Transcriptome dynamics of mutualistic poxvirus infection of tropical fruit fly hosts

Parasitoid wasps are one of the most species-rich groups of animals on Earth, due to their ability to successfully develop as parasites of nearly all types of insects. Unlike most known parasitoid wasps that specialize within one or a few host species, Diachasmimorpha longicaudata is a generalist that can survive within multiple genera of tephritid fruit fly hosts, including many globally important pest species. D. longicaudata has therefore been widely released to suppress pest populations as part of biological control efforts in tropical and subtropical agricultural systems. In this study, we investigated the role of a mutualistic poxvirus in shaping the host range of D. longicaudata across three genera of agricultural pest species: two of which are permissive hosts for D. longicaudata parasitism and one that is a nonpermissive host. We found that permissive hosts Ceratitis capitata and Bactrocera dorsalis were highly susceptible to virus infection, displaying rapid virus replication and abundant fly mortality. However, the nonpermissive host Zeugodacus cucurbitae largely overcame virus infection, exhibiting substantially lower mortality and no virus replication. Further investigation of transcriptional dynamics during virus infection demonstrated hindered viral gene expression and limited changes in fly gene expression within the nonpermissive host compared to the permissive species, indicating that the host range of the viral symbiont may dictate the host range of D. longicaudata wasps. These findings also reveal that viral symbiont activity may be a major contributor to the success of D. longicaudata as a generalist parasitoid species and a globally successful biological control agent. Overall design: We deep-sequenced total polyadenylated mRNA from 81 whole body fly samples: 3 biological replicate samples were collected at 0, 12, and 24 h post injection for both 1x and 0.1x viral doses, along with a saline-injected mock “dose” in three different fly species.