Significance Aging animals, particularly females, suffer from diminished reproductive ability, likely due to high costs of germline maintenance. Potential remedies may be found in signals exchanged by members of opposite sexes to promote reproductive success. We show that in the nematode Caenorhabditis elegans , male pheromone facilitates healthy oocyte aging. This pheromone increases germline proliferation and physiological cell death, which is required to maintain oocyte quality. We show that young adults that have not yet commenced reproduction are particularly sensitive to signals from mates and nutrients, likely because during this narrow time window, they set an environment-appropriate balance between germline and soma investment. We advocate the study of social signals as a productive avenue for identifying regulators of physiology and aging.

Behaviour and physiology are altered in reproducing animals, but neuronal circuits that regulate these changes remain largely unknown. Insights into mechanisms that regulate and possibly coordinate reproduction-related traits could be gleaned from the study of sex pheromones that can improve the reproductive success of potential mating partners. In Caenorhabditis elegans , the prominent male pheromone, ascr#10, modifies reproductive behaviour and several aspects of reproductive physiology in hermaphrodite recipients, including improving oocyte quality. Here we show that a circuit that contains serotonin-producing and serotonin-uptaking neurons plays a key role in mediating effects of ascr#10 on germline development and egg laying behaviour. We also demonstrate that increased serotonin signalling promotes proliferation of germline progenitors in adult hermaphrodites. Our results establish a role for serotonin in maintaining germline quality and highlight a simple neuronal circuit that acts as a linchpin that couples food intake, mating behaviour, reproductive output, and germline renewal and provisioning.

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Sex pheromones improve reproductive success, but also impose costs. Here we show that even brief exposure to physiological amounts of the dominantC. elegansmale pheromone, ascr#10, alters the expression of thousands of genes in hermaphrodites. The most dramatic effect on the transcriptome was the upregulation of genes expressed during oogenesis and downregulation of genes associated with male gametogenesis. Among the detrimental effects of ascr#10 on hermaphrodites is the increased risk of persistent infections caused by pathological pharyngeal hypertrophy. Our results reveal a way in which social signals help to resolve the inherent conflict between spermatogenesis and oogenesis in a simultaneous hermaphrodite, presumably to optimally align reproductive function to the presence of potential mating partners. They also show that the beneficial effects of the pheromone are accompanied by harmful consequences that reduce lifespan.

Reproduction alters animal behavior and physiology, but neuronal circuits that coordinate these changes remain largely unknown. Insights into mechanisms that regulate and possibly coordinate reproduction-related traits could be gleaned from the study of sex pheromones that manipulate potential mating partners to improve reproductive success. In C. elegans, the prominent male pheromone, ascr#10, modifies reproductive behavior and several aspects of reproductive physiology in hermaphrodite recipients, including improving oocyte quality. Here we show that a circuit that contains serotonin-producing and serotonin-uptaking neurons plays a key role in mediating these beneficial effects of ascr#10. We also demonstrate that increased serotonergic signaling promotes proliferation of germline progenitors in adult hermaphrodites. Our results establish a role for serotonin in maintaining germline quality and highlight a simple neuronal circuit that acts as a linchpin that couples food intake, mating behavior, reproductive output, and germline renewal and provisioning.