Benjamin Guinet

Ancient DNA research has primarily focused on host genomes, but the recovery of microbial genomes associated with extinct species remains a major challenge. This study reports the recovery and analysis of ancient host-associated microbial DNA obtained from mammoth remains. By combining state-of-the-art sequencing, authentication frameworks, and comparative genomics, the study identifies microbial lineages preserved in permafrost-preserved mammoth specimens. The findings highlight both the preservation potential of host-associated microbes and their evolutionary significance in understanding host–microbiome interactions over deep time.

Over the course of evolution, hymenopteran parasitoids have developed a close relationship with heritable viruses, sometimes integrating viral genes into their chromosomes. For example, in Drosophila parasitoids belonging to the Leptopilina genus, 13 viral genes from the Filamentoviridae family have been domesticated to deliver immunosuppressive factors to host immune cells, thereby protecting parasitoid offspring from the host immune response. The present study aims to comprehensively characterize this domestication event in terms of the viral genes involved, the wasp diversity affected by this event and its chronology. Our genomic analysis of 41 Cynipoidea wasps from six subfamilies revealed 18 viral genes that were endogenized during the early radiation of the Eucoilini/Trichoplastini clade around 75 million years ago. Wasps from this highly diverse clade develop not only from Drosophila but also from a variety of Schizophora. This event coincides with the radiation of Schizophora, a highly speciose Diptera clade, suggesting that viral domestication facilitated wasp diversification in response to host diversification. Additionally, in one of the species, at least one viral gene was replaced by another gene derived from a related filamentovirus. This study highlights the impact of viral domestication on the diversification of parasitoid wasps.

Large dsDNA viruses from the Naldaviricetes class are currently composed of four viral families infecting insects and/or crustaceans. Since the 1970s, particles described as filamentous viruses (FVs) have been observed by electronic microscopy in several species of Hymenoptera parasitoids but until recently, no genomic data was available. This study provides the first comparative morphological and genomic analysis of these FVs. We analyzed the genomes of seven FVs, six of which were newly obtained, to gain a better understanding of their evolutionary history. We show that these FVs share all genomic features of the Naldaviricetes while encoding five specific core genes that distinguish them from their closest relatives, the Hytrosaviruses. By mining public databases, we show that FVs preferentially infect Hymenoptera with parasitoid lifestyle and that these viruses have been repeatedly integrated into the genome of many insects, particularly Hymenoptera parasitoids, overall suggesting a long-standing specialization of these viruses to parasitic wasps. Finally, we propose a taxonomical revision of the class Naldaviricetes in which FVs related to the Leptopilina boulardi FV constitute a fifth family. We propose to name this new family, Filamentoviridae.

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.

Some species of parasitic wasps have domesticated viral machineries to deliver immunosuppressive factors to their hosts. Up to now, all described cases fall into the Ichneumonoidea superfamily, which only represents around 10% of hymenoptera diversity, raising the question of whether such domestication occurred outside this clade. Furthermore, the biology of the ancestral donor viruses is completely unknown. Since the 1980’s, we know that Drosophila parasitoids belonging to the Leptopilina genus, which diverged from the Ichneumonoidea superfamily 225My ago, do produce immuno-suppressive viruslike structure in their reproductive apparatus. However, the viral origin of these structures has been the subject of debate. In this paper, we provide genomic and experimental evidence that those structures do derive from an ancestral virus endogenization event. Interestingly, its close relatives induce a behaviour manipulation in present-day wasps. Thus, we conclude that virus domestication is more prevalent than previously thought and that behaviour manipulation may have been instrumental in the birth of such associations.