A light-entrained clock mechanism in a hydrozoan jellyfish synchronizes evening gamete release

For marine species that reproduce by external fertilization, spawning is precisely coordinated within a local population to maximize the chances of producing offspring. Gamete release is often synchronized with respect to the diel light changes at dawn and dusk. In the hydrozoan jellyfish Clytia hemisphaerica, spawning occurs when oocyte maturation and gamete release are induced by maturation-inducing hormone (MIH) neuropeptides released from opsin-expressing cells in the gonad, directly upon light stimulus. Here, we characterize the distinct spawning cycle of a previously undescribed species Clytia sp. IZ-D, identified on the Pacific coast of Japan, which releases gametes in the evening. Clytia sp. IZ-D jellyfish spawn 14 hours after a light stimulus under a 24-hour light cycle and exhibit autonomous and synchronized spawning cycles with a 20-hour interval under constant light. We find that the female spawning cycle reflects the oocyte growth and their acquisition of competence for maturation, such that each day a new batch of growing oocytes becomes responsive to MIH at a time that correlates with the timing of actual spawning. We propose that the synchronized evening spawning in this species is controlled by an atypical circadian timing mechanism based on the progressive development of gamete competence to MIH and modulation of the opsin-controlled MIH signaling pathway. This mechanism may provide resilience to light cycle instability due to local climate variation and ensure reproductive isolation from other Clytia species by shifting the gamete release timing.