Abstract
Social insects frequently engage in oral fluid exchange - trophallaxis - between adults, and between adults and larvae. Although trophallaxis is widely considered a food-sharing mechanism, we hypothesized that endogenous components of this fluid might underlie a novel means of chemical communication between colony members. Through protein and small-molecule mass spectrometry and RNA sequencing, we found that trophallactic fluid in the ant Camponotus floridanus contains a set of specific digestion- and non-digestion related proteins, as well as hydrocarbons, microRNAs, and a key developmental regulator, juvenile hormone. When C. floridanus workers' food was supplemented with this hormone, the larvae they reared via trophallaxis were twice as likely to complete metamorphosis and became larger workers. Comparison of trophallactic fluid proteins across social insect species revealed that many are regulators of growth, development and behavioral maturation. These results suggest that trophallaxis plays previously unsuspected roles in communication and enables communal control of colony phenotypes.
Highlights
Many fluids shared between individuals of the same species, such as milk or semen, can exert significant physiological effects on recipients (Poiani, 2006; Liu and Kubli, 2003; Liu et al, 2014; Bernt and Walker, 1999)
We have characterized the fluid that is orally exchanged during trophallaxis, a distinctive behavior of eusocial insects generally considered as a means of food sharing
Our results reveal that the transmitted liquid contains much more than food and digestive enzymes, and includes non-proteinaceous and proteinaceous molecules implicated in chemical discrimination of nestmates, growth and development, and behavioral maturation
Summary
Many fluids shared between individuals of the same species, such as milk or semen, can exert significant physiological effects on recipients (Poiani, 2006; Liu and Kubli, 2003; Liu et al, 2014; Bernt and Walker, 1999). While the functions of these fluids are well known in some cases (Liu and Kubli, 2003; Liu et al, 2014; Bernt and Walker, 1999; Perry et al, 2013), the role(s) of other socially exchanged fluids (e.g., saliva) are less clear. Genetics and Genomics Evolutionary Biology eLife digest Ants, bees and other social insects live in large colonies where all the individuals work together to gather food, rear young and defend the colony. This level of cooperation requires the insects in the colony to be able to communicate with each other
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