Juvenile hormone and energy metabolism shape the optimal timing of flight to reproduction transition in migratory locusts

Migratory insects are capable of long-distance flight and strong fecundity, but often have finite amounts of resources available for these energy-demanding traits. Although the trade-off between flight and reproduction has been reported in migratory insects, the optimal timing of flight to reproduction transition remains largely unknown. Here, using the gregarious phase of migratory locust Locusta migratoria, we report that 4-d-old adult females possessed the strongest flight capacity in the first gonadotrophic cycle. Tethered flight assays demonstrated that the timing point between ending of previtellogenesis and beginning of vitellogenesis, when vitellogenin (Vg) was not yet massively synthesized, was optimal for locust flight. Transcriptome and metabolome analyses showed that glycogen and triglyceride were primarily synthesized in the fat body of adult females during previtellogenic stage. Sustained flight of adult females significantly reduced Vg expression levels accompanied by blocked oocyte growth, prolonged preoviposition period and declined egg number. In addition, long-term flight led to significantly reduced expression of juvenile hormone (JH) synthesis genes JHAMT, HMGR, and allatotropin, but not JH metabolism genes JHE and JHEH. Application of JH mimic to JH-deprived 4-d-old adult females at a lower dose was conducive to flight. In contrast, JH administration at higher doses stimulated vitellogenesis and egg production but suppressed flight capacity. Our results suggest that JH along with energy metabolism regulate the optimal timing of flight to reproduction switch in adult females of migratory locust. The findings shed new light on the regulation of trade-off between flight and reproduction, as well as the sustainable control of migratory locusts.