Olfaction Modulates Reproductive Plasticity through Neuroendocrine Signaling in Caenorhabditis elegans

Reproductive plasticity describes the ability of organisms to adjust parameters such as volume, rate, or timing of progeny production in order to maximize successful reproduction under different environmental conditions. Reproductive plasticity in response to environmental variation has been observed in a wide range of animals; however, the mechanisms involved in translating environmental cues into reproductive outcomes remain unknown. Here, we show that olfaction modulates reproductive timing and senescence through neuroendocrine signaling in Caenorhabditis elegans. On their preferred diet, worms demonstrate an increased rate of reproduction and an early onset of reproductive aging. Perception of the preferred diet's odor by AWB olfactory neurons elicits these adjustments by increasing germline proliferation, and optogenetic stimulation of AWB neurons is sufficient to accelerate reproductive timing in the absence of dietary inputs. Furthermore, AWB neurons act through neuropeptide signaling to regulate reproductive rate and senescence. These findings reveal a neuroendocrine nexus linking olfactory sensation and reproduction in response to environmental variation and indicate the significance of olfaction in the regulation of reproductive decline during aging.