Modes of Salmonid MHC Class I and II Evolution Differ from the Primate Paradigm

Abstract

Rainbow trout (Oncorhynchus mykiss) and brown trout (Salmo trutta) represent two salmonid genera separated for 15–20 million years. cDNA sequences were determined for the classical MHC class I heavy chain gene UBA and the MHC class II β-chain gene DAB from 15 rainbow and 10 brown trout. Both genes are highly polymorphic in both species and diploid in expression. The MHC class I alleles comprise several highly divergent lineages that are represented in both species and predate genera separation. The class II alleles are less divergent, highly species specific, and probably arose after genera separation. The striking difference in salmonid MHC class I and class II evolution contrasts with the situation in primates, where lineages of class II alleles have been sustained over longer periods of time relative to class I lineages. The difference may arise because salmonid MHC class I and II genes are not linked, whereas in mammals they are closely linked. A prevalent mechanism for evolving new MHC class I alleles in salmonids is recombination in intron II that shuffles α1 and α2 domains into different combinations.

Patterns of variability at the major histocompatibility class II alpha locus in Atlantic salmon contrast with those at the class I locus

“…Branch lengths in each lineage were short, with low genetic distances suggesting a recent origin of the alleles at this locus (Shum et al 2001;Stet et al 2002). The class II alleles described in this study in both Norwegian and Irish populations have low divergence and all three new Irish alleles are located in one of the pre-existing clusters of shared alleles.…”

“…The existence of a large intron between α1 and α2 domains of the salmonid MH class I gene, where potential PBRs are located, may provide an additional mechanism for increasing variability through allele shuffling (Shum et al 2001;Grimholt et al 2002) compared to class II, where potential PBRs are only encoded in exon 2. In fact, the number of recombination events at the class II alpha locus was lower than that observed for the same populations for the class I locus, even when considering both class I domains independently.…”

“…Salmonids in general, and Atlantic salmon in particular, have proved to be a good model to analyse the mechanisms of MHC evolution because (1) as in the rest of the teleosts, class I and class II loci are not physically linked, allowing independent evolution of both classes of genes [as the class I and class II genes do not form a complex they are known as MH genes in teleosts (Stet et al 2003)], (2) single class I and class II MH loci are expressed (Shum et al 2001;Stet et al 2002;Grimholt et al 2002), making analyses simpler, and (3) most of the present distribution of the species was colonized from refugia after the last glaciation (Hewitt 1999), making possible the study of adaptation of similar lineages colonising different environments and the analysis of molecular evolution on a relatively short temporal scale.…”

“…It is not known, however, whether the class II loci (Sasa-DAA and Sasa-DAB), that are tightly linked to each other but not linked to class I (Grimholt et al 2000;Stet et al 2002), are evolving the same way in the short term. In particular, it is not known whether the role of recombination in generating new alleles is as important in class II as it appears to be in class I for salmonid fish (Shum et al 2001;Consuegra et al, submitted).…”

“…In primates, class II loci show trans-species sharing of allelic lineages that is not seen at class I loci (Boyson et al 1996;Seddon and Ellegren 2002). In contrast, in cyprinids and salmonids class I alleles represent highly divergent and ancient allelic lineages while class II alleles are more recent (Shum et al 2001;Stet et al 2002;Kruiswijk 2002). …”