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Open Access Research article

Ancestral polymorphism at the major histocompatibility complex (MHCIIβ) in the Nesospiza bunting species complex and its sister species (Rowettia goughensis)

Alexandra Jansen van Rensburg1*, Paulette Bloomer1, Peter G Ryan2 and Bengt Hansson3*

Author affiliations

1 Molecular Ecology and Evolution Program, Department of Genetics, University of Pretoria, Private bag X20, Hatfield 0028, South Africa

2 Percy FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch 7701, South Africa

3 Molecular Ecology and Evolution Lab, Department of Biology, Lund University, SE-22362 Lund, Sweden

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Citation and License

BMC Evolutionary Biology 2012, 12:143  doi:10.1186/1471-2148-12-143

Published: 15 August 2012

Abstract

Background

The major histocompatibility complex (MHC) is an important component of the vertebrate immune system and is frequently used to characterise adaptive variation in wild populations due to its co-evolution with pathogens. Passerine birds have an exceptionally diverse MHC with multiple gene copies and large numbers of alleles compared to other avian taxa. The Nesospiza bunting species complex (two species on Nightingale Island; one species with three sub-species on Inaccessible Island) represents a rapid adaptive radiation at a small, isolated archipelago, and is thus an excellent model for the study of adaptation and speciation. In this first study of MHC in Nesospiza buntings, we aim to characterize MHCIIß variation, determine the strength of selection acting at this gene region and assess the level of shared polymorphism between the Nesospiza species complex and its putative sister taxon, Rowettia goughensis, from Gough Island.

Results

In total, 23 unique alleles were found in 14 Nesospiza and 2 R. goughensis individuals encoding at least four presumably functional loci and two pseudogenes. There was no evidence of ongoing selection on the peptide binding region (PBR). Of the 23 alleles, 15 were found on both the islands inhabited by Nesospiza species, and seven in both Nesospiza and Rowettia; indications of shared, ancestral polymorphism. A gene tree of Nesospiza MHCIIß alleles with several other passerine birds shows three highly supported Nesospiza-specific groups. All R. goughensis alleles were shared with Nesospiza, and these alleles were found in all three Nesospiza sequence groups in the gene tree, suggesting that most of the observed variation predates their phylogenetic split.

Conclusions

Lack of evidence of selection on the PBR, together with shared polymorphism across the gene tree, suggests that population variation of MHCIIß among Nesospiza and Rowettia is due to ancestral polymorphism rather than local selective forces. Weak or no selection pressure could be attributed to low parasite load at these isolated Atlantic islands. The deep divergence between the highly supported Nesospiza-specific sequence Groups 2 and 3, and the clustering of Group 3 close to the distantly related passerines, provide strong support for preserved ancestral polymorphism, and present evidence of one of the rare cases of extensive ancestral polymorphism in birds.