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Structure and Evolution of a New Avian MHC Class II B Gene in a Sub-Antarctic Seabird, the Thin-Billed Prion (Procellariiformes: Pachyptila belcheri)

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Abstract

The major histocompatibility complex encodes molecules that present foreign peptides to T cells of the immune system. The peptide binding region (PBR) of these molecules is among the most polymorphic regions found in vertebrate taxa. Genomic cloning approaches are improving our understanding of the evolution of this multigene family in nonmodel avian groups. By building a cosmid library, a new MHC class II B gene, Pabe-DAB1, was isolated and characterized at the genomic level in a sub-Antarctic seabird, the thin-billed prion (Pachyptila belcheri). Pabe-DAB1 exhibits the hallmark structural features of functional MHC class II loci. Direct sequencing of the PBR encoding exon in a panel of prions revealed significantly higher levels of genetic diversity compared to two noncoding neutral loci, with most alleles differing by at least one replacement substitution in the peptide binding codons. We estimated evolutionary dynamics for Pabe-DAB1 using a variety of Bayesian and other approaches. Evidence for balancing selection comes from a spatially variable ratio of nonsynonymous-to-synonymous substitutions (mean d N/d S = 2.87) in the PBR, with sites predicted to be functionally relevant exhibiting the highest ω values. We estimate the population recombination rate to be approximately 0.3 per site per generation, indicating an important role for recombination in generating polymorphism at this locus. Pabe-DAB1 is among the few avian class II loci characterized at the genomic level and with a known intron-exon structure, a feature that greatly facilitated the amplification and sequencing of a single MHC locus in this species.

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Acknowledgments

Many thanks are due to I. Strange and the New Island Conservation Trust for allowing us access to New Island and to work with its population of thin-billed prions. The authors are grateful to J. Gasper for his invaluable help during lab work and assistance at different stages of this study. Help from W. Swanson and B. Wakimoto was also instrumental in the success of this project. S. MacKay helped with sample collection and software data analysis. H. Walsh kindly provided us with her MHC primers. J. C. Silva, H. Walsh, J. Gasper, and anonymous reviewer provided useful comments on the manuscript. Funding was provided by research grants from Fundação para a Ciência e a Tecnologia to MCS (BD/9356/96 and BPD/22276/2006). Financial support was also provided by the New Island Conservation Trust, the Margaret Morse Nice Fund, and Sigma-XI to M.C.S. and by grants from the National Science Foundation to SVE.

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  1. Department of Biology, University of Washington, Box 351800, Seattle, WA, 98195, USA

    Mónica C. Silva & Scott V. Edwards

  2. Departamento de Biologia Animal, Centro de Biologia Ambiental, Faculdade de Ciências, Universidade de Lisboa, Bloco C2, 3º Piso, Campo Grande, Lisboa, 1749-016, Portugal

    Mónica C. Silva

  3. Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA

    Scott V. Edwards

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  1. Mónica C. Silva
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Correspondence to Mónica C. Silva.

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Silva, M.C., Edwards, S.V. Structure and Evolution of a New Avian MHC Class II B Gene in a Sub-Antarctic Seabird, the Thin-Billed Prion (Procellariiformes: Pachyptila belcheri). J Mol Evol 68, 279–291 (2009). https://doi.org/10.1007/s00239-009-9200-2

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