Gonadal Maturation Changes Chemotaxis Behavior and Neural Processing in the Olfactory Circuit of Caenorhabditis elegans

Many animal species change their behavior according to their stage of development. However, the mechanisms involved in translating their developmental stage into the modifications of the neuronal circuits that underlie these behavioral changes remain unknown. Here we show that Caenorhabditis elegans changes its olfactory preferences during development. Larvae exhibit a weak chemotactic response to the food-associated odor diacetyl, whereas adults exhibit a strong response. We show that germline loss, caused either by laser ablation of germline precursor cells or mutations, results in a diacetyl-specific chemotactic defect in adult animals. These results suggest that germline cells, which proliferate dramatically during the larval stages, enhance chemotaxis to diacetyl. Removal experiments of specific neurons suggested that AWA olfactory neurons and their downstream interneurons, AIA and AIB, are required for germline-dependent chemotactic enhancement. Calcium imaging in animals lacking germline cells indicates that the neural responses of AWA and AIB to diacetyl stimuli are decreased compared with animals with an intact germline. These changes in neural activities may at least partly explain the behavioral change of animals lacking germline cells. Furthermore, this germline-dependent chemotactic change depends on the transcription factor DAF-16/FOXO. We find that organismal behavior changes throughout development by integrating information about physiological status from internal tissues to modify a simple sensory circuit.