Oviposition-promoting pars intercerebralis neurons showperiod-dependent photoperiodic changes in their firing activity in the bean bug

Abstract

Animals show photoperiodic responses in physiology and behavior to adapt to seasonal changes. Recent genetic analyses have demonstrated the significance of circadian clock genes in these responses. However, the importance of clock genes in photoperiodic responses at the cellular level and the physiological roles of the cellular responses are poorly understood. The bean bug Riptortus pedestris shows a clear photoperiodic response in its reproduction. In the bug, the pars intercerebralis (PI) is an important brain region for promoting oviposition. Here, we analyzed the role of the photoperiodic neuronal response and its relationship with clock genes, focusing on PI neurons. Large PI neurons exhibited photoperiodic firing changes, and high firing activities were primarily found under photoperiodic conditions suitable for oviposition. RNA interference-mediated knockdown of the clock gene period abolished the photoperiodic response in PI neurons, as well as the response in ovarian development. To clarify whether the photoperiodic response in the PI was dependent on ovarian development, we performed an ovariectomy experiment. Ovariectomy did not have significant effects on the firing activity of PI neurons. Finally, we identified the output molecules of the PI neurons and analyzed the relevance of the output signals in oviposition. PI neurons express multiple neuropeptides—insulin-like peptides and diuretic hormone 44—and RNA interference of these neuropeptides reduced oviposition. Our results suggest that oviposition-promoting peptidergic neurons in the PI exhibit a circadian clock-dependent photoperiodic firing response, which contributes to the photoperiodic promotion of oviposition.

Glutamate and clock help bean bugs track seasonal reproductive changes

“…An increase in extracellular glutamate is observed in brains from bean bugs reared in short photoperiod compared to those reared in long photoperiod. This change is dependent on the clock gene period ( per ), consistent with previous studies showing the importance of per in photoperiodism [ 5 , 6 ]. These results identify a new pathway by which the circadian clock could relay photoperiodic information to regulate seasonal biology.…”

“…This translates into defective adaptation as the bugs are unable to enter full diapause while exposed to short photoperiod and to fully promote reproduction under long photoperiod. In a previous study, the authors showed that the electrical activity of bean bug PI neurons is responsive to photoperiod [ 6 ]. In long photoperiod, PI neurons display bursts of activity while they go silent in short photoperiod.…”

Female reproductive dormancy in Drosophila melanogaster is regulated by DH31-producing neurons projecting into the corpus allatum

“…However, whether and how DH31 CA neurons are regulated in response to dormancy-inducing conditions has not been elucidated. Previous studies have reported that the circadian clock system is involved in the regulation of reproductive dormancy in many insect species (4, 53, 72, 73), including D. melanogaster (27, 51, 60, 74). Therefore, we propose that, to an extent, circadian clock neurons, such as 5 th s-LNv, s-LNv, LNd, and DN1p are connected with DH31 CA neurons and modulated its activity under dormancy-inducing conditions.…”

Photoperiodic control of electrophysiological properties of the caudo‐dorsal cells in the pond snail, Lymnaea stagnalis

“…Photoperiodic control of neural activities has been reported in a few insect brain neurosecretory cells (NSCs) (Hamanaka et al, 2004; Hasebe & Shiga, 2021; Tomioka et al, 1995). In the tobacco hornworm Manduca sexta , a neuropeptide prohoracicotropic hormone (PTTH) is a primary factor in pupal diapause regulation, the cessation of which is considered to be responsible for the pupal diapause (Bowen et al, 1984).…”

“…Some brain NSCs, which regulate reproductive diapause (Shiga & Numata, 2000), show significant differences in spike durations and spike heights between diapause‐averting and diapause‐inducing conditions (Hamanaka et al, 2004). In addition, in the bean bug Riptortus pedestris , brain NSCs essential for oviposition exhibit photoperiodic changes in firing, high firing activity being observed in photoperiodic conditions suitable for oviposition (Hasebe & Shiga, 2021). These findings imply that photoperiod‐dependent regulation of the electrophysiological properties of NSCs has a crucial role in diapause regulation.…”