The insect somatostatin pathway gates vitellogenesis progression during reproductive maturation and the post-mating response

Abstract Oogenesis is closely linked with reproductive maturation and mating status in females. In the fruit fly Drosophila melanogaster, vitellogenesis (yolk accumulation) is an important control point for oogenesis. Vitellogenesis begins upon eclosion and continues through the process of sexual maturation. Upon reaching sexual maturity, vitellogenesis is placed on hold until it is induced again by a mating signal. In flies, this mating signal is sex peptide (SP), a seminal substance that triggers robust egg-laying activity. However, the neural mechanisms that gate vitellogenesis in response to developmental and reproductive signals remain unclear. Here, we have identified a pair of thoracic ganglion neurons that produce the neuropeptide allatostatin C (AstC-mTh). AstC inhibits the biogenesis of juvenile hormone (JH), a key endocrine stimulator of vitellogenesis. Our genetic evidence indicates that AstC-mTh neurons gate both the initiation of vitellogenesis that occurs post-eclosion and its re-initiation post-mating. During sexual maturation, which takes place shortly after eclosion, AstC-mTh neurons are activated by excitatory inputs from SP abdominal ganglion (SAG) neurons. In mature virgin females, high sustained activity of SAG neurons seems to shut off vitellogenesis via continuous activation of the AstC-mTh neurons. Upon mating, however, SP inhibits SAG neurons, leading to AstC-mTh neuronal activation. As a result, the inhibition of the CA maintained by the AstC neurons is lifted. This permit both JH biosynthesis and the progression of vitellogenesis in mated females. Our work has uncovered a central neural circuit that gates the progression of oogenesis during sexual maturation and the post-mating response.