What makes a parasite successful? Parasitoid wasp venoms evolve rapidly in a host-specific manner
Parasitic success and venom composition evolve upon specialization of parasitoid wasps to different host species
Parasitoid wasps have developed different mechanisms to increase their parasitic success, usually at the expense of host survival (Fellowes and Godfray, 2000). Eggs of these insects are deposited inside the juvenile stages of their hosts, which in turn deploy several immune response strategies to eliminate or disable them (Yang et al., 2020). Drosophila melanogaster protects itself against parasitoid attacks through the production of specific elongated haemocytes called lamellocytes which form a capsule around the invading parasite (Lavine and Strand, 2002; Rizki and Rizki, 1992) and the subsequent activation of the phenol-oxidase cascade leading to the release of toxic radicals (Nappi et al., 1995). On the parasitoid side, robust responses have evolved to evade host immune defenses as for example the Drosophila-specific endoparasite Leptopilina boulardi, which releases venom during oviposition that modifies host behaviour (Varaldi et al., 2006) and inhibits encapsulation (Gueguen et al., 2011; Martinez et al., 2012).
Studies have shown that the wasp parasitic capacity is correlated to venom presence and its content (Colinet et al., 2009; Poirié et al., 2014), including that evolution of venom protein composition is driven by different levels of host susceptibility to infection (Cavigliasso et al., 2019). However, it had not been determined to this day, if and how parasitic range can affect venom protein composition and to which extent host specialization requires broad-spectrum factors or a plethora of specialized components.
These outstanding questions are now approached in a study by Cavigliasso and colleagues (Cavigliasso et al., 2021), where they perform experimental evolution of L. boulardi for 9 generations exposing it to different Drosophila host species and genetic backgrounds (two strains of D. melanogaster, D. simulans and D. yakuba). The authors tested whether the parasitic success of each selection regime was host-specific and how they influenced venom composition in parasitoids. For the first part, infection outcomes were assayed for each selection regime when cross-infecting different hosts. To get a finer measurement of the mechanisms under selection, the authors differentiated three phenotypes: overall parasitic success, encapsulation inhibition and escape from capsule. Throughout the course of experimental evolution, only encapsulation inhibition did not show an improved response upon selection on any host. Importantly, the cross-infection scenario revealed a clear specificity to the selected host for each evolved resistance.
As for venom composition, a trend of differential evolution was detected between host species, although a significant part of that was due to a larger differentiation in the D. yakuba regime, which showed a completely different directionality. Importantly, the authors could identify some of the specific proteins targeted by the several selection regimes, whether selected or counter-selected for. Interestingly, the D. yakuba regime is the only case where the key parasitoid protein LbSPNy (Colinet et al., 2009) was not counter-selected and the only regime in which the overall venom composition did not evolve towards the Ism strain, one of the two ancestral strains of L. boulardi used in the study. It is possible that these two results are correlated, since LbSPNy has been described to inhibit activation of the phenoloxidase cascade in D. yakuba and is one of the most abundant proteins in the ISy venom, making it a good target for selection (Colinet et al., 2013). The authors also discuss the possibility that this difference is related to the geographical distribution of the strains of L. boulardi, since each coincide with either D. melanogaster or D. yakuba.
This methodologically broad work by Cavigliasso and colleagues constitutes an important experimental contribution towards the understanding of how parasitoid adaptation to specific hosts is achieved at different phenotypic and mechanistic levels. It provides compelling evidence that venom composition evolves differently in response to specific parasitic ranges, particularly considering the evolutionary difference between the selective hosts. In line with this result, it is also concluded that the majority of venom proteins selected are lineage-specific, although a few broad-spectrum factors could also be detected.
The question of whether parasitic range can affect venom composition and parasitic success is still open to more contributions. A potentially interesting long-term direction will be to use a similar setup of experimental evolution on the generalist L. heterotoma (Schlenke et al., 2007) . On a more immediate horizon, comparing the venom evolution of both L. heterotoma and L. boulardi under selection with different hosts and under cross-infection scenarios could reveal interesting patterns. The recent sequencing of the L. boulardi genome together with the vast number of studies addressing mechanisms of Drosophila resistance to parasitoid infection, will enable the thorough characterization of the genetic basis of host-parasitoid interactions and the deeper understanding of these ubiquitous and economically-relevant relationships.
