Genetic intimacy of filamentous viruses and endoparasitoid wasps
A behavior-manipulating virus relative as a source of adaptive genes for parasitoid wasps
Viruses establish intimate relationships with the cells they infect. The virocell is a novel entity, different from the original host cell and beyond the mere combination of viral and cellular genetic material. In these close encounters, viral and cellular genomes often hybridise, combine, recombine, merge and excise. Such chemical promiscuity leaves genomics scars that can be passed on to descent, in the form of deletions or duplications and, importantly, insertions and back and forth exchange of genetic material between viruses and their hosts.
In this preprint , Di Giovanni and coworkers report the identification of 13 genes present in the extant genomes of members of the Leptopilina wasp genus, bearing sound signatures of having been horizontally acquired from an ancestral virus. Importantly the authors identify Leptopilina boulardi filamentous virus (LbFV) as an extant relative of the ancestral virus that served as donor for the thirteen horizontally transferred genes. While pinpointing genes with a likely possible viral origin in eukaryotic genomes is only relatively rare, identifying an extant viral lineage related to the ancestral virus that continues to infect an extant relative of the ancestral host is remarkable. But the amazing evolutionary history of the Leptopilina hosts and these filamentous viruses goes beyond this shared genes. These wasps are endoparasitoids of Drosophila larvae, the female wasp laying the eggs inside the larvae and simultaneously injecting venom that hinders the immune response. The composition of the venoms is complex, varies between wasp species and also between individuals within a species, but a central component of all these venoms are spiked structures that vary in morphology, symmetry and size, often referred to as virus-like particles (VLPs).
In this preprint, the authors convincingly show that the expression pattern in the Leptopilina wasps of the thirteen genes identified to have been horizontally acquired from the LbFV ancestor coincides with that of the production of VLPs in the female wasp venom gland. Based on this spatio-temporal match, the authors propose that these VLPs have a viral origin. The data presented in this preprint will undoubtedly stimulate further research on the composition, function, origin, evolution and diversity of these VLP structures, which are highly debated (see for instance  and ).
 Di Giovanni, D., Lepetit, D., Boulesteix, M., Ravallec, M., & Varaldi, J. (2018). A behavior-manipulating virus relative as a source of adaptive genes for parasitoid wasps. bioRxiv, 342758, ver. 5 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/342758
 Poirié, M., Colinet, D., & Gatti, J. L. (2014). Insights into function and evolution of parasitoid wasp venoms. Current Opinion in Insect Science, 6, 52-60. doi: 10.1016/j.cois.2014.10.004
 Heavner, M. E., Ramroop, J., Gueguen, G., Ramrattan, G., Dolios, G., Scarpati, M., ... & Govind, S. (2017). Novel organelles with elements of bacterial and eukaryotic secretion systems weaponize parasites of Drosophila. Current Biology, 27(18), 2869-2877. doi: 10.1016/j.cub.2017.08.019
Ignacio Bravo (2018) Genetic intimacy of filamentous viruses and endoparasitoid wasps. Peer Community in Evolutionary Biology, 100062. 10.24072/pci.evolbiol.100062
Revision round #22018-11-23
Decision round #2
Dear Dr. Varaldi
thank you very much for having submitted the revised version of your text to PCI Evol Biol. The same two reviewers that evaluated your text in first instance have provided feedback on the resubmitted one. As you can see in the accompanying reviews, both reviewers acknowlege that you have integrated a large number of their concerns, and I agree with them. Nevertheless, also both reviewers find that some of the points raised have not been properly addressed. I share also this view in what regards to the verbal argumentation of the consistence with the main hypothesis of partial trees that do not present all terminal taxa. I think this is a view that needs be substantiated on quantitative terms rather than on verbal ones. Also, the reviewers mention some instances in the text in which the wording may suggest that you have evidence to sustain a claim for the physical existence of VLPs, that need be substantiated.
Overall, I think that the comments raised by the reviewers can be properly addressed after minor changes to the text, and I think that if you respond in detail point-to-point to each of the criticisms, a third round of peer-review should not be needed.
I sincerely thank you for supporting PCI, and look forward to read your response to the reviewers and the revised version of your text.
Reviewed by Alejandro Manzano-Marín, 2018-10-05 22:56
Reviewed by anonymous reviewer, 2018-10-05 22:57
Revision round #12018-10-05
Decision round #1
thank you very much for submitting your preprint to the open PCI review process. As you can see in the accompanying files, two experts in the field have provided feedback on your submission. Both of them agree on the importance of the question and on the pertinence of the approaches used to tackle it, and I largely agree with them. Also both reviewers have invested a considerable amount of time and energy in providing a detailed report on the manuscript, with an overall very positive judgement on the methods and approaches. Notwithstanding, also both reviewers identify a number of flaws in the text that prevent recommendation in its present state, essentially centered in the , and I also largely agree with them. As you can see in their reviews, some concerns have been raised about the logical flow between results and interpretation. This is the case for instance for the support for the HGT event in the case of all genes depicted in figure 3; for the pertinence of the dn/ds values of conserved arthropod genes used to serve as reference for a set of genes only present in a subtree of these species. In other cases the questions are rather the pertinence and clarity of the figures used, as in fig 1 and fig 2. Finally, I would appreciate if you could include an assessment of the identity of the specimens actually used for the analyses, specially for the case of Ganaspis xanthopoda, as no RNA sequences were available in the screened databases.
Overall, the reviewers and myself are very supportive for recommendation upon revision. I would thus encourage you to respond to each and every point raised in the reviews. In case you think a verbose answer suffices for certain points, I would appreciate if you could make a clear case of scientific cost-benefit evaluation to justify that no novel data generation or analyses are needed.
I look very much forward to reading the revised version of the manuscript.