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Evolutionary history of black grouse major histocompatibility complex class IIB genes revealed through single locus sequence-based genotyping

BACKGROUND: Gene duplications are frequently observed in the Major Histocompatibility Complex (MHC) of many species, and as a consequence loci belonging to the same MHC class are often too similar to tell apart. In birds, single locus genotyping of MHC genes has proven difficult due to concerted evo...

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Autores principales: Strand, Tanja, Wang, Biao, Meyer-Lucht, Yvonne, Höglund, Jacob
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3652749/
https://www.ncbi.nlm.nih.gov/pubmed/23617616
http://dx.doi.org/10.1186/1471-2156-14-29
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author Strand, Tanja
Wang, Biao
Meyer-Lucht, Yvonne
Höglund, Jacob
author_facet Strand, Tanja
Wang, Biao
Meyer-Lucht, Yvonne
Höglund, Jacob
author_sort Strand, Tanja
collection PubMed
description BACKGROUND: Gene duplications are frequently observed in the Major Histocompatibility Complex (MHC) of many species, and as a consequence loci belonging to the same MHC class are often too similar to tell apart. In birds, single locus genotyping of MHC genes has proven difficult due to concerted evolution homogenizing sequences at different loci. But studies on evolutionary history, mode of selection and heterozygosity correlations on the MHC cannot be performed before it is possible to analyse duplicated genes separately. In this study we investigate the architecture and evolution of the MHC class IIB genes in black grouse. We developed a sequence-based genotyping method for separate amplification of the two black grouse MHC class IIB genes BLB1 and BLB2. Based on this approach we are able to study differences in structure and selection between the two genes in black grouse and relate these results to the chicken MHC structure and organization. RESULTS: Sequences were obtained from 12 individuals and separated into alleles using the software PHASE. We compared nucleotide diversity measures and employed selection tests for BLB1 and BLB2 to explore their modes of selection. Both BLB1 and BLB2 are transcribed and display classic characteristics of balancing selection as predicted for expressed MHC class IIB genes. We found evidence for both intra- and interlocus recombination or gene conversion, as well as indication for positive but differential selection at both loci. Moreover, the two loci appear to be linked. Phylogenetic analyses revealed orthology of the black grouse MHC class IIB genes to the respective BLB loci in chicken. CONCLUSIONS: The results indicate that the duplication of the BLB gene occurred before the species divergence into black grouse, chicken and pheasant. Further, we conclude that BLB1 and BLB2 in black grouse are subjected to homogenizing concerted evolution due to interlocus genetic exchange after species divergence. The loci are in linkage disequilibrium, which is in line with the theory of tightly coevolving genes within the MHC under the minimal essential MHC hypothesis. Our results support the conclusion that MHC form and function in birds derived from studies on the domesticated chicken are not artefacts of the domestication process.
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spelling pubmed-36527492013-05-14 Evolutionary history of black grouse major histocompatibility complex class IIB genes revealed through single locus sequence-based genotyping Strand, Tanja Wang, Biao Meyer-Lucht, Yvonne Höglund, Jacob BMC Genet Research Article BACKGROUND: Gene duplications are frequently observed in the Major Histocompatibility Complex (MHC) of many species, and as a consequence loci belonging to the same MHC class are often too similar to tell apart. In birds, single locus genotyping of MHC genes has proven difficult due to concerted evolution homogenizing sequences at different loci. But studies on evolutionary history, mode of selection and heterozygosity correlations on the MHC cannot be performed before it is possible to analyse duplicated genes separately. In this study we investigate the architecture and evolution of the MHC class IIB genes in black grouse. We developed a sequence-based genotyping method for separate amplification of the two black grouse MHC class IIB genes BLB1 and BLB2. Based on this approach we are able to study differences in structure and selection between the two genes in black grouse and relate these results to the chicken MHC structure and organization. RESULTS: Sequences were obtained from 12 individuals and separated into alleles using the software PHASE. We compared nucleotide diversity measures and employed selection tests for BLB1 and BLB2 to explore their modes of selection. Both BLB1 and BLB2 are transcribed and display classic characteristics of balancing selection as predicted for expressed MHC class IIB genes. We found evidence for both intra- and interlocus recombination or gene conversion, as well as indication for positive but differential selection at both loci. Moreover, the two loci appear to be linked. Phylogenetic analyses revealed orthology of the black grouse MHC class IIB genes to the respective BLB loci in chicken. CONCLUSIONS: The results indicate that the duplication of the BLB gene occurred before the species divergence into black grouse, chicken and pheasant. Further, we conclude that BLB1 and BLB2 in black grouse are subjected to homogenizing concerted evolution due to interlocus genetic exchange after species divergence. The loci are in linkage disequilibrium, which is in line with the theory of tightly coevolving genes within the MHC under the minimal essential MHC hypothesis. Our results support the conclusion that MHC form and function in birds derived from studies on the domesticated chicken are not artefacts of the domestication process. BioMed Central 2013-04-24 /pmc/articles/PMC3652749/ /pubmed/23617616 http://dx.doi.org/10.1186/1471-2156-14-29 Text en Copyright © 2013 Strand et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Strand, Tanja
Wang, Biao
Meyer-Lucht, Yvonne
Höglund, Jacob
Evolutionary history of black grouse major histocompatibility complex class IIB genes revealed through single locus sequence-based genotyping
title Evolutionary history of black grouse major histocompatibility complex class IIB genes revealed through single locus sequence-based genotyping
title_full Evolutionary history of black grouse major histocompatibility complex class IIB genes revealed through single locus sequence-based genotyping
title_fullStr Evolutionary history of black grouse major histocompatibility complex class IIB genes revealed through single locus sequence-based genotyping
title_full_unstemmed Evolutionary history of black grouse major histocompatibility complex class IIB genes revealed through single locus sequence-based genotyping
title_short Evolutionary history of black grouse major histocompatibility complex class IIB genes revealed through single locus sequence-based genotyping
title_sort evolutionary history of black grouse major histocompatibility complex class iib genes revealed through single locus sequence-based genotyping
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3652749/
https://www.ncbi.nlm.nih.gov/pubmed/23617616
http://dx.doi.org/10.1186/1471-2156-14-29
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