Olfactory inputs regulate <i>Drosophila melanogaster</i> oogenesis

Drosophila female germline development and maintenance require both local stem cell niche signaling and systemic regulation. Here, we show the indispensable function of the Drosophila melanogaster olfactory circuit in normal oogenesis and fecundity. Lack of olfactory inputs during development causes a reduction in germline stem cells. Although germline stem cells proliferate normally, the germline cysts undergo caspase-mediated apoptosis, leading to decreased follicle production and egg-laying in flies with defective olfaction. Strikingly, activation of olfactory circuits is sufficient to boost egg production, demonstrating that chemosensory-activated brain-derived inputs promote gamete development. Given the energy demands of oogenesis and its direct consequence on fitness, we propose that olfactory-stimulated systemic regulation evolved tightly with downstream diet-responsive pathways to control germline physiology in response to nutritional status. Additionally, these findings raise the possibility that sensory-mediated stem cell maintenance is a generalizable mechanism spanning a myriad of neuronal circuits, systems and species.