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Major histocompatibility complex variation and evolution at a single, expressed DQA locus in two genera of elephants

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Abstract

Genes of the vertebrate major histocompatibility complex (MHC) are crucial to defense against infectious disease, provide an important measure of functional genetic diversity, and have been implicated in mate choice and kin recognition. As a result, MHC loci have been characterized for a number of vertebrate species, especially mammals; however, elephants are a notable exception. Our study is the first to characterize patterns of genetic diversity and natural selection in the elephant MHC. We did so using DNA sequences from a single, expressed DQA locus in elephants. We characterized six alleles in 30 African elephants (Loxodonta africana) and four alleles in three Asian elephants (Elephas maximus). In addition, for two of the African alleles and three of the Asian alleles, we characterized complete coding sequences (exons 1–5) and nearly complete non-coding sequences (introns 2–4) for the class II DQA loci. Compared to DQA in other wild mammals, we found moderate polymorphism and allelic diversity and similar patterns of selection; patterns of non-synonymous and synonymous substitutions were consistent with balancing selection acting on the peptides involved in antigen binding in the second exon. In addition, balancing selection has led to strong trans-species allelism that has maintained multiple allelic lineages across both genera of extant elephants for at least 6 million years. We discuss our results in the context of MHC diversity in other mammals and patterns of evolution in elephants.

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Acknowledgments

We thank the Office of the President of Kenya for permission to work in Amboseli National Park under permit number MOES&T 13/001/30C 72/7. We thank the Kenya Wildlife Service for local sponsorship. We thank the Amboseli Elephant Research project for invaluable scientific and logistical support, particularly the team of N. Njiraini, K. Sayialel, and S. Sayialel who contributed greatly to the collection of genetic samples. We thank the Smithsonian National Zoo, the Philadelphia Zoo in Philadelphia, PA, the Gladys Porter Zoo in Brownsville, TX, and the Six Flags Wild Safari Park in Jackson, NJ for their support and cooperation in sample collection. This research was supported by the Smithsonian Institution Abbott Endowment Fund, the National Zoo’s Institution Center for Conservation and Evolutionary Genetics, the Friends of the National Zoo, the National Science Foundation (IBN0091612 to SCA), the Amboseli Trust for Elephants, the Amboseli Elephant Research Project, and Duke University.

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Authors and Affiliations

  1. Center for Conservation and Evolutionary Genetics, National Zoological Park & National Museum of Natural History, Smithsonian Institution, Washington, DC, USA

    Elizabeth A. Archie, Tammy Henry, Jesus E. Maldonado & Robert C. Fleischer

  2. Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA

    Elizabeth A. Archie

  3. Department of Environmental Science and Policy, George Mason University, Fairfax, VA, USA

    Tammy Henry

  4. Amboseli Trust for Elephants, Nairobi, Kenya

    Cynthia J. Moss & Joyce H. Poole

  5. Philadelphia Zoo, 3400 Girard Avenue, Philadelphia, PA, USA

    Virginia R. Pearson

  6. Animal Health, National Zoological Park, Washington, DC, USA

    Suzan Murray

  7. Department of Biology, Duke University, Durham, NC, USA

    Susan C. Alberts

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  1. Elizabeth A. Archie
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  2. Tammy Henry
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Correspondence to Elizabeth A. Archie.

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Archie, E.A., Henry, T., Maldonado, J.E. et al. Major histocompatibility complex variation and evolution at a single, expressed DQA locus in two genera of elephants. Immunogenetics 62, 85–100 (2010). https://doi.org/10.1007/s00251-009-0413-8

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  • DOI: https://doi.org/10.1007/s00251-009-0413-8

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