Wolbachia-Driven Memory Loss in a Parasitic Wasp Increases Superparasitism to Enhance Horizontal Transmission

Horizontal transmission of the endosymbiont, Wolbachia, may occur during superparasitism when parasitoid females deposit a second clutch of eggs on a host. Wolbachia may increase the superparasitism tendency of Trichogramma wasps by depriving their memory. To test this hypothesis, we investigated the effects of conditioning experience and memory inhibitors (actinomycin D [ACD] and anisomycin [ANI]) on memory capacity, and expressions of memory-related genes (CREB1 and PKA), and superparasitism frequency of Wolbachia-infected (TDW) and uninfected (TD) lines of Trichogramma dendrolimi after conditioning with lemon or peppermint odor. We detected the presence of Wolbachia in eggs, larvae, pre-pupae, pupae, and adults of Trichogramma by using fluorescence in situ hybridization. The results showed that TDW females had a more reduced memory capacity than TD females after conditioning. Compared with TD females, TDW females showed a higher proportion of superparasitism and a downregulation of CREB1 and PKA genes after conditioning. TD females fed ACD or ANI showed a higher tendency for superparasitism and a downregulation of CREB1 and PKA, along with memory loss after conditioning than TD females fed honey solution only. The presence of Wolbachia was detected in the anterior region of the larva, pre-pupa, and pupa, but was not found in the head of the adult. The results provide evidence of host behavioral manipulation of Wolbachia by depriving memory of host Trichogramma wasps based on Poulin' s criteria. These host behavioral changes led by Wolbachia may be caused by the virulence of Wolbachia on the nervous system of the host. IMPORTANCE The endosymbiotic bacteria, Wolbachia, live widely within cells of arthropods. Wolbachia are not only transmitted vertically from host mother to offspring, but are also transmitted horizontally among host individuals. Horizontal transmission is expected to occur during superparasitism when host parasitoid females deposit a clutch of eggs on a host previously parasitized by the same parasitoid species. Thus, a question is proposed regarding whether superparasitism behavior is a behavior modification induced by the symbiont to favor symbiont transmission. This study highlights behavioral mechanisms of Wolbachia-induced superparasitism in Trichogramma wasps and the manipulation of symbionts on host parasitoids.