MHC class II B diversity in blue tits: a preliminary study

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Abstract

In this study, we partly characterize major histocompatibility complex (MHC) class II B in the blue tit ( Cyanistes caeruleus). A total of 22 individuals from three different European locations: Spain, The Netherlands, and Sweden were screened for MHC allelic diversity. The MHC genes were investigated using both PCR-based methods and unamplified genomic DNA with restriction fragment length polymorphism (RFLP) and southern blots. A total of 13 different exon 2 sequences were obtained independently from DNA and/or RNA, thus confirming gene transcription and likely functionality of the genes. Nine out of 13 alleles were found in more than one country, and two alleles appeared in all countries. Positive selection was detected in the region coding for the peptide binding region (PBR). A maximum of three alleles per individual was detected by sequencing and the RFLP pattern consisted of 4–7 fragments, indicating a minimum number of 2–4 loci per individual. A phylogenetic analysis, demonstrated that the blue tit sequences are divergent compared to sequences from other passerines resembling a different MHC lineage than those possessed by most passerines studied to date.

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Concerted and birth-and-death evolution of multigene families.

Masatoshi Nei, Alejandro P Rooney (2005)

Until around 1990, most multigene families were thought to be subject to concerted evolution, in which all member genes of a family evolve as a unit in concert. However, phylogenetic analysis of MHC and other immune system genes showed a quite different evolutionary pattern, and a new model called birth-and-death evolution was proposed. In this model, new genes are created by gene duplication and some duplicate genes stay in the genome for a long time, whereas others are inactivated or deleted from the genome. Later investigations have shown that most non-rRNA genes including highly conserved histone or ubiquitin genes are subject to this type of evolution. However, the controversy over the two models is still continuing because the distinction between the two models becomes difficult when sequence differences are small. Unlike concerted evolution, the model of birth-and-death evolution can give some insights into the origins of new genetic systems or new phenotypic characters.

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Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1.

J. H. Brown, T S Jardetzky, J C Gorga … (1993)

The three-dimensional structure of the class II histocompatibility glycoprotein HLA-DR1 from human B-cell membranes has been determined by X-ray crystallography and is similar to that of class I HLA. Peptides are bound in an extended conformation that projects from both ends of an 'open-ended' antigen-binding groove. A prominent non-polar pocket into which an 'anchoring' peptide side chain fits is near one end of the binding groove. A dimer of the class II alpha beta heterodimers is seen in the crystal forms of HLA-DR1, suggesting class II HLA dimerization as a mechanism for initiating the cytoplasmic signalling events in T-cell activation.

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MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years?

L. Bernatchez, C. Landry (2003)

Elucidating how natural selection promotes local adaptation in interaction with migration, genetic drift and mutation is a central aim of evolutionary biology. While several conceptual and practical limitations are still restraining our ability to study these processes at the DNA level, genes of the major histocompatibility complex (MHC) offer several assets that make them unique candidates for this purpose. Yet, it is unclear what general conclusions can be drawn after 15 years of empirical research that documented MHC diversity in the wild. The general objective of this review is to complement earlier literature syntheses on this topic by focusing on MHC studies other than humans and mice. This review first revealed a strong taxonomic bias, whereby many more studies of MHC diversity in natural populations have dealt with mammals than all other vertebrate classes combined. Secondly, it confirmed that positive selection has a determinant role in shaping patterns of nucleotide diversity in MHC genes in all vertebrates studied. Yet, future tests of positive selection would greatly benefit from making better use of the increasing number of models potentially offering more statistical rigour and higher resolution in detecting the effect and form of selection. Thirdly, studies that compared patterns of MHC diversity within and among natural populations with neutral expectations have reported higher population differentiation at MHC than expected either under neutrality or simple models of balancing selection. Fourthly, several studies showed that MHC-dependent mate preference and kin recognition may provide selective factors maintaining polymorphism in wild outbred populations. However, they also showed that such reproductive mechanisms are complex and context-based. Fifthly, several studies provided evidence that MHC may significantly influence fitness, either by affecting reproductive success or progeny survival to pathogens infections. Overall, the evidence is compelling that the MHC currently represents the best system available in vertebrates to investigate how natural selection can promote local adaptation at the gene level despite the counteracting actions of migration and genetic drift. We conclude this review by proposing several directions where future research is needed.

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Author and article information

Journal

Journal ID (nlm-ta): Ecol Evol

Journal ID (iso-abbrev): Ecol Evol

Journal ID (publisher-id): ece3

Title: Ecology and Evolution

Publisher: Blackwell Publishing Ltd

ISSN (Print): 2045-7758

ISSN (Electronic): 2045-7758

Publication date (Print): July 2013

Publication date (Electronic): 21 May 2013

Volume: 3

Issue: 7

Pages: 1878-1889

Affiliations

[1 ]Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC) J. Gutiérrez Abascal 2, E-28006, Madrid, Spain

[2 ]Behavioural Ecology and Self-Organization, The University of Groningen PO Box 11103, 9700 CC, Groningen, The Netherlands

[3 ]Departamento de Microbiología y Parasitología, Facultad de Farmacia, Universidad de Alcalá Alcalá de Henares, E-28871, Madrid, Spain

[4 ]Molecular Ecology and Evolution Lab, Ecology Building, Lund University Sölvegatan 37, SE-22362, Lund, Sweden

Author notes

Juan Rivero-de Aguilar, Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), C/ José Gutiérrez Abascal 2, Madrid (Spain). Tel: +34 914111328; Fax: +34 915645078; E-mail: juan.rivero@ 123456mncn.csic.es

Funding Information This study was funded by different projects: CGL2009-09439 from Ministerio de Ciencia e Innovación, GEBACO (FP6/2002–2006, no. 28696), and INCORE (FP6–2005-NEST-Path, no. 043318).

Article

DOI: 10.1002/ece3.598

PMC ID: 3728931

PubMed ID: 23919136

SO-VID: 464f1e0e-15a0-49c1-b384-5e10db22ca8c

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Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

MHC class II B diversity in blue tits: a preliminary study

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Evolutionary Cell Biology

Most cited references 83

Concerted and birth-and-death evolution of multigene families.

Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1.

MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years?

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