The physiological control of reproduction in insects depends on a combination of environmental and internal cues. In the adult stage, insects become sexually mature and generate gametes. In females, the latter process is designated as oogenesis. Peptides are a versatile class of extracellular signalling molecules that regulate many processes, including oogenesis. At present, the best documented physiological control mechanism of insect oogenesis is the insulin-related peptide signalling pathway. It regulates different stages of the process and provides a functional link between nutritional status and reproduction. Several other peptides have been shown to exert gonadoregulatory activities, but in most cases their exact mode of action still has to be unravelled and their effects on oogenesis could be direct or indirect. Some regulatory peptides, such as the Drosophila sex peptide, are being transferred from the male to the female during the mating process.

Currently (2020), Africa and Asia are experiencing the worst desert locust (Schistocerca gregaria) plague in decades. Exceptionally high rainfall in different regions caused favorable environmental conditions for very successful reproduction and population growth. To better understand the molecular mechanisms responsible for this remarkable reproductive capacity, as well as to fill existing knowledge gaps regarding the regulation of male reproductive physiology, we investigated the role of methoprene-tolerant (Scg-Met) and Taiman (Scg-Tai), responsible for transducing the juvenile hormone (JH) signal, in adult male locusts. We demonstrated that knockdown of these components by RNA interference strongly inhibits male sexual maturation, severely disrupting reproduction. This was evidenced by the inability to show mating behavior, the absence of a yellow-colored cuticle, the reduction of relative testes weight, and the drastically reduced phenylacetonitrile (PAN) pheromone levels of the treated males. We also observed a reduced relative weight, as well as relative protein content, of the male accessory glands in Scg-Met knockdown locusts. Interestingly, in these animals the size of the corpora allata (CA), the endocrine glands where JH is synthesized, was significantly increased, as well as the transcript level of JH acid methyltransferase (JHAMT), a rate-limiting enzyme in the JH biosynthesis pathway. Moreover, other endocrine pathways appeared to be affected by the knockdown, as evidenced by changes in the expression levels of the insulin-related peptide and two neuroparsins in the fat body. Our results demonstrate that JH signaling pathway components play a crucial role in male reproductive physiology, illustrating their potential as molecular targets for pest control.

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