The Tra/Dsx-JHBP axis controls female-specific gene expression and oviposition in locusts

Sexual dimorphism is a crucial aspect of morphological and behavioral traits in animals. Unlike males, adult female locusts, i.e., Locusta migratoria, have highly extensible abdominal intersegmental membranes (ISMs) that facilitate deep oviposition into the soil, displaying an iconic sexual dimorphism, but the underlying mechanisms remain largely unknown. Here, we reveal that the extremely extensible ISMs in adult females are predominantly controlled by two female-specific proteins, LmAbd-1 and LmAbd-6, ensuring the oviposition behavior. Moreover, we discovered that LmJHBP, a juvenile hormone (JH) binding protein specifically expressed in adult female ISMs, mediates JH signaling to induce LmAbd-1 and LmAbd-6 expression. Importantly, the sex differentiation pathway (i.e., Tra-2 and Dsx) determines the female-specific expression pattern of LmJHBP, and thus those of JH signaling and LmAbd-1 and LmAbd-6 expression. The finding of Tra/Dsx-JHBP axis significantly advanced understanding of sexual dimorphism and the adaptation of oviposition behavior in insects, the evolutionarily successful "segmentation" animals.