Open Access Research article

Evolution of major histocompatibility complex class I and class II genes in the brown bear

Katarzyna Kuduk1, Wiesław Babik2, Katarzyna Bojarska1, Ewa B Śliwińska3, Jonas Kindberg4, Pierre Taberlet5, Jon E Swenson67 and Jacek Radwan1*

Author Affiliations

1 Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, Kraków, 30-387, Poland

2 Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Sławkowska 17, Kraków, 31-016, Poland

3 Institute of Nature Conservation, Polish Academy of Sciences, Mickiewicza 33, Kraków, 31-120, Poland

4 Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, Umeå, SE, 901 83, Sweden

5 Laboratoire d’Ecologie Alpine (LECA), Génomique des Populations et Biodiversité, CNRS UMR 5553, Université Joseph Fourier, BP 53, Grenoble Cedex 9, F-38041, France

6 Department of Ecology and Natural Resources Management, Norwegian University of Life Sciences, Ãs, NO-1432, Norway

7 Norwegian Institute for Nature Research, Trondheim, NO-7485, Norway

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BMC Evolutionary Biology 2012, 12:197  doi:10.1186/1471-2148-12-197

Published: 2 October 2012

Abstract

Background

Major histocompatibility complex (MHC) proteins constitute an essential component of the vertebrate immune response, and are coded by the most polymorphic of the vertebrate genes. Here, we investigated sequence variation and evolution of MHC class I and class II DRB, DQA and DQB genes in the brown bear Ursus arctos to characterise the level of polymorphism, estimate the strength of positive selection acting on them, and assess the extent of gene orthology and trans-species polymorphism in Ursidae.

Results

We found 37 MHC class I, 16 MHC class II DRB, four DQB and two DQA alleles. We confirmed the expression of several loci: three MHC class I, two DRB, two DQB and one DQA. MHC class I also contained two clusters of non-expressed sequences. MHC class I and DRB allele frequencies differed between northern and southern populations of the Scandinavian brown bear. The rate of nonsynonymous substitutions (dN) exceeded the rate of synonymous substitutions (dS) at putative antigen binding sites of DRB and DQB loci and, marginally significantly, at MHC class I loci. Models of codon evolution supported positive selection at DRB and MHC class I loci. Both MHC class I and MHC class II sequences showed orthology to gene clusters found in the giant panda Ailuropoda melanoleuca.

Conclusions

Historical positive selection has acted on MHC class I, class II DRB and DQB, but not on the DQA locus. The signal of historical positive selection on the DRB locus was particularly strong, which may be a general feature of caniforms. The presence of MHC class I pseudogenes may indicate faster gene turnover in this class through the birth-and-death process. South–north population structure at MHC loci probably reflects origin of the populations from separate glacial refugia.

Keywords:
Positive selection; Antigen binding sites; MHC gene expression; Phylogenetic analysis; Orthology; Ursidae