Biomarkers in a socially exchanged fluid reflect colony maturity, behavior and distributed metabolism
- University of Fribourg, Switzerland
Abstract
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.
Data availability
The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD028568. All other data are made available in this submission in supplemental figures, source code and supplemental files.
Article and author information
Author details
Marie-Pierre Meurville
Funding
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (PR00P3_179776)
- Adria C LeBoeuf
Bundesbehörden der Schweizerischen Eidgenossenschaft (2020.0228)
- Sanja M Hakala
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Hakala et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Biomarkers in a socially exchanged fluid reflect colony maturity, behavior and distributed metabolism
eLife 10:e74005.
https://doi.org/10.7554/eLife.74005
