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

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.

Time-course RNASeq of Camponotus floridanus forager and nurse ant brains indicate links between plasticity in the biological clock and behavioral division of labor

“…To measure and compare their daily rhythms in gene expression in forager and nurse brains, we sampled these behaviorally distinct castes using an approach similar to recent work that aimed to measure their trophallactic fluid protein levels [ 165 ]. We defined foragers as individuals that perform outside-nest (extranidal) tasks, including foraging for food.…”

Ruling the unruly: Innovation in ant larval feeding led to increased caste dimorphism and social complexity

“…Such food improvement can be achieved by nitrogen-fixing bacterial symbionts in the guts of workers (Russell et al 2009, Jackson et al 2022 or through metabolic labor performed by workers, transforming exogenous food into endogenous ant proteins (Hakala et al 2021). This transformation of sugary liquids requires the ingestion of the liquid by workers and consequent sharing of the products through trophic eggs or regurgitation (trophallaxis).…”

“…However, the use of liquid food for larval rearing is likely to require prior processing into a more consolidated form to meet the nutritional requirements of larval growth (Dussutour and Simpson 2009, Csata and Dussutour 2019). Such food improvement can be achieved by nitrogen-fixing bacterial symbionts in the guts of workers (Russell et al 2009, Jackson et al 2022) or through metabolic labor performed by workers, transforming exogenous food into endogenous ant proteins (Hakala et al 2021). This transformation of sugary liquids requires the ingestion of the liquid by workers and consequent sharing of the products through trophic eggs or regurgitation (trophallaxis).…”

Evolution and impact of socially transferred materials

“…-Finally, social transfers can be more or less frequent or sustained (Figure 1), ranging from a single brief event all the way to the shared physiology of placental viviparity, or an ant colony connected by the social feeding network of trophallaxis [24,35,36].…”