Endoparasitoid lifestyle promotes endogenization and domestication of dsDNA viruses.. Parasitoid wasps

During evolution, accidental integration of viral elements within eukaryotic genome may occur. These elements can sometimes provide major evolutionary advantages to recipient genomes: this is known as viral domestication. For instance, in some endo-parasitoid wasps (whose immature stages develop inside their hosts), the fusogenic property of viruses has been repeatedly domesticated following ancestral dsDNA viral integrations. Those endogenized viral genes are used by the female wasps as a delivery tool to inject virulence factors, essential to the developmental success of their offspring. Because all known cases of viral domestication involved endo-parasitic wasps, we hypothesized that this lifestyle (promoting close interaction between individuals) may have favored endogenization and domestication of viruses. By analyzing the genomic composition of 124 Hymenoptera genomes spread over the diversity of Hymenoptera and including free-living, ecto and endo-parasitoid species, we tested this hypothesis. Our analysis first revealed that double-stranded DNA viruses were more often endogenized and domesticated than expected based on their estimated relative abundance in viral communities infecting insects compared to other virus genomic structures (ssDNA, dsRNA, ssRNA). Secondly, our analysis revealed that endogenization and domestication of dsDNA viruses were more frequent in lineages with endo-parasitoid lifestyle compared to lineages with ecto-parasitoids or free-living lifestyles. Hence, these results suggest that endo-parasitoidism has favored the domestication of dsDNA viruses or conversely that dsDNA virus domestication has favored the evolution of endo-parasitoidism.