Cotesia parasitoid wasps and their endogenous viruses: harmonious relationships in an old couple

Parasitoid wasps of the genus Cotesia, which develop within caterpillars, have been used worldwide for biological control. One of the critical factors for impact of these parasitoid wasps on their pest hosts is possession of a bracovirus, an endogenous virus lineage associated with tens of thousands of parasitoid wasp species. Injected with the wasp eggs, bracovirus particles alter the caterpillar immune defenses, allowing parasite development. To understand how an endogenous virus evolves when it confers a benefit to its host, we aimed to obtain a comprehensive comparative view of the organization of the bracovirus DNA within wasp chromosomes, and of gene expression during the production of the viral particles. We determined the high quality 207 MB genome sequence of Cotesia congregata, assembled in 10 scaffolds using HiC, and draft genomes of 5 Cotesia species. Twenty-five genes of nudiviral origin were located in a region amplified during the production of particles, whereas the others were dispersed widely in the chromosomes, some of them having undergone a large expansion, comparable to that of some olfactory receptor genes, but not found in similar extent for immune or detoxification genes. Viral genes involved in parasitism success were clustered into 5 regions, the largest encoding 77% of them. Transcriptome analysis showed that genes involved in viral transcription were the first nudiviral genes expressed, whereas wasp immune genes were not induced. Although dispersed in the chromosomes, most nudiviral genes display coordinated expression patterns, suggesting they are still under nudiviral transcriptional control. The viral activity is, however, no longer perceived as pathogenic by the wasp. These results suggest that conflicts might disappear between symbiotic partners when the association is ancient and benefits converge.