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Open Access Research article

Gene duplication and fragmentation in the zebra finch major histocompatibility complex

Christopher N Balakrishnan18*, Robert Ekblom23, Martin Völker4, Helena Westerdahl5, Ricardo Godinez1, Holly Kotkiewicz6, David W Burt7, Tina Graves6, Darren K Griffin4, Wesley C Warren6 and Scott V Edwards1

Author affiliations

1 Department of Organismic & Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA

2 Department of Animal & Plant Sciences, University of Sheffield, Sheffield, UK

3 Department of Population Biology and Conservation Biology, Uppsala University, Uppsala, Sweden

4 Department of Biosciences, University of Kent, Kent, UK

5 Department of Animal Ecology, Lund University, Lund, Sweden

6 School of Medicine, Genome Sequencing Center, Washington University, St Louis, MO, USA

7 Roslin Institute, Division of Genetics & Genomics, University of Edinburgh, Edinburgh, UK

8 Current address: Institute for Genomic Biology, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, IL, USA

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Citation and License

BMC Biology 2010, 8:29  doi:10.1186/1741-7007-8-29

Published: 1 April 2010

Abstract

Background

Due to its high polymorphism and importance for disease resistance, the major histocompatibility complex (MHC) has been an important focus of many vertebrate genome projects. Avian MHC organization is of particular interest because the chicken Gallus gallus, the avian species with the best characterized MHC, possesses a highly streamlined minimal essential MHC, which is linked to resistance against specific pathogens. It remains unclear the extent to which this organization describes the situation in other birds and whether it represents a derived or ancestral condition. The sequencing of the zebra finch Taeniopygia guttata genome, in combination with targeted bacterial artificial chromosome (BAC) sequencing, has allowed us to characterize an MHC from a highly divergent and diverse avian lineage, the passerines.

Results

The zebra finch MHC exhibits a complex structure and history involving gene duplication and fragmentation. The zebra finch MHC includes multiple Class I and Class II genes, some of which appear to be pseudogenes, and spans a much more extensive genomic region than the chicken MHC, as evidenced by the presence of MHC genes on each of seven BACs spanning 739 kb. Cytogenetic (FISH) evidence and the genome assembly itself place core MHC genes on as many as four chromosomes with TAP and Class I genes mapping to different chromosomes. MHC Class II regions are further characterized by high endogenous retroviral content. Lastly, we find strong evidence of selection acting on sites within passerine MHC Class I and Class II genes.

Conclusion

The zebra finch MHC differs markedly from that of the chicken, the only other bird species with a complete genome sequence. The apparent lack of synteny between TAP and the expressed MHC Class I locus is in fact reminiscent of a pattern seen in some mammalian lineages and may represent convergent evolution. Our analyses of the zebra finch MHC suggest a complex history involving chromosomal fission, gene duplication and translocation in the history of the MHC in birds, and highlight striking differences in MHC structure and organization among avian lineages.