Biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism

In cooperative systems exhibiting division of labor, such as microbial communities, multicellular organisms, and social insect colonies, individual units share costs and benefits through both task specialization and exchanged materials. Socially exchanged fluids, like seminal fluid and milk, allow i...

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Autores principales:	Sanja M Hakala, Marie-Pierre Meurville, Michael Stumpe, Adria C LeBoeuf
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	life history evolution social behavior aging social physiology proteomics tradeoff Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/cabebd1032da46d88f063fcfbd9cc814
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spelling	oai:doaj.org-article:cabebd1032da46d88f063fcfbd9cc8142021-11-24T16:02:08ZBiomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism10.7554/eLife.740052050-084Xe74005https://doaj.org/article/cabebd1032da46d88f063fcfbd9cc8142021-11-01T00:00:00Zhttps://elifesciences.org/articles/74005https://doaj.org/toc/2050-084XIn cooperative systems exhibiting division of labor, such as microbial communities, multicellular organisms, and social insect colonies, individual units share costs and benefits through both task specialization and exchanged materials. Socially exchanged fluids, like seminal fluid and milk, allow individuals to molecularly influence conspecifics. Many social insects have a social circulatory system, where food and endogenously produced molecules are transferred mouth-to-mouth (stomodeal trophallaxis), connecting all the individuals in the society. To understand how these endogenous molecules relate to colony life, we used quantitative proteomics to investigate the trophallactic fluid within colonies of the carpenter ant Camponotus floridanus. We show that different stages of the colony life cycle circulate different types of proteins: young colonies prioritize direct carbohydrate processing; mature colonies prioritize accumulation and transmission of stored resources. Further, colonies circulate proteins implicated in oxidative stress, ageing, and social insect caste determination, potentially acting as superorganismal hormones. Brood-caring individuals that are also closer to the queen in the social network (nurses) showed higher abundance of oxidative stress-related proteins. Thus, trophallaxis behavior could provide a mechanism for distributed metabolism in social insect societies. The ability to thoroughly analyze the materials exchanged between cooperative units makes social insect colonies useful models to understand the evolution and consequences of metabolic division of labor at other scales.Sanja M HakalaMarie-Pierre MeurvilleMichael StumpeAdria C LeBoeufeLife Sciences Publications Ltdarticlelife history evolutionsocial behavioragingsocial physiologyproteomicstradeoffMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	life history evolution social behavior aging social physiology proteomics tradeoff Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	life history evolution social behavior aging social physiology proteomics tradeoff Medicine R Science Q Biology (General) QH301-705.5 Sanja M Hakala Marie-Pierre Meurville Michael Stumpe Adria C LeBoeuf Biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism
description	In cooperative systems exhibiting division of labor, such as microbial communities, multicellular organisms, and social insect colonies, individual units share costs and benefits through both task specialization and exchanged materials. Socially exchanged fluids, like seminal fluid and milk, allow individuals to molecularly influence conspecifics. Many social insects have a social circulatory system, where food and endogenously produced molecules are transferred mouth-to-mouth (stomodeal trophallaxis), connecting all the individuals in the society. To understand how these endogenous molecules relate to colony life, we used quantitative proteomics to investigate the trophallactic fluid within colonies of the carpenter ant Camponotus floridanus. We show that different stages of the colony life cycle circulate different types of proteins: young colonies prioritize direct carbohydrate processing; mature colonies prioritize accumulation and transmission of stored resources. Further, colonies circulate proteins implicated in oxidative stress, ageing, and social insect caste determination, potentially acting as superorganismal hormones. Brood-caring individuals that are also closer to the queen in the social network (nurses) showed higher abundance of oxidative stress-related proteins. Thus, trophallaxis behavior could provide a mechanism for distributed metabolism in social insect societies. The ability to thoroughly analyze the materials exchanged between cooperative units makes social insect colonies useful models to understand the evolution and consequences of metabolic division of labor at other scales.
format	article
author	Sanja M Hakala Marie-Pierre Meurville Michael Stumpe Adria C LeBoeuf
author_facet	Sanja M Hakala Marie-Pierre Meurville Michael Stumpe Adria C LeBoeuf
author_sort	Sanja M Hakala
title	Biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism
title_short	Biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism
title_full	Biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism
title_fullStr	Biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism
title_full_unstemmed	Biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism
title_sort	biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/cabebd1032da46d88f063fcfbd9cc814
work_keys_str_mv	AT sanjamhakala biomarkersinasociallyexchangedfluidreflectcolonymaturitybehavioranddistributedmetabolism AT mariepierremeurville biomarkersinasociallyexchangedfluidreflectcolonymaturitybehavioranddistributedmetabolism AT michaelstumpe biomarkersinasociallyexchangedfluidreflectcolonymaturitybehavioranddistributedmetabolism AT adriacleboeuf biomarkersinasociallyexchangedfluidreflectcolonymaturitybehavioranddistributedmetabolism
_version_	1718414956903268352

Biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism

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