Temperature profoundly affects aging in both poikilotherms and homeotherms. A general belief is that lower temperatures extend lifespan while higher temperatures shorten it. Though this “temperature law” has been widely accepted, it has not been extensively tested. Here, we carefully evaluated the role of temperature in lifespan regulation in C. elegans. We found that while exposure to low temperatures at the adult stage promotes longevity, low temperature treatment at the larval stage surprisingly reduces lifespan. Interestingly, this differential effect of temperature on lifespan in larvae and adults is mediated by the same thermosensitive channel TRPA-1 that signals to the transcription factor DAF-16/FOXO, a master regulator of lifespan. DAF-16/FOXO and TRPA-1 act in larvae to shorten lifespan, but extend lifespan in adulthood. Notably, DAF-16/FOXO differentially regulates gene expression in larvae and adults in a temperature-dependent manner. Our results uncover unexpected complexity underlying temperature modulation of longevity, demonstrating that temperature differentially regulates lifespan at different stages of life.
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