Brown et al 1993) and applied to salmonid fishes (Aguilar and Garza 2007;Gómez et al 2010).…”

Maintaining functional major histocompatibility complex diversity under inbreeding: the case of a selfing vertebrate

“…This is because too much allelic diversity could result in a reduction in T-cell receptor diversity driven by negative selection, ultimately reducing the ability to fight infection [25]. Evidence of MHC heterozygote advantage [26,27], rare-allele advantage [28], association of individual MHC genotypes or alleles with susceptibility to infection [29,30] and shifts in allele frequencies after exposure [31] suggest that parasites are the primary source of selection on MHC.…”