Cloak Scavenges the Reactive Oxygen Species around the Larvae of Drino inconspicuoides (Diptera: Tachinidae)

SIMPLE SUMMARY: The tachinid fly Drino inconspicuoides parasitizes various lepidopteran larvae, including Noctuidae and Nymphalidae. The adult female oviposits the eggs on the surface of the host, and the hatched larvae immediately penetrate into the host hemocoel and develop there during the larval stage. The caterpillar possesses immune defense mechanisms to eliminate such invaders, but the tachinid larva can avoid these defenses. Within 24 h, the parasitizing larva is surrounded by a black pigmented structure called the “funnel”, and the larva and the funnel are wrapped with a cottony structure called the “cloak”. The funnel is a physically rigid structure that penetrates the epidermis of the host, allowing the larva to breathe through contact with the outside air. This study aimed to clarify the function of the cloak, which has not previously been elucidated. Our findings suggest that formation of the funnel generates ROS, but that these are detoxified in the cloak to enhance the survival of the tachinid larva. The funnel and cloak are composed of host cells. Our study provides insight into the parasitic strategy of a tachinid fly by through which it ingeniously diverts host cells. ABSTRACT: Drino inconspicuoides (Diptera: Tachinidae) is an endoparasitoid that develops inside the lepidopteran host. When the larva of D. inconspicuoides penetrates into the host, Mythimna separata (Lepidoptera: Noctuidae), the larva creates a cap-like structure, called the funnel, by using host hemocytes, forming a respiratory attachment to permit efficient respiration. A newly described cloudy and cottony structure, called the “cloak”, is formed outside the funnel within 24 h of parasitism. The cloak contains the host fat body and hemocytes. In this study, we aimed to clarify the function of the cloak, which has to date remained unknown. We hypothesized that the funnel generates reactive oxygen species (ROS) through melanization, and that the cloak detoxifies them. We confirmed that the black pigments of the funnel were caused by melanization, which inevitably generates ROS that are potentially harmful to the D. inconspicuoides larva inside the funnel. The cloak showed high activities of antioxidant enzymes, including superoxide dismutase, glutathione peroxidase, and catalase. These results suggest that the cloak scavenged the ROS from the melanized funnel through the diversion of antioxidant enzymes in the fat body, thereby protecting the D. inconspicuoides larva from oxidative damage.