{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T22:03:02Z","timestamp":1792792982613,"version":"4.5.0"},"reference-count":48,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2019,10,29]],"date-time":"2019-10-29T00:00:00Z","timestamp":1572307200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Minist\u00e8re de l'Education Nationale, de l'Enseignement Superieur et de la Recherche","award":["ANR-09-BLAN-0243-01"],"award-info":[{"award-number":["ANR-09-BLAN-0243-01"]}]},{"DOI":"10.13039\/501100004792","name":"Minist\u00e8re de l'Enseignement Sup\u00e9rieur et de la Recherche","doi-asserted-by":"publisher","award":["ANR-11-LABX-0028"],"award-info":[{"award-number":["ANR-11-LABX-0028"]}],"id":[{"id":"10.13039\/501100004792","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100008935","name":"Universit\u00e9 Nice Sophia Antipolis","doi-asserted-by":"publisher","award":["Incentive Credits"],"award-info":[{"award-number":["Incentive Credits"]}],"id":[{"id":"10.13039\/501100008935","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006488","name":"Institut National de la Recherche Agronomique","doi-asserted-by":"publisher","award":["PhD Grant"],"award-info":[{"award-number":["PhD Grant"]}],"id":[{"id":"10.13039\/501100006488","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Toxins"],"abstract":"<jats:p>Parasitoid wasps rely primarily on venom to suppress the immune response and regulate the physiology of their host. Intraspecific variability of venom protein composition has been documented in some species, but its evolutionary potential is poorly understood. We performed an experimental evolution initiated with the crosses of two lines of Leptopilina boulardi of different venom composition to generate variability and create new combinations of venom factors. The offspring were maintained for 10 generations on two strains of Drosophila melanogaster differing in resistance\/susceptibility to the parental parasitoid lines. The venom composition of individuals was characterized by a semi-automatic analysis of 1D SDS-PAGE electrophoresis protein profiles whose accuracy was checked by Western blot analysis of well-characterized venom proteins. Results made evident a rapid and differential evolution of the venom composition on both hosts and showed that the proteins beneficial on one host can be costly on the other. Overall, we demonstrated the capacity of rapid evolution of the venom composition in parasitoid wasps, important regulators of arthropod populations, suggesting a potential for adaptation to new hosts. Our approach also proved relevant in identifying, among the diversity of venom proteins, those possibly involved in parasitism success and whose role deserves to be deepened.<\/jats:p>","DOI":"10.3390\/toxins11110629","type":"journal-article","created":{"date-parts":[[2019,10,31]],"date-time":"2019-10-31T05:18:26Z","timestamp":1572499106000},"page":"629","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":34,"title":["Rapid and Differential Evolution of the Venom Composition of a Parasitoid Wasp Depending on the Host Strain"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7764-4934","authenticated-orcid":false,"given":"Fanny","family":"Cavigliasso","sequence":"first","affiliation":[{"name":"Universit\u00e9 C\u00f4te d\u2019Azur, INRA, CNRS, ISA, 06 903 Sophia Antipolis, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4785-433X","authenticated-orcid":false,"given":"Hugo","family":"Math\u00e9-Hubert","sequence":"additional","affiliation":[{"name":"Universit\u00e9 C\u00f4te d\u2019Azur, INRA, CNRS, ISA, 06 903 Sophia Antipolis, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurent","family":"Kremmer","sequence":"additional","affiliation":[{"name":"Universit\u00e9 C\u00f4te d\u2019Azur, INRA, CNRS, ISA, 06 903 Sophia Antipolis, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Rebuf","sequence":"additional","affiliation":[{"name":"Universit\u00e9 C\u00f4te d\u2019Azur, INRA, CNRS, ISA, 06 903 Sophia Antipolis, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7683-718X","authenticated-orcid":false,"given":"Jean-Luc","family":"Gatti","sequence":"additional","affiliation":[{"name":"Universit\u00e9 C\u00f4te d\u2019Azur, INRA, CNRS, ISA, 06 903 Sophia Antipolis, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thibaut","family":"Malausa","sequence":"additional","affiliation":[{"name":"Universit\u00e9 C\u00f4te d\u2019Azur, INRA, CNRS, ISA, 06 903 Sophia Antipolis, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dominique","family":"Colinet","sequence":"additional","affiliation":[{"name":"Universit\u00e9 