A peptidergic neural system connects the circadian clock to the photoperiodic control of reproductive diapause in the bug Riptortus pedestris

A diapause program that anticipates harsh seasonal environments contributes to flexible seasonal adaptation of organisms. Many animals use the photoperiod as a cue for seasonal sensing, and a circadian clock system is suggested to be important for photoperiodic physiological regulation. Although brain regions that are important for photoperiodic responses have been reported, the detailed system linking the circadian clock to photoperiodic diapause switching remains unclear. Here, we show the circadian clock-based neural mechanism for diapause switching by the female insect Riptortus pedestris, which enters reproductive diapause . This study focused on the insect neuroendocrine center, pars lateralis (PL), and analyzed its role in the photoperiodic control of diapause. PL neurons mainly express two types of neuropeptides: corazonin or short neuropeptide F (sNPF). RNA interference (RNAi) has demonstrated the importance of these neuropeptides in controlling diapause. Corazonin is essential for diapause induction under short photoperiod, and sNPF contributes to the appropriate determination of diapause according to the photoperiod. Additionally, electrophysiological analyses revealed that PL peptidergic neurons photoperiodically changed their neural activity, switching from active to silent mode by diapause-averting long photoperiod. We demonstrated that positive and negative regulators of the circadian clock are reciprocally involved in switching of PL activity and diapause. RNAi of a positive regulator cycle activates PL activity and induces reproductive diapause under long photoperiod, whereas that of a negative regulator period silences PL activity and averts diapause under short photoperiod. Our findings highlight that PL peptidergic neurons mediate the circadian clock system and the photoperiodic control of diapause. Significance Statement Diapause is an important physiological response that enables organisms to survive in harsh seasonal environments. Many organisms enter a seasonal diapause in response to the photoperiod. The circadian clock system is involved in interpreting photoperiod. However, the neural mechanisms linking the circadian clock to photoperiodic diapause induction remain unclear. This study focused on the pars lateralis (PL), an insect brain endocrine center, and revealed that PL neurons express diapause-controlled neuropeptides and undergo photoperiodically regulated changes in their neural activity. We demonstrate that the molecular basis of the circadian clock underlies the photoperiodic switching of PL neural activity and reproductive diapause. These findings highlight the significance of PL peptidergic neurons in linking the circadian clock and photoperiodic control of diapause.