Domestications Virales et Transferts Horizontaux dans les Systèmes Hôtes-Parasitoïdes

Eukaryotic genomes retain traces of integrated viral sequences, remnants of ancient infections. Most of them gradually degenerate over generations. However, some have been preserved by natural selection and provide crucial functions to the host organism, a phenomenon known as viral domestication.In certain clades of parasitoid insects, (i.e. whose larval stages develop as internal parasites within a host), entire viral machineries have been domesticated. Viral genes are used to produce particles that are injected into the host along with the egg. These particles actively suppress the host’s immune system, thereby facilitating successful parasitism. Depending on the lineage, these systems are used either to deliver viral proteins (in the case of virus-like particles, or VLPs) or circular DNA (in the case of PolyDNAviruses, or PDVs). Such domesticated systems have evolved independently several times across parasitoid wasp lineages, particularly within the superfamily Ichneumonoidea, and represent the most advanced cases of viral domestication known in animals.This PhD work investigates, at multiple scales, the origin, evolutionary fate, and functional consequences of viral sequences found in the genomes of parasitoid insects. It builds on a unique dataset generated within our team, including extensive genomic sampling of parasitoid wasps and flies, along with their lepidopteran hosts, all collected from the Guanacaste conservation area in Costa Rica. The study relies on comparative genomics approaches to document viral integration events and their implications.Given the convergent patterns of viral domestication described in Hymenoptera, a key question arises: are these convergences specific to this order, or do they reflect a broader phenomenon linked to the endoparasitoid lifestyle? To address this, I extended the analysis to Diptera endoparasitoid species. Tachinid genomes contain numerous EVEs, yet these insertions are mostly recent and species specific, with no evidence of genome-wide domestication comparable to the PolyDNAviruses or virus-like particles seen in wasps.I then focused on domesticated viruses in parasitoid wasps. I performed large-scale analyses of the conservation of viral genes involved in the formation of PolyDNAvirus (PDVs) and Virus-Like-Particles (VLPs). Results show that, once established, these systems are remarkably stable with most domesticated genes belonging to a deeply conserved functional core. In the course of these analyses, sequencing data unexpectedly revealed a free-living virus related to ichnoviruses, the PDVs found in certain Ichneumonidae. This discovery confirms the viral origin of ichnoviruses and provides the first sequence of a modern relative of the ancestral donor virus.By transferring wasp DNA into the host, the PDV system constitutes a potential mechanism of horizontal gene transfer between insects. In an ongoing project, I explore this possibility by evaluating the contribution of PDVs to horizontal transfers that are detected between the parasitoids and their hosts.Through bioinformatic analyses applied to a large dataset generated by our team, this thesis examines horizontal gene transfer from multiple perspectives, ranging from virus-to-eukaryote exchanges to virus-mediated transfers between eukaryotic species.