C\u00f4te d\u2019Azur, INRA, CNRS, ISA, 06 903 Sophia Antipolis, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3349-6925","authenticated-orcid":false,"given":"Maryl\u00e8ne","family":"Poiri\u00e9","sequence":"additional","affiliation":[{"name":"Universit\u00e9 C\u00f4te d\u2019Azur, INRA, CNRS, ISA, 06 903 Sophia Antipolis, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,10,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1038\/379537a0","article-title":"Diet and snake venom evolution","volume":"379","author":"Daltry","year":"1996","journal-title":"Nature"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2443","DOI":"10.1098\/rspb.2009.0048","article-title":"Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution","volume":"276","author":"Barlow","year":"2009","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Chang, D., Olenzek, A.M., and Duda, T.F. (2015). Effects of geographical heterogeneity in species interactions on the evolution of venom genes. Proc. R. Soc. B Biol. Sci., 282.","DOI":"10.1098\/rspb.2014.1984"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Zancolli, G., Calvete, J.J., Cardwell, M.D., Greene, H.W., Hayes, W.K., Hegarty, M.J., Herrmann, H.W., Holycross, A.T., Lannutti, D.I., and Mulley, J.F. (2019). When one phenotype is not enough: Divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species. Proc. R. Soc. B Biol. Sci., 286.","DOI":"10.1098\/rspb.2018.2735"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.cois.2014.10.004","article-title":"Insights into function and evolution of parasitoid wasp venoms","volume":"6","author":"Colinet","year":"2014","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1146\/annurev-ento-120709-144849","article-title":"Venom proteins from endoparasitoid wasps and their role in host-parasite interactions","volume":"56","author":"Asgari","year":"2011","journal-title":"Annu. Rev. Entomol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2385","DOI":"10.3390\/toxins7072385","article-title":"Venom proteins from parasitoid wasps and their biological functions","volume":"7","author":"Moreau","year":"2015","journal-title":"Toxins (Basel)"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1111\/een.12480","article-title":"Venom is beneficial but not essential for development and survival of Nasonia","volume":"43","author":"Martinson","year":"2018","journal-title":"Ecol. Entomol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1007\/s11306-014-0697-z","article-title":"Parasitoid venom induces metabolic cascades in fly hosts","volume":"11","author":"Mrinalini","year":"2015","journal-title":"Metabolomics"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1016\/j.ibmb.2013.03.010","article-title":"Extensive inter- and intraspecific venom variation in closely related parasites targeting the same host: The case of Leptopilina parasitoids of Drosophila","volume":"43","author":"Colinet","year":"2013","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.jinsphys.2012.10.013","article-title":"Variability of venom components in immune suppressive parasitoid wasps: From a phylogenetic to a population approach","volume":"59","author":"Colinet","year":"2013","journal-title":"J. Insect Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"35873","DOI":"10.1038\/srep35873","article-title":"Comparative venomics of Psyttalia lounsburyi and P. concolor, two olive fruit fly parasitoids: A hypothetical role for a GH1 \u03b2-glucosidase","volume":"6","author":"Colinet","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Colinet, D., Schmitz, A., Cazes, D., Gatti, J.L., and Poiri\u00e9, M. (2010). The origin of intraspecific variation of virulence in an eukaryotic immune suppressive parasite. PLoS Pathog., 6.","DOI":"10.1371\/journal.ppat.1001206"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.ibmb.2004.10.004","article-title":"A RhoGAP protein as a main immune suppressive factor in the Leptopilina boulardi (Hymenoptera, Figitidae)-Drosophila melanogaster interaction","volume":"35","author":"Labrosse","year":"2005","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.jinsphys.2004.10.004","article-title":"Haemocyte changes in D. melanogaster in response to long gland components of the parasitoid wasp Leptopilina boulardi: A Rho-GAP protein as an important factor","volume":"51","author":"Labrosse","year":"2005","journal-title":"J. Insect Physiol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Colinet, D., Schmitz, A., Depoix, D., Crochard, D., and Poiri\u00e9, M. (2007). Convergent use of RhoGAP toxins by eukaryotic parasites and bacterial pathogens. PLoS Pathog., 