Endoparasitoid lifestyle promotes endogenization and domestication of dsDNA viruses

• Published in: eLife 2023-06, Vol.12
• Main Authors: Guinet, Benjamin, Lepetit, David, Charlat, Sylvain, Buhl, Peter N, Notton, David G, Cruaud, Astrid, Rasplus, Jean-Yves, Stigenberg, Julia, de Vienne, Damien M, Boussau, Bastien, Varaldi, Julien
• Format: Article
• Language: English
• Subjects: Animal genetics; Animals; Biodiversity; Biological Evolution; DNA; DNA viruses; Domestication; Double-stranded RNA; dsDNA virus; Ecology, environment; Eggs; Endoparasites; EVE; Evolutionary Biology; Female; Genetics; Genetics and Genomics; Genome, Viral; Genomes; horizontal gene transfer; Hymenoptera; Hypotheses; Life Sciences; Lifestyles; Membrane fusion; Microbiology and Parasitology; parasitoid; Populations and Evolution; Symbiosis; Virology; Virulence; Virulence factors; Viruses; Viruses - genetics; Wasps - genetics
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.85993

The accidental endogenization of viral elements within eukaryotic genomes can occasionally provide significant evolutionary benefits, giving rise to their long-term retention, that is, to viral domestication. For instance, in some endoparasitoid wasps (whose immature stages develop inside their hosts), the membrane-fusion property of double-stranded DNA viruses have been repeatedly domesticated following ancestral endogenizations. The endogenized genes provide female wasps with a delivery tool to inject virulence factors that are essential to the developmental success of their offspring. Because all known cases of viral domestication involve endoparasitic wasps, we hypothesized that this lifestyle, relying on a close interaction between individuals, may have promoted the endogenization and domestication of viruses. By analyzing the composition of 124 Hymenoptera genomes, spread over the diversity of this clade and including free-living, ecto, and endoparasitoid species, we tested this hypothesis. Our analysis first revealed that double-stranded DNA viruses, in comparison with other viral genomic structures (ssDNA, dsRNA, ssRNA), are more often endogenized and domesticated (that is, retained by selection) than expected from their estimated abundance in insect viral communities. Second, our analysis indicates that the rate at which dsDNA viruses are endogenized is higher in endoparasitoids than in ectoparasitoids or free-living hymenopterans, which also translates into more frequent events of domestication. Hence, these results are consistent with the hypothesis that the endoparasitoid lifestyle has facilitated the endogenization of dsDNA viruses, in turn, increasing the opportunities of domestications that now play a central role in the biology of many endoparasitoid lineages.