Variation in positively selected major histocompatibility complex class I loci in rufous-collared sparrows (Zonotrichia capensis)
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The major histocompatibility complex (MHC) is a highly variable family of genes involved in parasite recognition and the initiation of adaptive immune system responses. Variation in MHC loci is maintained primarily through parasite-mediated selection or disassortative mate choice. To characterize MHC diversity of rufous-collared sparrows (Zonotrichia capensis), an abundant South American passerine, we examined allelic and nucleotide variation in MHC class I exon 3 using pyrosequencing. Exon 3 comprises a substantial portion of the peptide-binding region (PBR) of class I MHC and thus plays an important role in intracellular pathogen defense. We identified 98 putatively functional alleles that produce 56 unique protein sequences across at least 6 paralogous loci. Allelic diversity per individual and exon-wide nucleotide diversity were relatively low; however, we found specific amino acid positions with high nucleotide diversity and signatures of positive selection (elevated d N /d S ) that may correspond to the PBR. Based on the variation in physicochemical properties of amino acids at these “positively selected sites,” we identified ten functional MHC supertypes. Spatial variation in nucleotide diversity and the number of MHC alleles, proteins, and supertypes per individual suggests that environmental heterogeneity may affect patterns of MHC diversity. Furthermore, populations with high MHC diversity have higher prevalence of avian malaria, consistent with parasite-mediated selection on MHC. Together, these results provide a framework for subsequent investigations of selective agents acting on MHC in Z. capensis.
KeywordsGenetic variation Elevational gradient Major histocompatibility complex Natural selection Parasites Zonotrichia capensis
This work was funded by the American Museum of Natural History Frank M. Chapman Fund, Sigma Xi Grant-In-Aid-Of-Research, the American Ornithologists’ Union, and the University of Wyoming. Voucher specimens and pectoral muscle tissue samples of all of the specimens included in this study are accessioned at the Louisiana State University Museum of Natural Science (Baton Rouge), the Museo de Historia Natural, Universidad Nacional Mayor de San Marcos (Lima, Peru), and the Centro de Ornitologia y Biodiversidad (Lima, Peru). The Genome Sequencing and Analysis Core Resource at Duke University sequenced MHC amplicon libraries. We thank Amy Ellison for advice with designing MHC sequencing protocol. We thank Shawn M. Billerman, C. Alex Buerkle, Michael E. Dillon, James M. Maley, Melanie M. Murphy, and three anonymous reviewers for providing helpful comments on the manuscript.
- Hedrick PW (2002) Pathogen resistance and genetic variation at MHC loci. Evolution 56(1902):1908Google Scholar
- R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
- Schulenberg TS, Stotz DF, Lane DF, O’Neill JP, Parker TA III (2007) Birds of Peru. Princeton University Press, Princeton, p 656Google Scholar
- Schut E, Rivero-de Aguilar J, Merino S, Magrath MJL, Komdeur J, Westerdahl H (2011) Characterization of MHC-I in the blue tit (Cyanistes caeruleus) reveals low levels of genetic diversity and trans-population evolution across European populations. Immunogenetics 63:531–542PubMedCentralPubMedCrossRefGoogle Scholar
- Shiina T, Briles WE, Goto RM, Hosomichi K, Yanagiya K, Shimizu S, Inoko H, Miller MM (2007) Extended gene map reveals tripartite motif, C-type lectin, and Ig superfamily type genes within a subregion of the chicken MHC-B affecting infectious disease. J Immunol 178:7162–7172PubMedCrossRefGoogle Scholar
- Stager M, Cerasale DJ, Dor R, Winkler DW, Cheviron ZA (2014) Signatures of natural selection in the mitochondrial genomes of Tachycineta swallows and their implications for latitudinal patterns of the ‘pace of life’. Gene. In press.Google Scholar
- Strandh M, Westerdahl H, Pontarp M, Canbäck B, Dubois MP, Miquel C, Taberlet P, Bonadonna F (2012) Major histocompatibility complex class II compatibility, but not class I, predicts mate choice in a bird with highly developed olfaction. Proc R Soc B 279:4457–4463PubMedCentralPubMedCrossRefGoogle Scholar
- Tao N, Bruno WJ, Abfalterer W, Moret BME, Leitner, T, Kuiken C (2005) FINDMODEL: a tool to select the best-fit model of nucleotide substitution. http://hcv.lanl.gov/content/sequence/findmodel/findmodel.html
- Wallny H-J, Avila D, Hunt LG, Powell TJ, Riegert P, Salomonsen J, Skjødt K, Vainio O, Vilbois F, Wiles MV, Kaufman J (2006) Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC determined response to Rous sarcoma virus in chickens. Proc Natl Acad Sci 103:1434–1439PubMedCentralPubMedCrossRefGoogle Scholar
- Wiseman RW, Karl JA, Bimber BN, O’Leary CE, Lank SM, Tuscher JJ, Detmer AM, Bouffard P, Levenkova N, Turcotte CL, Szekeres E Jr, Wright C, Harkins T, O’Connor DH (2009) Major histocompatibility complex genotyping with massively parallel pyrosequencing. Nat Med 15:1322–1327PubMedCentralPubMedCrossRefGoogle Scholar
- Wucherpfennig KW, Yu B, Bhol K, Monos DS, Argyris E, Karr RW, Ahmed AR, Strominger JL (1995) Structural basis for major histocompatibility complex (MHC)-linked susceptibility to autoimmunity: charged residues of a single MHC binding pocket confer selective presentation of self-peptides in pemphigus vulgaris. Proc Natl Acad Sci 92:11935–11939PubMedCentralPubMedCrossRefGoogle Scholar