Evaluating Patterns of Convergent Evolution and Trans-Species Polymorphism at MHC Immunogenes in Two Sympatric Stickleback Species

Abstract

The immunologically important major histocompatibility complex (MHC) harbors some of the most polymorphic genes in vertebrates. These genes presumably evolve under parasite-mediated selection and frequently show inconsistent allelic genealogies, where some alleles are more similar between species than within species. This phenomenon is thought to arise either from convergent evolution under parallel selection or from the preservation of ancient allelic lineages beyond speciation events (trans-species polymorphism, TSP). Here, we examine natural populations of two sympatric stickleback species (Gasterosteus aculeatus and Pungitius pungitius) to investigate the contribution of these two mechanisms to the evolution of inconsistent allelic genealogies at the MHC. Overlapping parasite taxa between the two host species in three different habitats suggest contemporary parallel selection on the MHC genes. Accordingly, we detected a lack of species-specific phylogenetic clustering in the immunologically relevant antigen-binding residues of the MHC IIB genes which contrasted with the rest of the coding and noncoding sequence.However, clustering was not habitat-specific and a codon-usage analysis revealed patterns of similarity by descent. In this light, common descent via TSP, in combination with intraspecies gene conversion, rather than convergent evolution is the more strongly supported scenario for the inconsistent genealogy at the MHC. K E Y W O R D S :Balancing selection, major histocompatibility complex (MHC), nine-spined stickleback, peptide-binding region (PBR), sequence evolution, three-spined stickleback.

MHC class II variation in a rare and ecological specialist mouse lemur reveals lower allelic richness and contrasting selection patterns compared to a generalist and widespread sympatric congener

“…Nucleotide and amino acid sequence similarity between alleles of the two species, as well as the presence of a two-codon insertion located at the same position in 19 Mimu - and 7 Mibe -DQB sequences, could indicate the retention of MHC motifs in both loci during periods of time exceeding the evolutionary split between species (trans-species polymorphism; Klein 1987). MHC sequence similarity limited to exons encoding peptide binding regions have been detected many times between species that were sometimes distantly related (summarised in Klein et al 2007; Lenz et al 2013) and may represent examples of trans-species polymorphism or result from convergent evolution (independent evolution of similar traits in response to similar ecological pressures) (e.g. Klein et al 2007).…”

Stepwise Threshold Clustering: A New Method for Genotyping MHC Loci Using Next-Generation Sequencing Technology

“…Similarly, the same sequence was found in a highly conserved cluster of similar sequences in a sample of 30 threespine stickleback and in a sample of 30 nine-spine stickleback ( Pungitius pungitius ) [33]. These authors speculated that these sequences, because of their lack of diversity among individuals, could potentially originate from an invariant MHC class-II like locus involved in antigen processing [81].…”

“…In practice, a locus by locus approach is usually not feasible, for several reasons. First, MHC loci often share allelic lineages (groups of similar alleles that are highly divergent from other such groups) which can persist even beyond speciation events [31]–[33]. Second, different MHC loci can exhibit substantial sequence similarity due to the high rates of inter-locus recombination and gene conversion [34]–[36].…”

“…Given these challenges, sequencing MHC loci in non-model organisms has, until recently, been accomplished by 1) extensive bacterial cloning and direct sequencing [33] or 2) conformation based detection methods [24], [38]–[41]. The latter approaches rely on running PCR-amplified sequences through a charged gel matrix or capillary sequencer to identify alleles based on differences in DNA strand mobility.…”

Evolution of MHC class I genes in the endangered loggerhead sea turtle (Caretta caretta) revealed by 454 amplicon sequencing

“…[9-12]. TSP can occur either through allelic lineages being maintained over long periods of time across speciation events [13,14] or through convergent evolution presumably due to similar parasite pressures [15,16]. Secondly, genetic diversity at MHC loci has been used to measure the immunological fitness of wild populations [1].…”