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

Jansen van Rensburg, Alexandra; Bloomer, Paulette; Ryan, Peter G. and Hansson, Bengt LU (2012) In BMC Evolutionary Biology 12.
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 MHCII ss variation, determine... (More)
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 MHCII ss 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 MHCII ss 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 MHCII ss 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. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
BMC Evolutionary Biology
volume
12
publisher
BioMed Central
external identifiers
  • wos:000310331500001
  • scopus:84864910647
ISSN
1471-2148
DOI
10.1186/1471-2148-12-143
project
Speciation in island birds
Avian MHC genes
BECC
language
English
LU publication?
yes
id
6bac8247-5625-4084-8d9f-73d12bf9a601 (old id 3284015)
date added to LUP
2012-12-20 10:51:11
date last changed
2017-09-10 04:02:01
@article{6bac8247-5625-4084-8d9f-73d12bf9a601,
  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 MHCII ss 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 MHCII ss 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 MHCII ss 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.},
  author       = {Jansen van Rensburg, Alexandra and Bloomer, Paulette and Ryan, Peter G. and Hansson, Bengt},
  issn         = {1471-2148},
  language     = {eng},
  publisher    = {BioMed Central},
  series       = {BMC Evolutionary Biology},
  title        = {Ancestral polymorphism at the major histocompatibility complex (MHCII ss) in the Nesospiza bunting species complex and its sister species (Rowettia goughensis)},
  url          = {http://dx.doi.org/10.1186/1471-2148-12-143},
  volume       = {12},
  year         = {2012},
}