Reproduction and Wing Differentiation of Gynoparae Are Regulated by Juvenile Hormone Signaling in Aphis gossypii

Gynopara is a specific winged type in the life history of Aphis gossypii. As a key reproduction mode between parthenogenesis and sexual reproduction, it lays sexual females in late autumn. However, little is known about gynoparae because of its rare presence in the wild and the lack of its detailed descriptions. In this study, we investigated the morphological characteristics, ovary maturation process, and key signaling pathways during the development of gynoparae of A. gossypii. With the extension of development stage, the gynoparae exhibited gradually enlarged and thickened abdomen, deepened color. Obviously differentiated wing primordia in the second instar nymphs. Two nested U-shaped zones containing a series of waxy secreta spots were present on the abdomen of the fourth instar nymphs, and these morphological characteristics could be used as important markers for identifying gynoparae. Temporal transcriptomic analysis suggested that juvenile hormone (JH) might be involved in regulating the development of gynoparae. After the application JH analog kinoprene to the first instar nymphs, almost all treated individuals failed to complete wing differentiation, and most lost the ability to produce progeny, suggesting the destructive effect of JH on wing differentiation and reproduction of gynoparae. Moreover, exogenous addition of kinoprene also significantly altered the expression levels of four key genes responsible for the synthesis and degradation of JH. Our findings reveal the mechanism by which JH regulated wing differentiation and reproductive capacity of gynoparae, which lay a foundation for the further research on reproduction mode switch in aphids in the future.