Coloniality and migration are related to selection on MHC genes in birds

Abstract

The major histocompatibility complex (MHC) plays a key role in pathogen recognition as a part of the vertebrate adaptive immune system. The great diversity of MHC genes in natural populations is maintained by different forms of balancing selection and its strength should correlate with the diversity of pathogens to which a population is exposed and the rate of exposure. Despite this prediction, little is known about how life-history characteristics affect selection at the MHC. Here, we examined whether the strength of balancing selection on MHC class II genes in birds (as measured with nonsynonymous nucleotide substitutions, dN) was related to their social or migratory behavior, two life-history characteristics correlated with pathogen exposure. Our comparative analysis indicated that the rate of nonsynonymous substitutions was higher in colonial and migratory species than solitary and resident species, suggesting that the strength of balancing selection increases with coloniality and migratory status. These patterns could be attributed to: (1) elevated transmission rates of pathogens in species that breed in dense aggregations, or (2) exposure to a more diverse fauna of pathogens and parasites in migratory species. Our study suggests that differences in social structure and basic ecological traits influence MHC diversity in natural vertebrate populations.

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

“…It is possible, however, that combinations of rare alleles may be associated with decreased infection in FL, but our sample sizes are too small to test for such an association. Overall, our results for class I are consistent with the hypothesis that migratory behaviour is associated with increased MHC diversity, as suggested by comparative studies (Buehler et al ., ; Minias et al ., ), and a comparison of closely related migratory and resident warbler species (Richardson & Westerdahl, ).…”

“…However, little is known about how life‐history traits, that may affect exposure to parasites, are related to MHC variation (Šimková et al ., ). The results of a recent comparative study of nonpasserine birds showed that MHC class I diversity was positively associated with both coloniality and migratory behaviour across species (Minias et al ., ), suggesting that these traits play an important role in shaping genetic variation at MHC genes.…”

“…Comparative studies support the prediction that species that are migratory will have greater MHC diversity than those that remain in the same location all year (Westerdahl et al ., ; Shiina et al ., ; Buehler et al ., ; Minias et al ., ); however, studies of closely related species, or populations of the same species that differ in migratory behaviour are rare. One interspecific study found greater MHC class I diversity in a widespread migratory warbler than in a closely related island resident species; however, the island species experienced a population bottleneck that reduced overall genetic diversity and this could have confounded the comparison (Richardson & Westerdahl, ).…”

“…Across taxa, there is mounting evidence that MHC variation is related to the diversity of pathogens and parasites to which populations are exposed (Wegner et al, 2003;Prugnolle et al, 2005;Simkov a et al, 2006;Go€ uy de Bellocq et al, 2008) and, thus, identifying which factors influence exposure to pathogens has become an important research focus. Although environmental conditions are considered an important factor influencing exposure to pathogens (Valkiunas, 2005;Dionne et al, 2007;Møller & Sz ep, 2011), little attention has been given to the role of life-history traits ( Simkov a et al, 2006;Minias et al, 2017).…”

Infection risk and extensive parental care govern the molecular evolution of Toll-like receptors in birds

“…Despite recent advances (Minias, et al 2017;O'Connor, et al 2018), it remains generally 72 unknown how pathogen-mediated selection affects immune gene evolution across species. Do signatures of positive selection mostly evolve convergent, or do they evolve divergent 74 depending on pathogen exposure and life-history trade-offs?…”