A viral mutualist employs post-hatch transmission for vertical and horizontal spread among parasitoid wasps

Authors: Coffman, Kelsey; HARKINSON, QUINN - University Of Georgia; BURKE, GAELEN - University Of Georgia

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/10/2022
Publication Date: 4/11/2022
Citation: Coffman, K.A., Harkinson, Q.M., Burke, G.R. 2022. A viral mutualist employs post-hatch transmission for vertical and horizontal spread among parasitoid wasps. Proceedings of the National Academy of Sciences(PNAS). 119. https://doi.org/10.1073/pnas.2120048119.
DOI: https://doi.org/10.1073/pnas.2120048119

Interpretive Summary: The crucial roles that microbes play in insect biology often result in hereditary associations, in which microbes are passed down from insect parents to offspring. This type of microbial inheritance can strengthen a symbiotic relationship by aligning the fitness of the microbe to that of its insect host. Parasitoid wasps, which are obligate parasites of other insects, have repeatedly formed heritable associations with viruses that are beneficial to the wasps during development. Most of these viruses are permanently integrated within their respective wasp genomes, and therefore are transmitted through the wasp germline. However, a heritable poxvirus, known as Diachasmimorpha longicaudata entomopoxvirus (DlEPV), may display alternative transmission modes within Diachasmimorpha longicaudata wasps and their fruit fly hosts due to its non-integrated genome. In this study, we discovered a novel form of beneficial virus transmission, in which virus particles were acquired by developing wasps after they hatched, rather than through the germline. Our findings therefore indicate that DlEPV is the first beneficial virus shown to utilize post-hatch transmission within parasitoid wasps. In addition, our results demonstrated limited viral transmission within fruit fly hosts, implying that DlEPV transmission has evolved to be fully dependent on parasitoid wasps.

Technical Abstract: Heritable symbionts display a wide variety of transmission strategies to travel from one insect generation to the next. Parasitoid wasps, one of the most diverse insect groups, maintain several heritable associations with viruses that are beneficial for wasp survival during development as parasites of other insects. Most of these beneficial viral entities are strictly transmitted through the wasp germline as endogenous viral elements (EVEs) within wasp genomes. However, a beneficial poxvirus inherited by Diachasmimorpha longicaudata wasps, known as Diachasmimorpha longicaudata entomopoxvirus (DlEPV), is not integrated into the wasp genome and therefore, may employ different tactics to infect future wasp generations. Here, we demonstrated that DlEPV transmission is dependent on parasitoid wasps and uncovered a previously undocumented form of post-hatch transmission for a mutualistic virus, entailing external acquisition and localization of the virus within the adult wasp venom gland. We showed that this route is extremely effective for vertical and horizontal transmission of the virus within D. longicaudata wasps. Furthermore, the beneficial phenotype provided by DlEPV during parasitism was also transmitted with perfect efficiency, indicating an effective mode of symbiont spread to the advantage of infected wasps. These results provide novel insight into how beneficial viruses can be transmitted among insects.