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Variation in positively selected major histocompatibility complex class I loci in rufous-collared sparrows (Zonotrichia capensis)

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Abstract

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.

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Acknowledgments

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.

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  1. Matthew R. Jones

    Present address: Division of Biological Sciences, University of Montana, 32 Campus Dr. HS104, Missoula, MT, 59812, USA

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  1. Department of Zoology and Physiology, Berry Biodiversity Conservation Center, University of Wyoming, 1000 E. University Ave., Dept. 4304, Laramie, WY, 82071, USA

    Matthew R. Jones & Matthew D. Carling

  2. Department of Animal Biology, School of Integrative Biology, University of Illinois Urbana-Champaign, 505 South Goodwin Ave., Urbana, IL, 61801, USA

    Zachary A. Cheviron

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Jones, M.R., Cheviron, Z.A. & Carling, M.D. Variation in positively selected major histocompatibility complex class I loci in rufous-collared sparrows (Zonotrichia capensis). Immunogenetics 66, 693–704 (2014). https://doi.org/10.1007/s00251-014-0800-7

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