Ovomermis sinensis parasitism arrests midgut replacement by altering ecdysone and juvenile hormone in Helicoverpa armigera larvae

Many entomopathogens regulate the development of their insect hosts. However, the influence of mermithid nematodes on the development of their host remains unclear. In the current study, we provide insights into how Ovomermis sinensis parasitism affects the development of Helicoverpa armigera. We observed that O. sinensis arrests host development, as evidenced by the reduced body size and failure of Helicoverpa armigera to pupate. Moreover, midgut replacement of the host was significantly blocked by parasitism. Furthermore, juvenile hormone (JHIII) titers of the host were dramatically elevated by parasitism, but JH esterase (JHE) activities were strongly inhibited. By contrast, steroid hormone (20–hydroxyecdysone, 20E) titers of the host were significantly depressed by parasitism on days 4–6. The expression profiles of hormone-related genes in the host also showed similar patterns with the hormone titer. For this reason, rescue experiments were performed by injecting 20E and JHIII into developmentally arrested hosts. Notably, the midgut replacement of the host was rescued by the injection of 20E, whereas JHIII injection resulted in negative effects. Altogether, O. sinensis arrests H. armigera midgut replacement by reducing 20E and maintaining JH, thereby causing developmental arrests. Our study is the first report of the possible mechanism of mermithid nematodes in regulating insect development.