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

Abstract

Female insects can enter reproductive diapause, a state of suspended egg development, to conserve energy under adverse environments. In many insects, including the fruit fly, Drosophila melanogaster, reproductive diapause, also frequently called reproductive dormancy, is induced under low-temperature and short-day conditions by the downregulation of juvenile hormone (JH) biosynthesis in the corpus allatum (CA). In this study, we demonstrate that neuropeptide Diuretic hormone 31 (DH31) produced by brain neurons that project into the CA plays an essential role in regulating reproductive dormancy by suppressing JH biosynthesis in adult D. melanogaster. The CA expresses the gene encoding the DH31 receptor, which is required for DH31-triggered elevation of intracellular cAMP in the CA. Knocking down Dh31 in these CA-projecting neurons or DH31 receptor in the CA suppresses the decrease of JH titer, normally observed under dormancy-inducing conditions, leading to abnormal yolk accumulation in the ovaries. Our findings provide the first molecular genetic evidence demonstrating that CA-projecting peptidergic neurons play an essential role in regulating reproductive dormancy by suppressing JH biosynthesis.

Characterization of clock‐related proteins and neuropeptides in Drosophila littoralis and their putative role in diapause

“…Both clock neurons have putative dendritic arborizations in the accessory medulla and project to the PI, where their arborizations overlap with the AstCpositive projections stemming from the LPNs and possibly the DN 3 s (Figure 7g, white arrow). Furthermore, based on the ITP-positive LN d and 5th LN dense arborizations in the PL and PI (Hermann-Luibl et al, 2014), it is very likely that there are additional contacts with the neurosecretory cells of the PL and PI, as already shown by Kurogi et al (2023) for DH31-positive neurosecretory cells of the PL in D. melanogaster.…”

“…DH31 was recently described in three neurosecretory cells in the PL that project to the CA ("DH31CA neurons"; Kurogi et al, 2023) (Figure 1b) and were linked to reproductive dormancy in D. melanogaster (Kurogi et al, 2023). This prompted us to investigate DH31 immunostaining in the brain of D. littoralis.…”

“…Further, AstC from some dorsal neurons (DN 3 s) (Figure 1b) inhibits the dormancy response to low temperatures via still unknown cholinergic neurons (Meiselman et al, 2022). Lastly, multiple clock neurons provide inputs to DH31-positive neurosecretory cells, which in turn regulate reproductive dormancy by modulating juvenile hormone (JH) biosynthesis in the CA (Kurogi et al, 2023). Hence, most of our current knowledge on the link between the circadian clock and photoperiodic responses stems from work done in D. melanogaster despite them exhibiting a shallow diapause that is highly variable and often does not involve the entire population (Saunders et al, 1989).…”

“…Each fly was singly dissected in phosphate-buffered saline (PBS) to verify the status of the ovaries and fat bodies. The flies were considered as diapausing when no oocyte at stage 14 was present (Kurogi et al, 2023). This state can also be defined as stage II ovaries following the description of Lankinen et al (2022).…”

Managing fuels and fluids: Network integration of osmoregulatory and metabolic hormonal circuits in the polymodal control of homeostasis in insects

“…The DH31-producing neurons innervate the corpora allata that expresses DH31-R. Activation of the neuronal circuit leads to an increase in intracellular cAMP in the corpora allata, which results in decreased juvenile hormone biosynthesis. [101] Knocking down Dh31 in the corpora allata projecting neurons or DH31-R in the corpora allata causes a failure in reducing juvenile hormone concentrations, which results in abnormal yolk accumulation in the ovaries under reproductive dormancy-inducing conditions, [101] Thus, given that reproductive dormancy is under influence of day-light length and temperature, DH31 production is indirectly influenced by these two environmental stimuli.…”