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RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens

BACKGROUND: Mating is a complex process, which is frequently associated with behavioural and physiological changes. However, understanding of the genetic underpinnings of these changes is limited. Honey bees are both a model system in behavioural genomics, and the dominant managed pollinator of huma...

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Autores principales: Manfredini, Fabio, Brown, Mark J F, Vergoz, Vanina, Oldroyd, Benjamin P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4521450/
https://www.ncbi.nlm.nih.gov/pubmed/26227994
http://dx.doi.org/10.1186/s12864-015-1750-7
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author Manfredini, Fabio
Brown, Mark J F
Vergoz, Vanina
Oldroyd, Benjamin P
author_facet Manfredini, Fabio
Brown, Mark J F
Vergoz, Vanina
Oldroyd, Benjamin P
author_sort Manfredini, Fabio
collection PubMed
description BACKGROUND: Mating is a complex process, which is frequently associated with behavioural and physiological changes. However, understanding of the genetic underpinnings of these changes is limited. Honey bees are both a model system in behavioural genomics, and the dominant managed pollinator of human crops; consequently understanding the mating process has both pure and applied value. We used next-generation transcriptomics to probe changes in gene expression in the brains of honey bee queens, as they transition from virgin to mated reproductive status. In addition, we used CO(2)-narcosis, which induces oviposition without mating, to isolate the process of reproductive maturation. RESULTS: The mating process produced significant changes in the expression of vision, chemo-reception, metabolic, and immune-related genes. Differential expression of these genes maps clearly onto known behavioural and physiological changes that occur during the transition from being a virgin queen to a newly-mated queen. A subset of these changes in gene expression were also detected in CO(2)-treated queens, as predicted from previous physiological studies. In addition, we compared our results to previous studies that used microarray techniques across a range of experimental time-points. Changes in expression of immune- and vision-related genes were common to all studies, supporting an involvement of these groups of genes in the mating process. CONCLUSIONS: Our study is an important step in understanding the molecular mechanisms regulating post-mating behavioural transitions in a natural system. The weak overlap in patterns of gene expression with previous studies demonstrates the high sensitivity of genome-wide approaches. Thus, while we build on previous microarray studies that explored post-mating changes in honey bees, the broader experimental design, use of RNA-sequencing, and focus on Australian honey bees, which remain free from the devastating parasite Varroa destructor, in the current study, provide unique insights into the biology of the mating process in honey bees. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1750-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-45214502015-08-01 RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens Manfredini, Fabio Brown, Mark J F Vergoz, Vanina Oldroyd, Benjamin P BMC Genomics Research Article BACKGROUND: Mating is a complex process, which is frequently associated with behavioural and physiological changes. However, understanding of the genetic underpinnings of these changes is limited. Honey bees are both a model system in behavioural genomics, and the dominant managed pollinator of human crops; consequently understanding the mating process has both pure and applied value. We used next-generation transcriptomics to probe changes in gene expression in the brains of honey bee queens, as they transition from virgin to mated reproductive status. In addition, we used CO(2)-narcosis, which induces oviposition without mating, to isolate the process of reproductive maturation. RESULTS: The mating process produced significant changes in the expression of vision, chemo-reception, metabolic, and immune-related genes. Differential expression of these genes maps clearly onto known behavioural and physiological changes that occur during the transition from being a virgin queen to a newly-mated queen. A subset of these changes in gene expression were also detected in CO(2)-treated queens, as predicted from previous physiological studies. In addition, we compared our results to previous studies that used microarray techniques across a range of experimental time-points. Changes in expression of immune- and vision-related genes were common to all studies, supporting an involvement of these groups of genes in the mating process. CONCLUSIONS: Our study is an important step in understanding the molecular mechanisms regulating post-mating behavioural transitions in a natural system. The weak overlap in patterns of gene expression with previous studies demonstrates the high sensitivity of genome-wide approaches. Thus, while we build on previous microarray studies that explored post-mating changes in honey bees, the broader experimental design, use of RNA-sequencing, and focus on Australian honey bees, which remain free from the devastating parasite Varroa destructor, in the current study, provide unique insights into the biology of the mating process in honey bees. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1750-7) contains supplementary material, which is available to authorized users. BioMed Central 2015-07-31 /pmc/articles/PMC4521450/ /pubmed/26227994 http://dx.doi.org/10.1186/s12864-015-1750-7 Text en © Manfredini et al. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Manfredini, Fabio
Brown, Mark J F
Vergoz, Vanina
Oldroyd, Benjamin P
RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens
title RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens
title_full RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens
title_fullStr RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens
title_full_unstemmed RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens
title_short RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens
title_sort rna-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4521450/
https://www.ncbi.nlm.nih.gov/pubmed/26227994
http://dx.doi.org/10.1186/s12864-015-1750-7
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