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

Abstract

Female reproductive dormancy in insects is a process that drastically suppresses oogenesis to conserve energy under adverse environments. In many insects, including the fruit fly, Drosophila melanogaster, reproductive dormancy is induced under low-temperature and short-day conditions by the downregulation of juvenile hormone (JH) biosynthesis by the corpus allatum (CA). Previous studies have suggested that brain neurons that project directly to the CA are important for the regulation of reproductive dormancy. However, the role of CA-projecting neurons in JH-mediated reproductive dormancy has not yet been confirmed by molecular genetic studies. In this study, we report that, in adult D. melanogaster, the neuropeptide diuretic hormone 31 (DH31) is produced by brain neurons that project into the CA. DH31-producing-CA-projecting neurons are connected downstream with a subset of circadian clock neurons, such as s-LNvs, which are known to be involved in reproductive dormancy regulation. 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 leads to a failure in the decrease of the 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. Significance StatementDormancy is an adaptive physiological response to environmental changes that are unsuitable for survival. Adult females of many insect species undergo reproductive dormancy in which oogenesis is drastically arrested; it is induced by a decrease in juvenile hormone (JH) titers. However, we are yet to fully understand the molecular mechanisms underlying the control of JH biosynthesis under dormancy-inducing conditions. In this study using the fruit fly, we demonstrated that brain neurons projecting directly to the JH-producing organ, corpus allatum, play an essential role in regulating reproductive dormancy via the neuropeptide DH31. As the morphologically-similar neurons have previously been suggested to be involved in reproductive dormancy regulation, this study provides a fundamental molecular and neuronal basis for reproductive dormancy in insects.