3.","DOI":"10.1371\/journal.ppat.0030203"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1688","DOI":"10.3389\/fimmu.2019.01688","article-title":"Venom atypical extracellular vesicles as interspecies vehicles of virulence factors involved in host specificity: The case of a Drosophila parasitoid wasp","volume":"10","author":"Wan","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1016\/j.dci.2008.11.013","article-title":"A serpin from the parasitoid wasp Leptopilina boulardi targets the Drosophila phenoloxidase cascade","volume":"33","author":"Colinet","year":"2009","journal-title":"Dev. Comp. Immunol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"156","DOI":"10.3389\/fevo.2019.00156","article-title":"Variation in the venom of parasitic wasps, drift, or selection? Insights from a multivariate QST analysis","volume":"7","author":"Kremmer","year":"2019","journal-title":"Front. Ecol. Evol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1038\/sj.hdy.6800182","article-title":"Genetic dimension of the coevolution of virulence-resistance in Drosophila\u2014Parasitoid wasp relationships","volume":"90","author":"Dupas","year":"2003","journal-title":"Heredity (Edinb.)"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/j.dci.2007.10.009","article-title":"Variation of success of Leptopilina boulardi in Drosophila yakuba: The mechanisms explored","volume":"32","author":"Dubuffet","year":"2008","journal-title":"Dev. Comp. Immunol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1038\/hdy.1992.141","article-title":"Genetic determinism of the cellular immune reaction in Drosophila melanogaster","volume":"69","author":"Carton","year":"1992","journal-title":"Heredity (Edinb.)"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1046\/j.1365-2540.1998.00303.x","article-title":"A new specific gene for wasp cellular immune resistance in Drosophila","volume":"80","author":"Benassi","year":"1998","journal-title":"Heredity (Edinb.)"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1098\/rspb.2000.1158","article-title":"Drosophila resistance genes to parasitoids: Chromosomal location and linkage analysis","volume":"267","author":"Frey","year":"2000","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1101\/gr.9.5.471","article-title":"Genetic localization of a Drosophila melanogaster resistance gene to a parasitoid wasp and physical mapping of the region","volume":"9","author":"Hita","year":"1999","journal-title":"Genome Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1017\/S001667230600841X","article-title":"Mapping candidate genes for Drosophila melanogaster resistance to the parasitoid wasp Leptopilina boulardi","volume":"88","author":"Hita","year":"2006","journal-title":"Genet. Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1120","DOI":"10.1111\/1755-0998.12389","article-title":"Statistical analysis of the individual variability of 1D protein profiles as a tool in ecology: An application to parasitoid venom","volume":"15","author":"Gatti","year":"2015","journal-title":"Mol. Ecol. Resour."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"879","DOI":"10.2135\/cropsci1997.0011183X003700030030x","article-title":"Path analyses identify indirect selection criteria for yield of late-planted soybean","volume":"37","author":"Board","year":"1997","journal-title":"Crop Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/S0022-1910(00)00102-5","article-title":"Haemocyte changes in resistant and susceptible strains of D. melanogaster caused by virulent and avirulent strains of the parasitic wasp Leptopilina boulardi","volume":"47","author":"Russo","year":"2001","journal-title":"J. Insect Physiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1038\/sj.hdy.6800893","article-title":"Genetic interactions between the parasitoid wasp Leptopilina boulardi and its Drosophila hosts","volume":"98","author":"Dubuffet","year":"2007","journal-title":"Heredity (Edinb.)"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1111\/j.1600-0587.1999.tb00504.x","article-title":"Geographic variation and evolution of immunosuppressive genes in a Drosophila parasitoid","volume":"22","author":"Dupas","year":"1999","journal-title":"Ecography (Cop.)"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1080\/00379271.2013.815045","article-title":"Is parasitoid virulence against multiple hosts adaptive or constrained by phylogeny? A study of Leptopilina spp.(Hymenoptera: Figitidae)\/Drosophila (Diptera: Drosophilidae) interactions","volume":"49","author":"Dupas","year":"2013","journal-title":"Ann. Soc. Entomol. Fr."