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Tachykinin signaling inhibits task-specific behavioral responsiveness in honeybee workers.

ABSTRACT: 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.

SUBMITTER: Han B

PROVIDER: S-EPMC8016481 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Olfaction and chemical communication are fundamental for coordination in insect societies, especially in species forming large colonies. Reproductive and task partitioning suggest that colony members belonging to different castes or subcastes or performing different tasks during their life (polyethism) may produce different semiochemicals and be differently sensitive to the variety of pheromones and/or environmental odours. The main peripheral olfactory organs are the antennal chemosensilla, where the early olfactory processes take place. At this stage, members of two different families of soluble chemosensory proteins (Odorant Binding Proteins -OBPs-, Chemosensory Proteins -CSPs-) show a remarkable affinity for different odorants and act as carriers while a further family, the Niemann Pick type C2 proteins (NPC2) may have a similar function, although this has not been fully demonstrated. Sensillar lymph also contains Odorant degrading enzymes (ODEs) which are involved in inactivation through degradation of the chemical signals, once the message is conveyed. Despite their importance in chemical communication, poor is known about how proteins involved in peripheral olfaction and, more generally antennal proteins, differ in honeybees of different caste, task and age. Here we investigate for the first time, using a shotgun proteomic approach, the antennal profile of honeybee of different castes (queens and workers) and of workers performing different tasks (nursers, guards and foragers) by controlling for the potential confounding effect of age. Regarding olfactory proteins, major differences were observed between queens and workers, some of which were found to be more abundant in queens (OBP3, OBP18, NPC2-1) and others to be more abundant in workers (OBP15, OBP21, CSP1, CSP3); while between workers performing different tasks, OBP14 was more abundant in nurses with respect to guards and foragers, and two ODEs were more abundant in guards with respect to workers of 2nd week. Apart from proteins involved in olfaction, we have found that the antennal proteomes are mainly characterized by castes and tasks, while age has a limited effect on antennal protein profile.

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Tachykinin signaling inhibits task-specific behavioral responsiveness in honeybee workers.

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