Coevolution between MHC Class I and Antigen-Processing Genes in Salamanders

Molecular Biology and Evolution, vol. 38, pp. 5092–5106

Abstract

Proteins encoded by antigen-processing genes (APGs) provide major histocompatibility complex (MHC) class I (MHC-I) with antigenic peptides. In mammals, polymorphic multigenic MHC-I family is served by monomorphic APGs, whereas in certain nonmammalian species both MHC-I and APGs are polymorphic and coevolve within stable haplotypes. Coevolution was suggested as an ancestral gnathostome feature, presumably enabling only a single highly expressed classical MHC-I gene. In this view coevolution, while optimizing some aspects of adaptive immunity, would also limit its flexibility by preventing the expansion of classical MHC-I into a multigene family. However, some nonmammalian taxa, such as salamanders, have multiple highly expressed MHC-I genes, suggesting either that coevolution is relaxed or that it does not prevent the establishment of multigene MHC-I. To distinguish between these two alternatives, we use salamanders (30 species from 16 genera representing six families) to test, within a comparative framework, a major prediction of the coevolution hypothesis: the positive correlation between MHC-I and APG diversity. We found that MHC-I diversity explained both within-individual and species-wide diversity of two APGs, TAP1 and TAP2, supporting their coevolution with MHC-I, whereas no consistent effect was detected for the other three APGs (PSMB8, PSMB9, and TAPBP). Our results imply that although coevolution occurs in salamanders, it does not preclude the expansion of the MHC-I gene family. Contrary to the previous suggestions, nonmammalian vertebrates thus may be able to accommodate diverse selection pressures with flexibility granted by rapid expansion or contraction of the MHC-I family, while retaining the benefits of coevolution between MHC-I and TAPs.

Authors 14

1. Gemma Palomar

   Jagiellonian University

   Affiliation as printed

   Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland

2. Katarzyna Dudek

   Jagiellonian University

   Affiliation as printed

   Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland

3. Magdalena Migalska

   Jagiellonian University

   Affiliation as printed

   Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland

4. Jan W. Arntzen Aachen Institute of Biology, Leiden University Naturalis Biodiversity Center

   Leiden University · Naturalis Biodiversity Center

   Affiliation as printed

   Institute of Biology, Leiden University, Leiden, The Netherlands

   Naturalis Biodiversity Center, Leiden, The Netherlands

5. Gentile Francesco Ficetola

   Centre National de la Recherche Scientifique · University of Milan · Laboratoire d'Écologie Alpine · Université Savoie Mont Blanc · Université Grenoble Alpes

   Affiliation as printed

   Department of Environmental Sciences and Policy, University of Milan, Milan, Italy

   Laboratoire d’Ecologie Alpine (LECA), CNRS, Université Grenoble Alpes and Université Savoie Mont Blanc, Grenoble, France

6. Dušan Jelić
   Affiliation as printed

   Croatian Institute for Biodiversity, Zagreb, Croatia

7. Elizabeth L. Jockusch

   University of Connecticut

   Affiliation as printed

   Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, USA

8. Í‪ñigo Martínez-Solano

   Consejo Superior de Investigaciones Científicas · Museo Nacional de Ciencias Naturales

   Affiliation as printed

   Museo Nacional de Ciencias Naturales (MNCN), Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain

9. Masatoshi Matsunami

   University of the Ryukyus

   Affiliation as printed

   Department of Advanced Genomic and Laboratory Medicine, Graduate School of Medicine, University of the Ryukyus, Nishihara-cho, Japan

10. Howard Bradley Shaffer

    University of California, Los Angeles

    Affiliation as printed

    Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, CA, USA

    La Kretz Center for California Conservation Science, Institute of the Environment and Sustainability, University of California, Los Angeles, Los Angeles, CA, USA

11. Judit Vörös

    Hungarian Natural History Museum

    Affiliation as printed

    Department of Zoology, Hungarian Natural History Museum, Budapest, Hungary

12. Bruce Waldman

    Oklahoma State University · Seoul National University

    Affiliation as printed

    Department of Integrative Biology, Oklahoma State University, Stillwater, OK, USA

    School of Biological Sciences, Seoul National University, Seoul, South Korea

13. Ben Wielstra Aachen Institute of Biology, Leiden University Naturalis Biodiversity Center

    Leiden University · Naturalis Biodiversity Center

    Affiliation as printed

    Institute of Biology, Leiden University, Leiden, The Netherlands

    Naturalis Biodiversity Center, Leiden, The Netherlands

14. Wiesław Babik corresponding

    Jagiellonian University

    Affiliation as printed

    Institute of Environmental Sciences, Faculty of Biology, Jagiellonian University, Kraków, Poland