*This recommendation text has been co-written with Tânia F. Paulo who is not a recommender of PCI Evol Biol
Cavigliasso, F., Mathé-Hubert, H., Gatti, J.-L., Colinet, D. and Poirié, M. (2021) Parasitic success and venom composition evolve upon specialization of parasitoid wasps to different host species. bioRxiv, 2020.10.24.353417, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.10.24.353417
Cavigliasso, F., Mathé-Hubert, H., Kremmer, L., Rebuf, C., Gatti, J.-L., Malausa, T., Colinet, D., Poiré, M. and Léne. (2019). Rapid and Differential Evolution of the Venom Composition of a Parasitoid Wasp Depending on the Host Strain. Toxins, 11(629). https://doi.org/10.3390/toxins11110629
Colinet, D., Deleury, E., Anselme, C., Cazes, D., Poulain, J., Azema-Dossat, C., Belghazi, M., Gatti, J. L. and Poirié, M. (2013). Extensive inter- and intraspecific venom variation in closely related parasites targeting the same host: The case of Leptopilina parasitoids of Drosophila. Insect Biochemistry and Molecular Biology, 43(7), 601–611. https://doi.org/10.1016/j.ibmb.2013.03.010
Colinet, D., Dubuffet, A., Cazes, D., Moreau, S., Drezen, J. M. and Poirié, M. (2009). A serpin from the parasitoid wasp Leptopilina boulardi targets the Drosophila phenoloxidase cascade. Developmental and Comparative Immunology, 33(5), 681–689. https://doi.org/10.1016/j.dci.2008.11.013
Fellowes, M. D. E. and Godfray, H. C. J. (2000). The evolutionary ecology of resistance to parasitoids by Drosophila. Heredity, 84(1), 1–8. https://doi.org/10.1046/j.1365-2540.2000.00685.x
Gueguen, G., Rajwani, R., Paddibhatla, I., Morales, J. and Govind, S. (2011). VLPs of Leptopilina boulardi share biogenesis and overall stellate morphology with VLPs of the heterotoma clade. Virus Research, 160(1–2), 159–165. https://doi.org/10.1016/j.virusres.2011.06.005
Lavine, M. D. and Strand, M. R. (2002). Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology, 32(10), 1295–1309. https://doi.org/10.1016/S0965-1748(02)00092-9
Martinez, J., Duplouy, A., Woolfit, M., Vavre, F., O’Neill, S. L. and Varaldi, J. (2012). Influence of the virus LbFV and of Wolbachia in a host-parasitoid interaction. PloS One, 7(4), e35081. https://doi.org/10.1371/journal.pone.0035081
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Poirié, M., Colinet, D. and Gatti, J. L. (2014). Insights into function and evolution of parasitoid wasp venoms. Current Opinion in Insect Science, 6, 52–60. https://doi.org/10.1016/j.cois.2014.10.004
Rizki, T. M. and Rizki, R. M. (1992). Lamellocyte differentiation in Drosophila larvae parasitized by Leptopilina. Developmental and Comparative Immunology, 16(2–3), 103–110. https://doi.org/10.1016/0145-305X(92)90011-Z
Schlenke, T. A., Morales, J., Govind, S. and Clark, A. G. (2007). Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathogens, 3(10), 1486–1501. https://doi.org/10.1371/journal.ppat.0030158
Varaldi, J., Petit, S., Boulétreau, M. and Fleury, F. (2006). The virus infecting the parasitoid Leptopilina boulardi exerts a specific action on superparasitism behaviour. Parasitology, 132(Pt 6), 747–756. https://doi.org/10.1017/S0031182006009930
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Élio Sucena (2021) What makes a parasite successful? Parasitoid wasp venoms evolve rapidly in a host-specific manner. Peer Community in Evolutionary Biology, 100124. 10.24072/pci.evolbiol.100124
Evaluation round #110 Dec 2020
DOI or URL of the preprint: https://doi.org/10.1101/2020.10.24.353417
Version of the preprint: 1
Decision by Élio Sucena