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.toxicon.2012.11.022","article-title":"The venom optimization hypothesis revisited","volume":"63","author":"King","year":"2013","journal-title":"Toxicon"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2015","DOI":"10.1242\/jcs.02920","article-title":"Rac1 signalling in the Drosophila larval cellular immune response","volume":"119","author":"Williams","year":"2006","journal-title":"J. Cell Sci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1111\/j.1365-2443.2005.00883.x","article-title":"Drosophila melanogaster Rac2 is necessary for a proper cellular immune response","volume":"10","author":"Williams","year":"2005","journal-title":"Genes to Cells"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2007","DOI":"10.1016\/j.cub.2017.05.032","article-title":"The evolution of venom by co-option of single-copy genes","volume":"27","author":"Martinson","year":"2017","journal-title":"Curr. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2599","DOI":"10.1111\/evo.13333","article-title":"Parasitoid gene expression changes after adaptation to symbiont-protected hosts","volume":"71","author":"Dennis","year":"2017","journal-title":"Evolution"},{"key":"ref_38","unstructured":"Cavigliasso, F., Math\u00e9-hubert, H., Gatti, J., Colinet, D., and Poiri\u00e9, M. Experimental evolution of parasitism success and venom composition of the parasitoid wasp Leptopilina boulardi on different Drosophila host species, Manuscript in preparation."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1093\/jhered\/89.4.306","article-title":"A single parasitoid segregating factor controls immune suppression in Drosophila","volume":"89","author":"Dupas","year":"1998","journal-title":"J. Hered."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1016\/S0169-4758(97)01058-2","article-title":"Drosophila cellular immunity against parasitoids","volume":"13","author":"Carton","year":"1997","journal-title":"Parasitol. Today"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Futuyma, D.J., and Bennett, A.F. (2009). The importance of experimental studies in evolutionary biology. Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments, University of California Press.","DOI":"10.1525\/california\/9780520247666.003.0002"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/0003-2697(81)90783-1","article-title":"Silver stain for proteins in polyacrylamide gels: A modified procedure with enhanced uniform sensitivity","volume":"117","author":"Morrissey","year":"1981","journal-title":"Anal. Biochem."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"4350","DOI":"10.1073\/pnas.76.9.4350","article-title":"Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications","volume":"76","author":"Towbin","year":"1979","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.jinsphys.2014.02.011","article-title":"Development of RNAi in a Drosophila endoparasitoid wasp and demonstration of its efficiency in impairing venom protein production","volume":"63","author":"Colinet","year":"2014","journal-title":"J. Insect Physiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1111\/j.1654-1103.2003.tb02228.x","article-title":"VEGAN, a package of R functions for community ecology","volume":"14","author":"Dixon","year":"2003","journal-title":"J. Veg. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1408","DOI":"10.1093\/bioinformatics\/btn179","article-title":"Forward-time simulations of non-random mating populations using simuPOP","volume":"24","author":"Peng","year":"2008","journal-title":"Bioinformatics"},{"key":"ref_47","unstructured":"Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., and The R Core Team (2011). nlme: Linear and nonlinear mixed effects models. R Packag. Vers."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1002\/bimj.200810425","article-title":"Simultaneous inference in general parametric models","volume":"50","author":"Hothorn","year":"2008","journal-title":"Biometrical J."}],"container-title":["Toxins"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6651\/11\/11\/629\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:30:20Z","timestamp":1760189420000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6651\/11\/11\/629"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,29]]},"references-count":48,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2019,11]]}},"alternative-id":["toxins11110629"],"URL":"https:\/\/doi.org\/10.3390\/toxins11110629","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/796649","asserted-by":"object"}]},"ISSN":["2072-6651"],"issn-type":[{"value":"2072-6651","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,29]]}}}