Collective Regulation of Metabolism, Development and Longevity Through a Socially Exchanged Fluid

Abstract

Socially exchanged fluids, like seminal fluid and milk, present a direct and effective means through which an individual can influence conspecifics. As organisms heavily adapted to social life, social insects have evolved a suite of behavioral, morphological and molecular mechanisms to ensure cooperation and inclusive fitness benefits for all group members, just as multicellular organisms have. As a part of their social physiology, some species have developed a social circulatory system, where exogenous food and endogenously produced material, such as hormones, proteins and small molecules, are transferred mouth-to-mouth from the foregut of one individual to another. This fluid transfer – stomodeal trophallaxis – ensures that both food and endogenously produced components are distributed throughout the social network.To understand how the endogenous materials in trophallactic fluid relate to colony life, we investigated trophallactic fluid of the carpenter ant Camponotus floridanus, monitoring this fluid within colonies under different biotic and abiotic conditions and in different individuals within colonies. Using quantitative proteomic analyses of over 100 colony and single-individual trophallactic fluid samples, we established a set of core trophallactic fluid proteins. By combining frequentist, empirical Bayesian and machine-learning classification tools, we identified sets of proteins that are significantly induced in trophallactic fluid under different conditions: proteins that differ between young and mature colonies in the field, proteins that differ between colonies in the field and in the lab, and proteins that differ between the trophallactic fluid of nurses and foragers.Results reveal that different stages of the colony life cycle utilize classic metabolic processes in different ways, with young colonies prioritizing direct carbohydrate processing, while mature colonies prioritizing transmission of stored resources over the trophallactic network. Further, proteins from pathways that govern the fecundity-longevity trade-off and that have been previously implicated in social insect caste determination are being transferred between individuals within colonies, potentially acting as superorganismal hormones. Nurses in particular show higher abundances in proteins and pathways involved in defense against aging. Thus, we show that the protein composition of ant trophallactic fluid varies with social and developmental conditions both at the colony and at the individual level, suggesting that the trophallactic fluid proteome plays a key role in the social physiology of colonies.

Ecological change and conflict reduction led to the evolution of a transformative social behavior in ants

“…Trophallaxis likely first evolved in ants as a mode of sharing exogenous food, yet in ants that perform this behavior frequently (e.g. Camponotus ), trophallactic fluid has become a rich and complex socially transferred material similar to mammalian milk 17,19 . Various proteins and small molecules used elsewhere in ant physiology have been co-opted and neo- or sub-functionalized as they became part of trophallactic fluid 18 .…”

“…Species that use trophallaxis tend not to have a sting and tend to have sterile workers or workers that cannot be mated, suggesting that these traits might prohibit the evolution of trophallaxis 14 . In some ants where trophallactic fluid has been characterized ( Camponotus ), it has been shown to contain not only food but also endogenously produced materials including proteins, small molecules, RNA and even hormones that shift with colony maturation 17–19 . This suggests that in such superorganismal species, trophallaxis behavior may enable a form of social circulatory system or shared metabolism across the colony 14,19 , and large colonies have been proposed to require more coordination 20–22 .…”

“…In some ants where trophallactic fluid has been characterized ( Camponotus ), it has been shown to contain not only food but also endogenously produced materials including proteins, small molecules, RNA and even hormones that shift with colony maturation 17–19 . This suggests that in such superorganismal species, trophallaxis behavior may enable a form of social circulatory system or shared metabolism across the colony 14,19 , and large colonies have been proposed to require more coordination 20–22 . At present, the evolutionary dynamics that led to the single or repeated origins of this behavioral trait remain largely unexplored.…”