Knockdown of ecdysone receptor in male desert locusts affects relative weight of accessory glands and mating behavior

Locusts have been known as pests of agricultural crops for thousands of years. Recently (2018-2021) the world has faced the largest swarms of desert locusts, Schistocerca gregaria, in decades and food security in large parts of Africa and Asia was under extreme pressure. There is an urgent need for the development of highly specific biorational pesticides to combat these pests. However, to do so, fundamental research is needed to better understand the molecular mechanisms behind key physiological processes underpinning swarm formation, such as development and reproduction. The scope of this study is to investigate the possible role(s) of the ecdysteroid receptor in the reproductive physiology of male S. gregaria. Ecdysteroids and juvenile hormones are two important classes of insect hormones and are key regulators of post-embryonic development. Ecdysteroids are best known for their role in moulting and exert their function via a heterodimer consisting of the nuclear receptors ecdysone receptor (EcR) and retinoid-X receptor (RXR). To gain insight into the role of SgEcR and/or SgRXR in the male reproductive physiology of S. gregaria we performed RNAi-induced knockdown experiments. A knockdown of SgEcR, but not SgRXR, resulted in an increased relative weight of the male accessory glands (MAG). Furthermore, the knockdown of these genes, either in combination or separately, caused a significant delay in the onset of mating behavior. Nevertheless, the MAG appeared to mature normally and the fertility of mated males was not affected. The high transcript levels of SgEcR in the fat body, especially towards the end of sexual maturation in both males and females, represent a remarkable finding since as of yet the exact role of SgEcR in this tissue in S. gregaria is unknown. Finally, our data suggest that in some cases SgEcR and SgRXR might act independently of each other. This is supported by the fact that the spatiotemporal expression profiles of SgEcR and SgRXR do not always coincide and that knockdown of SgEcR, but not SgRXR, significantly affected the relative weight of the MAG.

Automated summary

Locusts, known as pests of agricultural crops, have caused the largest swarms in recent years, posing a threat to food security in Africa and Asia. The development of specific pesticides is urgently needed, requiring fundamental research on the molecular mechanisms of key physiological processes involved in swarm formation.