Neuronal RNAi and oxygen-sensing circuit shape germline resilience to heat stress

Thermal pollution, whether local or driven by global warming, threatens biodiversity in part through its detrimental effects on reproduction. Non-coding small RNAs (sRNAs) are crucial for maintaining germline developmental robustness under heat stress. Remarkably, we uncovered that neuronal sRNAs regulate germ cells’ thermotolerance, affecting both spermatogenic and oogenic germlines in a cell-non-autonomous manner. Furthermore, we demonstrate that, in RNAi mutants, an oxygen-sensing neural circuit, modulated by neuropeptide signaling, antagonizes germline maintenance, likely reflecting the nematode’s innate association of reduced oxygen levels with food availability and reproductive permissive environments. Finally, we provide evidence that laboratory-domesticated alleles of oxygen-response genes encoding neuropeptide receptor NPR-1 and hexacoordinated globin GLB-5 compromise germline thermotolerance. Hence, our findings raise the possibility that sensory perception, independent of direct environmental change, modulates germline integrity, highlighting a novel mechanism by which neural circuits integrate environmental information to safeguard reproductive fitness in fluctuating environments.