Vitellogenin-like A–associated shifts in social cue responsiveness regulate behavioral task specialization in an ant

Abstract

Division of labor and task specialization explain the success of human and insect societies. Social insect colonies are characterized by division of labor, with workers specializing in brood care early and foraging later in life. Theory posits that this task switching requires shifts in responsiveness to task-related cues, yet experimental evidence is weak. Here, we show that a Vitellogenin ( Vg) ortholog identified in an RNAseq study on the ant T. longispinosus is involved in this process: using phylogenetic analyses of Vg and Vg-like genes, we firstly show that this candidate gene does not cluster with the intensively studied honey bee Vg but falls into a separate Vg-like A cluster. Secondly, an experimental knockdown of Vg-like A in the fat body caused a reduction in brood care and an increase in nestmate care in young ant workers. Nestmate care is normally exhibited by older workers. We demonstrate experimentally that this task switch is at least partly based on Vg-like A–associated shifts in responsiveness from brood to worker cues. We thus reveal a novel mechanism leading to early behavioral maturation via changes in social cue responsiveness mediated by Vg-like A and associated pathways, which proximately play a role in regulating division of labor.

Author summary

In social insects such as ants and bees, workers specialize in different tasks. This specialization is thought to be regulated via response thresholds to task-specific cues, which vary between workers conducting different tasks. Whether a worker takes care of the brood, cares for other workers, or leaves the nest to search for food is influenced by age, fat content, and the expression of associated genes. In the ant Temnothorax longispinosus, workers specializing in brood care are younger and exhibit a high expression of the gene Vg-like A. Here, we demonstrate that young workers reduce brood care activity upon down-regulation of Vg-like A. Simultaneously, they increase care for adult nestmates, a behavior typically exhibited by older workers. We show experimentally that Vg-like A down-regulation alters perception of social cues: a shift in the responsiveness from chemical cues from brood to adult worker underlies the behavioral switch to nestmate care. Hence, the expression of Vg-like A and its associated pathways influences task choice in ants and is involved in the regulation of division of labor. Copies of Vg-like A are present in other ants and further social and solitary insects, and future studies will reveal the role of this gene in these organisms.