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Clonal raider ant brain transcriptomics identifies candidate molecular mechanisms for reproductive division of labor

BACKGROUND: Division of labor between reproductive queens and workers that perform brood care is a hallmark of insect societies. However, studies of the molecular basis of this fundamental dichotomy are limited by the fact that the caste of an individual cannot typically be experimentally manipulate...

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Autores principales: Libbrecht, Romain, Oxley, Peter R., Kronauer, Daniel J. C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6090591/
https://www.ncbi.nlm.nih.gov/pubmed/30103762
http://dx.doi.org/10.1186/s12915-018-0558-8
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author Libbrecht, Romain
Oxley, Peter R.
Kronauer, Daniel J. C.
author_facet Libbrecht, Romain
Oxley, Peter R.
Kronauer, Daniel J. C.
author_sort Libbrecht, Romain
collection PubMed
description BACKGROUND: Division of labor between reproductive queens and workers that perform brood care is a hallmark of insect societies. However, studies of the molecular basis of this fundamental dichotomy are limited by the fact that the caste of an individual cannot typically be experimentally manipulated at the adult stage. Here we take advantage of the unique biology of the clonal raider ant, Ooceraea biroi, to study brain gene expression dynamics during experimentally induced transitions between reproductive and brood care behavior. RESULTS: Introducing larvae that inhibit reproduction and induce brood care behavior causes much faster changes in adult gene expression than removing larvae. In addition, the general patterns of gene expression differ depending on whether ants transition from reproduction to brood care or vice versa, indicating that gene expression changes between phases are cyclic rather than pendular. Finally, we identify genes that could play upstream roles in regulating reproduction and behavior because they show large and early expression changes in one or both transitions. CONCLUSIONS: Our analyses reveal that the nature and timing of gene expression changes differ substantially depending on the direction of the transition, and identify a suite of promising candidate molecular regulators of reproductive division of labor that can now be characterized further in both social and solitary animal models. This study contributes to understanding the molecular regulation of reproduction and behavior, as well as the organization and evolution of insect societies. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0558-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-60905912018-08-17 Clonal raider ant brain transcriptomics identifies candidate molecular mechanisms for reproductive division of labor Libbrecht, Romain Oxley, Peter R. Kronauer, Daniel J. C. BMC Biol Research Article BACKGROUND: Division of labor between reproductive queens and workers that perform brood care is a hallmark of insect societies. However, studies of the molecular basis of this fundamental dichotomy are limited by the fact that the caste of an individual cannot typically be experimentally manipulated at the adult stage. Here we take advantage of the unique biology of the clonal raider ant, Ooceraea biroi, to study brain gene expression dynamics during experimentally induced transitions between reproductive and brood care behavior. RESULTS: Introducing larvae that inhibit reproduction and induce brood care behavior causes much faster changes in adult gene expression than removing larvae. In addition, the general patterns of gene expression differ depending on whether ants transition from reproduction to brood care or vice versa, indicating that gene expression changes between phases are cyclic rather than pendular. Finally, we identify genes that could play upstream roles in regulating reproduction and behavior because they show large and early expression changes in one or both transitions. CONCLUSIONS: Our analyses reveal that the nature and timing of gene expression changes differ substantially depending on the direction of the transition, and identify a suite of promising candidate molecular regulators of reproductive division of labor that can now be characterized further in both social and solitary animal models. This study contributes to understanding the molecular regulation of reproduction and behavior, as well as the organization and evolution of insect societies. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0558-8) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-13 /pmc/articles/PMC6090591/ /pubmed/30103762 http://dx.doi.org/10.1186/s12915-018-0558-8 Text en © Libbrecht et al. 2018 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
Libbrecht, Romain
Oxley, Peter R.
Kronauer, Daniel J. C.
Clonal raider ant brain transcriptomics identifies candidate molecular mechanisms for reproductive division of labor
title Clonal raider ant brain transcriptomics identifies candidate molecular mechanisms for reproductive division of labor
title_full Clonal raider ant brain transcriptomics identifies candidate molecular mechanisms for reproductive division of labor
title_fullStr Clonal raider ant brain transcriptomics identifies candidate molecular mechanisms for reproductive division of labor
title_full_unstemmed Clonal raider ant brain transcriptomics identifies candidate molecular mechanisms for reproductive division of labor
title_short Clonal raider ant brain transcriptomics identifies candidate molecular mechanisms for reproductive division of labor
title_sort clonal raider ant brain transcriptomics identifies candidate molecular mechanisms for reproductive division of labor
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6090591/
https://www.ncbi.nlm.nih.gov/pubmed/30103762
http://dx.doi.org/10.1186/s12915-018-0558-8
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