Factors affecting success in the survival of a parasitoid wasp, Diachasmimorpha longicaudata

Endoparasitoid wasps have evolved associations with domesticated endogenized viruses (DEVs) that derive from virus ancestors. DEVs have lost the ability to replicate in hosts, but they can replicate in female wasps and resulting particles are injected into hosts during egg laying. DEV particles are used by female wasps to transfer gene products that protect wasp offspring from host defenses. Diachasmimorpha longicaudata is a larval-pupal parasitoid of the fruit fly, Anastrepha suspensa, that has recently acquired Diachasmimorpha longicaudata entomopoxvirus (DlEPV). DIEPV differs from DEVs as it remains a fully functional exogenous virus that replicates in flies and venom glands of female wasps. In this study, we investigated factors that maintain the relationship between D. longicaudata and DIEPV. We found little evidence that DIEPV protects wasps from host immune defenses but further investigation revealed that DIEPV delays fly development and ultimately kills them in the absence of wasps. We show that DIEPV strongly benefits the survival of wasp progeny in the absence of superparasitism, but also found that these benefits dose-dependently diminish with superparasitism. In addition, we found that DIEPV cannot persist intergenerationally without passage through wasps. We conclude that DIEPV benefits D. longicaudata by allowing wasps to reduce the number of eggs they lay per host, while D. longicaudata benefits DIEPV by serving as an intermediate host that is essential for persistence and transmission to A. suspensa. Our findings shed light on the potential origins of how a fly-specific virus is transitioning into a beneficial symbiont of a parasitoid.