Horizontal transfers of polydnavirus segments extend the known range of parasitoid attacks to stick insects and orthopterans

Horizontal gene transfer occurs beyond anecdotal frequencies in metazoans. Among insects, some parasitoid wasps even carry gene delivery agents called polydnaviruses (PDVs). These domesticated viral elements mediate the integration of wasp genes into the genome of parasitized hosts, thereby protecting developing larvae from immune defenses. The frequency of PDV-mediated transfers is sufficiently high that it could be exploited to better characterize the range of organisms attacked by parasitoid wasps. Here, we apply this rationale by screening for the specific molecular footprints of these transfers in 6,814 protostome genomes. We found a total of 6,556 PDV-mediated integrations, all of which were in insects. The distribution of these integrations is highly consistent with the known host range of PDV-encoding parasitoid wasps. Most were found in lepidopterans (6,260 integrations in 303 species) – the main hosts of PDV-encoding wasps – and a few were retrieved in sawflies (139 integrations in 14 species) and leaf beetles (4 integrations in 2 species), also known to be parasitized by some of these wasps. Remarkably, we found a total of 232 integrations in 3 species of stick insects and one integration in an orthopteran, two insect lineages that have never been reported to be attacked by PDV-encoding wasps. We show that these integrations are mostly recent and that stick insects and sawflies were attacked recurrently, by multiple wasp lineages. Overall, our study warrants accounting for stick insects and orthopterans as possible new targets of parasitoid attacks, both in community ecology and in assessments of biological control strategies.