Abstract Many species synchronize their physiology and behavior to specific hours. It is commonly assumed that sunlight acts as the main entrainment signal for ~24h clocks. However, the moon provides similarly regular time information, and increasingly studies report correlations between diel behavior and lunidian cycles. Yet, mechanistic insight into the possible influences of the moon on ~24hr timers is scarce. We studied Platynereis dumerilii and uncover that the moon, besides its role in monthly timing, also schedules the exact hour of nocturnal swarming onset to the nights’ darkest times. Moonlight adjusts a plastic clock, exhibiting <24h (moonlit) or >24h (no moon) periodicity. Abundance, light sensitivity, and genetic requirement indicate Platynereis r-Opsin1 as receptor to determine moonrise, while the cryptochrome L-Cry is required to discriminate between moon- and sunlight valence. Comparative experiments in Drosophila suggest that Cryptochrome’s requirement for light valence interpretation is conserved. Its exact biochemical properties differ, however, between species with dissimilar timing ecology. Our work advances the molecular understanding of lunar impact on fundamental rhythmic processes, including those of marine mass spawners endangered by anthropogenic change.
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