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Duplication, balancing selection and trans-species evolution explain the high levels of polymorphism of the DQA MHC class II gene in voles (Arvicolinae)

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Abstract

Major histocompatibility complex (MHC) genes play important role in host–parasite interactions and parasites are crucial factors influencing the population dynamics of hosts. We described the structure and diversity of exon 2 of the MHC class II DQA gene in three species of voles (Arvicolinae) exhibiting regular multi-annual fluctuations of population density and analysed the processes leading to the observed MHC polymorphism. By using cloning–sequencing methodology and capillary electrophoresis-single strand conformation polymorphism, we described seven sequences in the water, eight in the common, and seven in the bank voles coming from an area of 70 km2 around the Nozeroy canton in the Jura Mountains (Franche Comté, France). All exon 2 sequences translate to give unique amino acid sequences and positive selection was found to act very intensively on antigen binding sites. We documented the presence of recombination at vole DQA region but its importance in generating allelic polymorphism seems to be relatively limited. For the first time within rodents, we documented the duplication of the DQA gene in all three species with both copies being transcriptionally active. Phylogenetic analysis of allelic sequences revealed extensive trans-species polymorphism within the subfamily although no alleles were shared between species in our data set. We discuss possible role of parasites in forming the recent polymorphism pattern of the DQA locus in voles.

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Acknowledgements

The authors acknowledge the assistance of Julie Deter and Yannick Chaval in the provision of samples, Serge Morand for access to his database on rodent parasites and three anonymous referees for useful comments on the manuscript. This work received financial support from the Institut National de la Recherche Agronomique, the Region of Franche-Comté, the DIREN Franche-Comté, and the Ministry of the Environment of France. This publication has been also partially funded under the EU 6th Framework Program (GOCE-CT-2003-010284 Emerging Diseases in a Changing European Environment (EDEN) and is officially catalogued by the EDEN Steering Committee as EDEN0006). Its content does not represent the official position of the European Commission and is entirely under the responsibility of the authors.

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  1. Centre de Biologie et Gestion des Populations (UMR 22), INRA, Campus International de Baillarguet, CS 30016,, 34988 Montferrier sur Lez, Cedex, France

    J. Bryja, M. Galan, N. Charbonnel & J. F. Cosson

  2. Department of Population Biology, Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, 67502, Studenec 122,, Czech Republic

    J. Bryja

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Bryja, J., Galan, M., Charbonnel, N. et al. Duplication, balancing selection and trans-species evolution explain the high levels of polymorphism of the DQA MHC class II gene in voles (Arvicolinae). Immunogenetics 58, 191–202 (2006). https://doi.org/10.1007/s00251-006-0085-6

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