This manuscript by Cavigliasso, Colinet, Poirié and co-workers, tests the relationship between the evolution of parasitic success and venom composition in L. boulardi and several Drosophila hosts. It combines a wide range of techniques to connect the evolutionary process to its underlying molecular genetics. This is a thorough and courageous approach to a difficult problem of ultimately understanding the mechanisms that “make a parasite successful”. They also explore the specificity versus generality of the evolved responses touching upon another central question in evolutionary biology. All three reviewers are generally positive about the manuscript, and concur on the originality and importance of the approach and of the question posed. However, they also suggest important clarifications, additions and extensions that would benefit the manuscript. A great deal of the proposed changes are mostly directed to improve the reading, the clarify of its data and message, and to deepen some aspects of its conclusions and discussion. Discussion/interpretation Several requests and recommendations have been put forward by reviewers that I summarize as: 1) Reviewer 2 expresses concern with the interpretation of mel SNasr venom composition evolution as it could derive from an experimental design artifact. Please address this concern argumentatively or experimentally; 2) The potential paradox between survival at 100% (sim and mel strains) and the evolution of venom composition (reviewer #2) must be addressed; 3) The relationship between the success of experimental evolution and the phylogenetic distance of the host used relative to the parasitoid strain; 4) Reviewer #3 has an interesting suggestion to correlate venom evolution with the two distinct strategies for parasitic success (avoidance and evasion), as well as some mention/discussion of parthenogenesis that you may consider; 5) Another potential relationship to explore and discuss pertains to the success of experimental evolution (replicate extinction) vis-a-vis the phylogenetic distance of the host used relative to the parasitoid strain. Analyses and Format: All reviewers have remarks concerning the presentation of the data that should be revised, mostly to ease the reader´s job. 1) Address the issue of infection status classification (reviewer 2#) 2) Reviewer #1 concerns and suggestions (shared by reviewer #2 and myself) regarding figures 1 and 3 and tables 1 and 2. In addition, please review some of the legends (tables and figures) to ensure all necessary elements are provided to fully understand the information they contain. For example, what is “estimate” on figures S2 and S3, how what is calculated and what does it mean? 3) Justify and explain the use of MANOVA and address the apparent lack of nesting raised by reviewer #1 and correct the minor points on statistics presentation pointed out by reviewer #2. 4) I am not sure about this but I wonder if figure S1 should not be part of the main text. I find it really helpful… 5) Please consider the remaining small points included in all three reviews. A final recommendation would be to revise the syntax throughout the manuscript. It need not be Shakespeare but some revision would ease the read. For example, the second term of the first two sentences of the introduction need revision: “and strong selection…success”; “but also host species”. **Additional requirements of the managing board**: As indicated in the 'How does it work?’ section and in the code of conduct, please make sure that: -Data are available to readers, either in the text or through an open data repository such as Zenodo (free), Dryad or some other institutional repository. Data must be reusable, thus metadata or accompanying text must carefully describe the data. -Details on quantitative analyses (e.g., data treatment and statistical scripts in R, bioinformatic pipeline scripts, etc.) and details concerning simulations (scripts, codes) are available to readers in the text, as appendices, or through an open data repository, such as Zenodo, Dryad or some other institutional repository. The scripts or codes must be carefully described so that they can be reused. -Details on experimental procedures are available to readers in the text or as appendices. -Authors have no financial conflict of interest relating to the article. The article must contain a "Conflict of interest disclosure" paragraph before the reference section containing this sentence: "The authors of this preprint declare that they have no financial conflict of interest with the content of this article." If appropriate, this disclosure may be completed by a sentence indicating that some of the authors are PCI recommenders: “XXX is one of the PCI XXX recommenders.”