Crucial Role of Juvenile Hormone Receptor Components Methoprene-Tolerant and Taiman in Sexual Maturation of Adult Male Desert Locusts

The desert locust, Schistocerca gregaria, is an infamous migrating insect, generally considered to be one of the most dangerous pest species worldwide. In an area that encompasses one fifth of the Earth’s land surface, desert locust swarms can devastate the agricultural production. Consequently, they pose a serious threat to food security and can have a dramatic socio-economic impact. Currently (in 2020), large parts of East Africa, Southwest and South Asia are experiencing the worst desert locust plague in many decades. Exceptionally high rainfall in different regions has caused the 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 decided to investigate the role of the methoprene-tolerant (Scg-Met) and taiman (Scg-Tai) genes in adult male desert locusts. Methoprene-tolerant and Taiman belong to the basic helix-loop-helix/Per-Arnt-Sim (bHLH/PAS) family of transcription factors and form a complex that is responsible for transducing the Juvenile Hormone (JH) signal. So far, in vivo research has mainly focused on the role of these JH receptor components in post-embryonic development, as well as in the reproductive physiology of adult female insects. In the current study, we show that silencing these components by RNA interference strongly inhibits sexual maturation of gregarious desert locust males, thereby severely disrupting reproduction. This observation is evidenced by the absence of a yellow colored cuticle, the significant reduction in the relative weight of the testes, the inability to show mating behavior, and the drastically reduced phenylacetonitrile (PAN) pheromone levels of the treated males. In addition, we also observed significant reductions of the relative weight, as well as the 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, and a significant rise was observed in the relative transcript levels of JH acid methyltransferase (JHAMT), a rate-limiting enzyme in the JH biosynthesis pathway. Moreover, other endocrine pathways also appeared to be affected by the knockdown, as evidenced by significant changes in the levels of the transcripts coding for the insulin-related peptide and for two neuroparsins in the fat body. Our results demonstrate that JH signaling pathway components play a crucial role in male reproductive physiology. Since they are crucial for a successful reproduction, they may hold great potential as candidate targets for the design of novel strategies for locust population management. Significance statement Desert locusts can form devastating swarms that threaten the livelihood in many of the world’s poorest countries, as demonstrated by the plagues in East Africa, Southwest and South Asia that are currently covered in the news worldwide. Control of this migratory pest mainly relies on the large-scale use of neurotoxic insecticides, also affecting non-target organisms in their already fragile habitats. Therefore, the identification of novel molecular targets for the design of more sustainable and more selective pest management techniques remains of crucial importance. Potential candidate targets in this respect are pathway components that transduce signals of typical insect hormones, such as ecdysteroids and juvenile hormones. By focusing in our current study on the JH receptor components, we showed that the reproductive capacities of desert locust males can be severely inhibited in an early stage, resulting in individuals that display no mating behavior, do not produce an important pheromone and do not show the characteristic yellow color of sexually mature gregarious males. Specifically targeting molecular components of the JH signaling pathway in future, more biorational control strategies could therefore be a very successful way by which expansion of these devastating plagues might be prevented.