Sex-biased juvenile hormone and gene expression underlie sex difference of stress resistance in the American cockroach

Abstract

Sexually dimorphic traits are prevalent throughout the animal kingdom, extending to insects. In addition to sex-biased gene expression networks, these traits often involve variations in hormone levels. Juvenile hormone (JH), which is synthesized by corpora allata (CA), regulates development and reproduction in insects. However, there is limited understanding regarding sex-biased gene expression in CA and the sexually dimorphic functions of JH. We discovered sexual dimorphism in JH levels in cockroaches. To explore the underlying mechanism, we analyzed RNA-sequencing data from CA tissues in the adult females and males of the American cockroach, Periplaneta americana. Our investigation revealed significant variation in sex-biased gene expression, with female-biased genes primarily involved in cytochrome P450, glutathione S-transferase and peroxidase pathways, associating with resistance to environmental stress. Notably, exposure to the insecticide imidacloprid, injection of Escherichia coli and H₂O₂ led to a higher mortality rate in males, whereas females exhibited resistance. Importantly, the application of the JH analog methoprene following the injection of E. coli and H₂O₂ rescued survival and the expression of stress response-related genes in males. Furthermore, these stressors resulted in reduced JH biosynthesis in males, while females remained unaffected. In summary, our results reveal that sexually dimorphic JH levels and gene expression modulate stress responses in P. americana. These findings shed light on sex-specific responses to environmental stress, offering tailored strategies for pest control based on gender.