PMID- 35412888 OWN - NLM STAT- MEDLINE DCOM- 20220414 LR - 20221012 IS - 1091-6490 (Electronic) IS - 0027-8424 (Print) IS - 0027-8424 (Linking) VI - 119 IP - 16 DP - 2022 Apr 19 TI - A viral mutualist employs posthatch transmission for vertical and horizontal spread among parasitoid wasps. PG - e2120048119 LID - 10.1073/pnas.2120048119 [doi] LID - e2120048119 AB - 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 their development as parasites of other insects. Most of these beneficial viral entities are strictly transmitted through the wasp germline as endogenous viral elements 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 transmission of DlEPV is primarily dependent on parasitoid wasps, since viral transmission within fruit fly hosts of the wasps was limited to injection of the virus directly into the larval fly body cavity. Additionally, we uncovered a previously undocumented form of posthatch transmission for a mutualistic virus that entails 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 insight into the transmission of beneficial viruses among insects and indicate that viruses can share features with cellular microbes during their evolutionary transitions into symbionts. FAU - Coffman, Kelsey A AU - Coffman KA AUID- ORCID: 0000-0002-7609-6286 AD - Daniel K. Inouye US Pacific Basin Agricultural Research Center, Agricultural Research Service, US Department of Agriculture, Hilo, HI 96720. FAU - Hankinson, Quinn M AU - Hankinson QM AUID- ORCID: 0000-0001-6090-5299 AD - Department of Entomology, University of Georgia, Athens, GA 30602. FAU - Burke, Gaelen R AU - Burke GR AUID- ORCID: 0000-0003-3472-0420 AD - Department of Entomology, University of Georgia, Athens, GA 30602. LA - eng PT - Journal Article DEP - 20220411 PL - United States TA - Proc Natl Acad Sci U S A JT - Proceedings of the National Academy of Sciences of the United States of America JID - 7505876 SB - IM MH - Animals MH - Biological Evolution MH - *Entomopoxvirinae/physiology MH - *Host Microbial Interactions MH - *Symbiosis MH - *Tephritidae/virology MH - *Wasps/genetics/virology PMC - PMC9169864 OTO - NOTNLM OT - Diachasmimorpha longicaudata OT - parasitoid wasp OT - poxvirus OT - symbiosis OT - transmission COIS- The authors declare no competing interest. EDAT- 2022/04/13 06:00 MHDA- 2022/04/15 06:00 PMCR- 2022/10/11 CRDT- 2022/04/12 17:11 PHST- 2022/04/12 17:11 [entrez] PHST- 2022/04/13 06:00 [pubmed] PHST- 2022/04/15 06:00 [medline] PHST- 2022/10/11 00:00 [pmc-release] AID - 202120048 [pii] AID - 10.1073/pnas.2120048119 [doi] PST - ppublish SO - Proc Natl Acad Sci U S A. 2022 Apr 19;119(16):e2120048119. doi: 10.1073/pnas.2120048119. Epub 2022 Apr 11.