A global analysis of selection at the avian MHC

Abstract

Recent advancements in sequencing technology have resulted in rapid progress in the study of the major histocompatibility complex (MHC) in non-model avian species. Here, we analyze a global dataset of avian MHC class I and class II sequences (ca. 11,000 sequences from over 250 species) to gain insight into the processes that govern macroevolution of MHC genes in birds. Analysis of substitution rates revealed striking differences in the patterns of diversifying selection between passerine and non-passerine birds. Non-passerines showed stronger selection at MHC class II, which is primarily involved in recognition of extracellular pathogens, while passerines showed stronger selection at MHC class I, which is involved in recognition of intracellular pathogens. Positions of positively selected amino-acid residues showed marked discrepancies with peptide-binding residues (PBRs) of human MHC molecules, suggesting that using a human classification of PBRs to assess selection patterns at the avian MHC may be unjustified. Finally, our analysis provided evidence that indel mutations can make a substantial contribution to adaptive variation at the avian MHC.

“Balancing” balancing selection? Assortative mating at the major histocompatibility complex despite molecular signatures of balancing selection

“… The estimated proportion of sites subject to purifying selection, neutral evolution (drift), and positive selection are denoted by p 0 , p 1 , and p 2 respectively. Underlining denotes codons that correspond to antigen‐binding sites in humans (Brown et al ); asterisks denote codons that are positively selected in passerines in general (Minias et al, ). …”

“… Underlining denotes codons that correspond to antigen‐binding sites in humans (Brown et al ); asterisks denote codons that are positively selected in passerines in general (Minias et al, ). …”

“…Two of these, based on alignment to human MHC sequence, correspond to antigen‐binding positions that are likely to experience particularly intense selection (Hughes & Hughes, ). Moreover, four of the six codons identified correspond to the consensus of positively selected sites across passerines (Minias et al, ). The remaining positively selected codon (site 24) did not correspond to an antigen‐binding position based on sequence alignment with human MHC, nor was it reported to be positively selected site across passerines in general (Minias et al, ).…”

“…Moreover, four of the six codons identified correspond to the consensus of positively selected sites across passerines (Minias et al, ). The remaining positively selected codon (site 24) did not correspond to an antigen‐binding position based on sequence alignment with human MHC, nor was it reported to be positively selected site across passerines in general (Minias et al, ). Positive selection at MHC is widespread: In a recent review of the literature (25 publications on 25 vertebrate species), positive selection within the peptide‐binding region of MHC was reported in every study (Slade, ).…”

“…First, chemical composition of preen oil covaries with MHC class II genotype (Slade et al, ), raising the possibility that olfactory cues of class II similarity could facilitate nonrandom mating. Second, this region shows the highest individual‐ and population‐level variability in song sparrows (Slade, Sarquis‐Adamson, Gloor, Lachance, & MacDougall‐Shackleton, ) and other passerines (Minias et al, ). Song sparrows show as many as 26 alleles per individual at MHC class II, implying at least 13 loci (Slade, Sarquis‐Adamson, et al, ), and common yellowthroats as many as 39 alleles per individual, implying at least 20 loci (Bollmer et al, ).…”