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Diversification of the ant odorant receptor gene family and positive selection on candidate cuticular hydrocarbon receptors

BACKGROUND: Chemical communication plays important roles in the social behavior of ants making them one of the most successful groups of animals on earth. However, the molecular evolutionary process responsible for their chemosensory adaptation is still elusive. Recent advances in genomic studies ha...

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Autores principales: Engsontia, Patamarerk, Sangket, Unitsa, Robertson, Hugh M., Satasook, Chutamas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4549895/
https://www.ncbi.nlm.nih.gov/pubmed/26306879
http://dx.doi.org/10.1186/s13104-015-1371-x
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author Engsontia, Patamarerk
Sangket, Unitsa
Robertson, Hugh M.
Satasook, Chutamas
author_facet Engsontia, Patamarerk
Sangket, Unitsa
Robertson, Hugh M.
Satasook, Chutamas
author_sort Engsontia, Patamarerk
collection PubMed
description BACKGROUND: Chemical communication plays important roles in the social behavior of ants making them one of the most successful groups of animals on earth. However, the molecular evolutionary process responsible for their chemosensory adaptation is still elusive. Recent advances in genomic studies have led to the identification of large odorant receptor (Or) gene repertoires from ant genomes providing fruitful materials for molecular evolution analysis. The aim of this study was to test the hypothesis that diversification of this gene family is involved in olfactory adaptation of each species. RESULTS: We annotated the Or genes from the genome sequences of two leaf-cutter ants, Acromyrmex echinatior and Atta cephalotes (385 and 376 putative functional genes, respectively). These were used, together with Or genes from Camponotus floridanus, Harpegnathos saltator, Pogonomyrmex barbatus, Linepithema humile, Cerapachys biroi, Solenopsis invicta and Apis mellifera, in molecular evolution analysis. Like the Or family in other insects, ant Or genes evolve by the birth-and-death model of gene family evolution. Large gene family expansions involving tandem gene duplications, and gene gains outnumbering losses, are observed. Codon analysis of genes in lineage-specific expansion clades revealed signatures of positive selection on the candidate cuticular hydrocarbon receptor genes (9-exon subfamily) of Cerapachys biroi, Camponotus floridanus, Acromyrmex echinatior and Atta cephalotes. Positively selected amino acid positions are primarily in transmembrane domains 3 and 6, which are hypothesized to contribute to the odor-binding pocket, presumably mediating changing ligand specificity. CONCLUSIONS: This study provides support for the hypothesis that some ant lineage-specific Or genes have evolved under positive selection. Newly duplicated genes particularly in the candidate cuticular hydrocarbon receptor clade that have evolved under positive selection may contribute to the highly sophisticated lineage-specific chemical communication in each ant species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13104-015-1371-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-45498952015-08-27 Diversification of the ant odorant receptor gene family and positive selection on candidate cuticular hydrocarbon receptors Engsontia, Patamarerk Sangket, Unitsa Robertson, Hugh M. Satasook, Chutamas BMC Res Notes Research Article BACKGROUND: Chemical communication plays important roles in the social behavior of ants making them one of the most successful groups of animals on earth. However, the molecular evolutionary process responsible for their chemosensory adaptation is still elusive. Recent advances in genomic studies have led to the identification of large odorant receptor (Or) gene repertoires from ant genomes providing fruitful materials for molecular evolution analysis. The aim of this study was to test the hypothesis that diversification of this gene family is involved in olfactory adaptation of each species. RESULTS: We annotated the Or genes from the genome sequences of two leaf-cutter ants, Acromyrmex echinatior and Atta cephalotes (385 and 376 putative functional genes, respectively). These were used, together with Or genes from Camponotus floridanus, Harpegnathos saltator, Pogonomyrmex barbatus, Linepithema humile, Cerapachys biroi, Solenopsis invicta and Apis mellifera, in molecular evolution analysis. Like the Or family in other insects, ant Or genes evolve by the birth-and-death model of gene family evolution. Large gene family expansions involving tandem gene duplications, and gene gains outnumbering losses, are observed. Codon analysis of genes in lineage-specific expansion clades revealed signatures of positive selection on the candidate cuticular hydrocarbon receptor genes (9-exon subfamily) of Cerapachys biroi, Camponotus floridanus, Acromyrmex echinatior and Atta cephalotes. Positively selected amino acid positions are primarily in transmembrane domains 3 and 6, which are hypothesized to contribute to the odor-binding pocket, presumably mediating changing ligand specificity. CONCLUSIONS: This study provides support for the hypothesis that some ant lineage-specific Or genes have evolved under positive selection. Newly duplicated genes particularly in the candidate cuticular hydrocarbon receptor clade that have evolved under positive selection may contribute to the highly sophisticated lineage-specific chemical communication in each ant species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13104-015-1371-x) contains supplementary material, which is available to authorized users. BioMed Central 2015-08-27 /pmc/articles/PMC4549895/ /pubmed/26306879 http://dx.doi.org/10.1186/s13104-015-1371-x Text en © Engsontia et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Engsontia, Patamarerk
Sangket, Unitsa
Robertson, Hugh M.
Satasook, Chutamas
Diversification of the ant odorant receptor gene family and positive selection on candidate cuticular hydrocarbon receptors
title Diversification of the ant odorant receptor gene family and positive selection on candidate cuticular hydrocarbon receptors
title_full Diversification of the ant odorant receptor gene family and positive selection on candidate cuticular hydrocarbon receptors
title_fullStr Diversification of the ant odorant receptor gene family and positive selection on candidate cuticular hydrocarbon receptors
title_full_unstemmed Diversification of the ant odorant receptor gene family and positive selection on candidate cuticular hydrocarbon receptors
title_short Diversification of the ant odorant receptor gene family and positive selection on candidate cuticular hydrocarbon receptors
title_sort diversification of the ant odorant receptor gene family and positive selection on candidate cuticular hydrocarbon receptors
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4549895/
https://www.ncbi.nlm.nih.gov/pubmed/26306879
http://dx.doi.org/10.1186/s13104-015-1371-x
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