Major histocompatibility complex variation and blood parasites in resident and migratory populations of the common yellowthroat

Abstract

Genes of the major histocompatibility complex (MHC) are a critical part of the adaptive immune response, and the most polymorphic genes in the vertebrate genome, especially in passerine birds. This diversity is thought to be influenced by exposure to pathogens which can vary in relation to numerous factors. Migratory behaviour may be a particularly important trait to consider because migratory birds are exposed to a greater number of different pathogens and parasites at both breeding (i.e. temperate) and overwintering (i.e. tropical and subtropical) areas, as well as at stopover sites during migration. Thus, migrants are predicted to have greater MHC diversity than residents. We compared MHC variation, at both class I and II, and levels of haemosporidian infection between one resident and two migratory populations of the common yellowthroat (Geothlypis trichas). We found that residents were less likely to be infected with haemosporidian parasites and had lower MHC diversity at class I; however, variation at MHC class II was greater in residents than migrants, contrary to our prediction. These patterns were not likely to be caused by differences in population demography as genomewide heterozygosity (based on 9225 single nucleotide polymorphisms) was high in all three populations and not correlated with MHC variation. Our different results for MHC class I and II suggest that studies of immune gene variation in relation to life history need to consider that there could be different selection pressures arising from intracellular (class I) and extracellular (class II) pathogens in different populations.

Evolution of Copy Number at the MHC Varies across the Avian Tree of Life

“…While this hypothesis needs further testing, we also have to acknowledge that the link between migration and the mechanisms shaping genetic variation at the two MHC classes may differ between species. For example, a recent study by Whittingham et al. (2018) revealed higher MHC class I, but not class II, diversity in migratory than resident populations of the common yellowthroat.…”

Non-random association of MHC-I alleles in favor of high diversity haplotypes in wild songbirds revealed by computer-assisted MHC haplotype inference using the R package MHCtools

“…The MHC exhibits extraordinary evolutionary dynamics with rapid expansions and contractions of MHC gene copy number, and substantial variation in MHC sequence and haplotype structure (Kelley, Walter, & Trowsdale, 2005;Minias et al, 2018;Masatoshi Nei & Rooney, 2005;O'Connor et al, 2016;Ohta, 1991;Spurgin et al, 2011). Thus, previous studies have reported considerable variation in the number of different MHC alleles between individuals within species, suggesting that MHC gene copy number variation may be a common trait, at least among birds (Biedrzycka, O'Connor, et al, 2017;Gaigher et al, 2016;Roved et al, 2018;Stervander, Dierickx, Thorley, Brooke, & Westerdahl, 2020;Whittingham, Dunn, Freeman-Gallant, Taff, & Johnson, 2018). Our analyses of MHC-I haplotypes confirmed previous indications of substantial MHC-I gene copy number variation in the great reed warbler (O'Connor et al, 2016;Roved et al, 2018), with a minimum of 4 and a maximum of 21 different MHC-I alleles per haplotype (Fig.…”

Sex and hatching order modulate the association between MHC‐II diversity and fitness in early‐life stages of a wild seabird

“…For instance, increased mean MHC diversity has been associated with migratory behaviour and female promiscuity, two traits that may increase exposure and/or reduce immune response to parasites (Gohli et al, 2013;Minias, Pikus, Whittingham, & Dunn, 2019;Whittingham, Dunn, Freeman-Gallant, Taff, & Johnson, 2018;Winternitz et al, 2013). In contrast, studies investigating interindividual variation in the fitness consequences of MHC diversity within a population are scarce, although there is extensive evidence for interindividual variations in these potential selective pressures (i.e., exposure to parasites, immune response strength or susceptibility to autoimmunity).…”