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Evolution of the MHC-DQB exon 2 in marine and terrestrial mammals

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Abstract

On the basis of a general low polymorphism, several studies suggest that balancing selection in the class II major histocompatibility complex (MHC) is weaker in marine mammals as compared with terrestrial mammals. We investigated such differential selection among Cetacea, Artiodactyla, and Primates at exon 2 of MHC-DQB gene by contrasting indicators of molecular evolution such as occurrence of transpecific polymorphisms, patterns of phylogenetic branch lengths by codon position, rates of nonsynonymous and synonymous substitutions as well as accumulation of variable sites on the sampling of alleles. These indicators were compared between the DQB and the mitochondrial cytochrome b gene (cytb) as a reference of neutral expectations and differences between molecular clocks resulting from life history and historical demography. All indicators showed that the influence of balancing selection on the DQB is more variable and overall weaker for cetaceans. In our sampling, ziphiids, the sperm whale, monodontids and the finless porpoise formed a group with lower DQB polymorphism, while mysticetes exhibited a higher DQB variation similar to that of terrestrial mammals as well as higher occurrence of transpecific polymorphisms. Different dolphins appeared in the two groups. Larger variation of selection on the cetacean DQB could be related to greater stochasticity in their historical demography and thus, to a greater complexity of the general ecology and disease processes of these animals.

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Acknowledgments

We are grateful to all people who, at the labs and/or in the sea, have contributed to this work. In particular, we acknowledge the technical work of M. Dalebout, J. Murrell, M.R. Robles, and D. Steel as well as the review and advice from M.L. Fanjul, D. Heimeier, and M. Uribe, and the scholar orientation by G. Vilaclara. We appreciate the assistance of J. Zúñiga on statistical tests as well as the comments of two anonymous reviewers who greatly improved this article. Institutional, academic, legal, and funding supports were received from The Marsden Foundation, University of Auckland, Consejo Nacional de Ciencia y Tecnología, Facultad de Ciencias-Universidad Nacional Autónoma de México, Posgrado en Ciencias del Mar y Limnología-Universidad Nacional Autónoma de México, Secretaría del Medio Ambiente y Recursos Naturales, Instituto Nacional de Ecología, and Convention on International Trade in Endangered Species of Wild Fauna and Flora.

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Authors and Affiliations

  1. Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, México, 04510, México

    María José Villanueva-Noriega & Luis Medrano-González

  2. School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

    Charles Scott Baker & Luis Medrano-González

  3. Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, México, 04510, México

    María José Villanueva-Noriega

  4. Marine Mammal Institute, Oregon State University, 2030 SE Marine Science Drive, Newport, OR, 97365, USA

    Charles Scott Baker

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  1. María José Villanueva-Noriega
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  2. Charles Scott Baker
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  3. Luis Medrano-González
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Correspondence to Luis Medrano-González.

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Villanueva-Noriega, M.J., Baker, C.S. & Medrano-González, L. Evolution of the MHC-DQB exon 2 in marine and terrestrial mammals. Immunogenetics 65, 47–61 (2013). https://doi.org/10.1007/s00251-012-0647-8

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