Transcriptomic basis and evolution of the ant social interactome

Abstract

Social interactions are a fundamental feature of life for most organisms. Organismal development is often strongly regulated by interactions among close relatives, yet little is known about how genes expressed in social partners indirectly affect developmental trajectories and trait expression. In eusocial insects, social interactions between caregiving worker nurses and larvae strictly regulate larval development and resultant adult phenotypes. Here, we study the social interactome regulating larval development by collecting and sequencing interacting nurses and larvae across a time course of larval development. First, we find that the majority of nurse and larval transcriptomes exhibit parallel expression dynamics across larval development, providing a strong transcriptomic signature of the social interactome regulating larval development. Next, we leverage this widespread nurse-larva gene co-expression to infer social gene regulatory networks acting between nurses and larvae. We find that genes with the strongest social effects tend to be peripheral elements of within-tissue regulatory networks and are often known to encode secreted proteins. For example, our data suggest that the gene giant-lens expressed by nurses may inhibit larval epidermal growth factor signaling, which is known to affect various aspects of insect development, including caste in honey bees. Finally, we find that genes recruited for social regulatory processes tend to be relatively evolutionarily young and tend to experience relaxed selective constraint. Overall, our study provides a first glimpse into the molecular details and evolutionary features of the social mechanisms that regulate all aspects of life in eusocial insects.