Tachykinin signaling inhibits task-specific behavioral responsiveness in honeybee workers

Behavioral specialization is key to the success of social insects and leads to division of labor among colony members. Response thresholds to task-specific stimuli are thought to proximally regulate behavioral specialization but their neurobiological regulation is complex and not well-understood. Here, we show that response thresholds to task-relevant stimuli correspond to the specialization of three behavioral phenotypes of honeybee workers in the well-studied and important Apis mellifera and Apis cerana. Quantitative neuropeptidome comparisons suggest two tachykinin-related peptides (TRP2 and TRP3) as candidates for the modification of these response thresholds. Based on our characterization of their receptor binding and downstream signaling, we confirm a functional role of tachykinin signaling in regulating specific responsiveness of honeybee workers: TRP2 injection and RNAi-mediated downregulation cause consistent, opposite effects on responsiveness to task-specific stimuli of each behaviorally specialized phenotype but not to stimuli that are unrelated to their tasks. Thus, our study demonstrates that TRP-signaling regulates the degree of task-specific responsiveness of specialized honeybee workers and may control the context-specificity of behavior in animals more generally.

Neuromodulation of Behavioral Specialization: Tachykinin Signaling Inhibits Task-specific Behavioral Responsiveness in Honeybee Workers

Behavioral specialization is key to the success of social insects and often compartmentalized among colony members leading to division of labor. Response thresholds to task-specific stimuli proximally regulate behavioral specialization but their neurobiological regulation is not understood. Here, we show that response thresholds to task-relevant stimuli correspond to the specialization of three behavioral phenotypes of honeybee workers. Quantitative neuropeptidome comparisons suggest two tachykinin-related peptides (TRP2 and TRP3) as candidates for the modification of these response thresholds. Based on our characterization of their receptor binding and downstream signaling, we then confirm the functional role of tachykinins: TRP2 injection and RNAi cause consistent, opposite effects on responsiveness to task-specific stimuli of each behaviorally specialized phenotype but not to stimuli that are unrelated to their tasks. Thus, our study demonstrates that TRP-signaling regulates the degree of task-specific responsiveness of specialized honeybee workers and may control the context-specificity of behavior in animals more generally.

Search behavior of individual foragers involves neurotransmitter systems characteristic for social scouting

SUMMARYBehavioral specialization in honey bees is regulated by hormones and neuromodulators that tune neuronal activity and gene expression, and can be viewed as a temporarily fixed behavioral state associated with a specific brain state. Honey bee scouts, which search for new food sources, show a higher expression of genes involved in glutamate, GABA and catecholamine signaling than recruits that remain loyal to a food source. We asked whether recruits visiting a feeder initiated a search behavior when the feeder was experimentally removed, and if similar neuromodulators might be involved in the initiation and performance of that behavior. We found that recruits perform a relatively stereotyped search behavior that shows inter-individual variation in its intensity. Quantitative single brain mass spectrometric analyses showed that glutamate and GABA titers changed during search behavior supporting the hypothesis that behavioral specialization in social insects is based on reinforcing brain molecular processes involved in solitary behavior.