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The pupal moulting fluid has evolved social functions in ants

Insect societies are tightly integrated, complex biological systems in which group-level properties arise from the interactions between individuals(1–4). However, these interactions have not been studied systematically and therefore remain incompletely known. Here, using a reverse engineering approa...

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Autores principales: Snir, Orli, Alwaseem, Hanan, Heissel, Søren, Sharma, Anurag, Valdés-Rodríguez, Stephany, Carroll, Thomas S., Jiang, Caroline S., Razzauti, Jacopo, Kronauer, Daniel J. C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9750870/
https://www.ncbi.nlm.nih.gov/pubmed/36450990
http://dx.doi.org/10.1038/s41586-022-05480-9
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author Snir, Orli
Alwaseem, Hanan
Heissel, Søren
Sharma, Anurag
Valdés-Rodríguez, Stephany
Carroll, Thomas S.
Jiang, Caroline S.
Razzauti, Jacopo
Kronauer, Daniel J. C.
author_facet Snir, Orli
Alwaseem, Hanan
Heissel, Søren
Sharma, Anurag
Valdés-Rodríguez, Stephany
Carroll, Thomas S.
Jiang, Caroline S.
Razzauti, Jacopo
Kronauer, Daniel J. C.
author_sort Snir, Orli
collection PubMed
description Insect societies are tightly integrated, complex biological systems in which group-level properties arise from the interactions between individuals(1–4). However, these interactions have not been studied systematically and therefore remain incompletely known. Here, using a reverse engineering approach, we reveal that unlike solitary insects, ant pupae extrude a secretion derived from the moulting fluid that is rich in nutrients, hormones and neuroactive substances. This secretion elicits parental care behaviour and is rapidly removed and consumed by the adults. This behaviour is crucial for pupal survival; if the secretion is not removed, pupae develop fungal infections and die. Analogous to mammalian milk, the secretion is also an important source of early larval nutrition, and young larvae exhibit stunted growth and decreased survival without access to the fluid. We show that this derived social function of the moulting fluid generalizes across the ants. This secretion thus forms the basis of a central and hitherto overlooked interaction network in ant societies, and constitutes a rare example of how a conserved developmental process can be co-opted to provide the mechanistic basis of social interactions. These results implicate moulting fluids in having a major role in the evolution of ant eusociality.
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spelling pubmed-97508702022-12-16 The pupal moulting fluid has evolved social functions in ants Snir, Orli Alwaseem, Hanan Heissel, Søren Sharma, Anurag Valdés-Rodríguez, Stephany Carroll, Thomas S. Jiang, Caroline S. Razzauti, Jacopo Kronauer, Daniel J. C. Nature Article Insect societies are tightly integrated, complex biological systems in which group-level properties arise from the interactions between individuals(1–4). However, these interactions have not been studied systematically and therefore remain incompletely known. Here, using a reverse engineering approach, we reveal that unlike solitary insects, ant pupae extrude a secretion derived from the moulting fluid that is rich in nutrients, hormones and neuroactive substances. This secretion elicits parental care behaviour and is rapidly removed and consumed by the adults. This behaviour is crucial for pupal survival; if the secretion is not removed, pupae develop fungal infections and die. Analogous to mammalian milk, the secretion is also an important source of early larval nutrition, and young larvae exhibit stunted growth and decreased survival without access to the fluid. We show that this derived social function of the moulting fluid generalizes across the ants. This secretion thus forms the basis of a central and hitherto overlooked interaction network in ant societies, and constitutes a rare example of how a conserved developmental process can be co-opted to provide the mechanistic basis of social interactions. These results implicate moulting fluids in having a major role in the evolution of ant eusociality. Nature Publishing Group UK 2022-11-30 2022 /pmc/articles/PMC9750870/ /pubmed/36450990 http://dx.doi.org/10.1038/s41586-022-05480-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Snir, Orli
Alwaseem, Hanan
Heissel, Søren
Sharma, Anurag
Valdés-Rodríguez, Stephany
Carroll, Thomas S.
Jiang, Caroline S.
Razzauti, Jacopo
Kronauer, Daniel J. C.
The pupal moulting fluid has evolved social functions in ants
title The pupal moulting fluid has evolved social functions in ants
title_full The pupal moulting fluid has evolved social functions in ants
title_fullStr The pupal moulting fluid has evolved social functions in ants
title_full_unstemmed The pupal moulting fluid has evolved social functions in ants
title_short The pupal moulting fluid has evolved social functions in ants
title_sort pupal moulting fluid has evolved social functions in ants
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9750870/
https://www.ncbi.nlm.nih.gov/pubmed/36450990
http://dx.doi.org/10.1038/s41586-022-05480-9
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