Transcriptomic basis and evolution of the ant nurse-larval social interactome

Abstract

Development is often strongly regulated by interactions among close relatives, but the underlying molecular mechanisms are largely unknown. In eusocial insects, interactions between caregiving worker nurses and larvae regulate larval development and resultant adult phenotypes. Here, we begin to characterize the social interactome regulating ant larval development by collecting and sequencing the transcriptomes of interacting nurses and larvae across time. We find that the majority of nurse and larval transcriptomes exhibit parallel expression dynamics across larval development. We leverage this widespread nurse-larva gene co-expression to infer putative social gene regulatory networks acting between nurses and larvae. Genes with the strongest inferred social effects tend to be peripheral elements of within-tissue regulatory networks and are often known to encode secreted proteins. This includes interesting candidates such as the nurse-expressed giant-lens , which may influence larval epidermal growth factor signaling, a pathway known to influence various aspects of insect development. Finally, we find that genes with the strongest signatures of social regulation tend to experience relaxed selective constraint and are evolutionarily young. Overall, our study provides a first glimpse into the molecular and evolutionary features of the social mechanisms that regulate all aspects of social life.

Functional genomics of parental care of insects

“…For the nurses, they found ~2,650 differentially expressed genes through the developmental time-series. This study reinforced earlier findings of nursing genes being enriched for genes that produce secreted proteins and being less evolutionarily constrained (i.e., higher rates of non-synonymous substitutions; Warner et al, 2019b). It might be that during a major evolutionary transition, such as, a transition from solitary to social, there is an increased likelihood of evolving novel genes as novel master regulators of established regulatory network.…”

Brood recognition and discrimination in ants

“…In spite of these advances, many open questions remain about brood-directed behavior, and more generally, about social interactions involving brood in ants. As the role of development in driving evolutionary processes receives more attention, studies focusing on brood-adult interactions are beginning to provide insight into the physiological and genetic mechanisms underlying these complex interaction networks (Chandra et al 2018;Walsh et al 2018b;Warner et al 2019) and their evolutionary basis (Walsh et al 2018a). Hopefully, this review will help inspire future research on the fascinating life of ant brood.…”

Distributed physiology and the molecular basis of social life in eusocial insects

“…Predictions for gene regulatory networks : Gene regulatory networks of derived organismal colonies may be more complex than those controlling solitary insect physiology and behavior 12,48,152 . Here we mean that eusocial regulatory networks are more complex in the sense that they allow for a broader range of functional connections among genes (through interactions among nestmates), increased spatial partitioning of expression (e.g.…”

“…This means that there is the potential for diversified types of signaling and response in the eusocial insect colony, as well as elaboration of the molecular mechanisms underlying the response to stimuli. Functional genomic approaches that simultaneously consider multiple socially-interacting individuals, e.g., based on sequencing a time series of interacting nurse workers and larvae 152 shows that even the most fundamentally important conserved genes have distinctly different expression patterns in eusocial insects as compared to solitary insects, as well as expression variation between related eusocial species and among nestmates 31,[158][159][160] . The convention has been to act as if use of an ortholog constitutes conservation, but already for key cases such as PKG we know the same locus can be associated with a trait (e.g.…”