Dataset Information

Convergent origin and accelerated evolution of vesicle-associated RhoGAP proteins in two unrelated parasitoid wasps

ABSTRACT: Gene duplication, accompanied by modification of the expression and/or function of one of the duplicates under the action of positive selection, followed by further duplication to produce multigene families of toxins is a well-documented process in venomous animals. This evolutionary model has been less described in parasitoid wasps, which use maternal fluids, including venom, to protect their eggs from encapsulation by the host immune system. The leptopilina venom proteomic data were used to evidence that specific RhoGAPs formed a family of protein that are associated with vesicles that act as transport systems to deliver them in the immune cells of their drosophila larval host. We showed that the gene encoding the cellular RacGAP1 is at the origin of the virulent RhoGAP family formed by successive duplications that evolved under positive selection. Almost all of these RhoGAPs lost their GAP activity and GTPase binding ability due to mutations in key amino acids suggesting new function(s) and mechanism of action in host cells that remain to be elucidated.

INSTRUMENT(S): Q-Tof Ultima

ORGANISM(S): Leptopilina Boulardi Leptopilina Heterotoma

TISSUE(S): Venom Sac

SUBMITTER: Maya BELGHAZI

LAB HEAD: Jean Luc gatti

PROVIDER: PXD041695 | Pride | 2023-06-09

REPOSITORIES: Pride

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Publications

Extensive inter- and intraspecific venom variation in closely related parasites targeting the same host: the case of Leptopilina parasitoids of Drosophila.

Colinet Dominique D Deleury Emeline E Anselme Caroline C Cazes Dominique D Poulain Julie J Azema-Dossat Carole C Belghazi Maya M Gatti Jean-Luc JL Poirié Marylène M

Insect biochemistry and molecular biology 20130402 7

The arms race between immune suppressive parasites that produce virulence factors and hosts that evolve resistance to these factors is suggested to be a key driver for the diversification of both partners. However, little is known regarding the diversity of virulence factors in closely related parasites or the mechanisms underlying the variation of virulence. One of the best-described model to address this issue is the interaction between Leptopilina parasitic wasps and their Drosophila hosts, i ...[more]

PMID: 23557852

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Project description:The venom apparatus is a conserved organ in parasitoid wasps that shows adaptations correlated with life-style diversification. Recent venom analyses from selected species reveal considerable complexity and high diversity in venom composition existing not only between closely related species but even between strains and individuals, which may partly determine the potential for parasitoid adaptation. However, the investigations have paid little attention to secondary venom components that also have significant functions in parasitism, and the data in regard to full and accurate quantity of venom compositions at the protein level is not available. Using a combination of transcriptomic and label-free quantitative proteomic, we here explored the venom components of the endoparasitoid Tetrastichus brontispae (Eulophidae), a species devoid of polydnavirus, and provided an in-depth comparison of the venom proteomes between its two closely related strains, Tb-On and Tb-Bl. Results showed that approximately 1505 venom proteins were identified in the venom apparatus of T. brontispae, consistent with the classical venom protein characteristics, including enzymes, protease inhibitors, binding proteins and some immune related proteins. The venom extracts also contained novel venom proteins, such as kynurenine-oxoglutarate transaminase, 4-coumarate CoA ligase and venom protein r-like protein. Comparative venom proteomes revealed that significant quantitative and qualitative changes in venom composition occurred when Tb-Bl strain, with an invasive beetle Brontispae longissima pupa as its habitual host, was exposed to another invasive beetle Octodonta nipae pupa as host consecutively for two years; although the most abundant venom proteins were shared between them. These significantly differentially expressed proteins were mainly enriched in fatty acid biosynthesis and melanotic encapsulation response by enrichment analyses. Furthermore, most of the significantly enriched proteins presented strikingly increased levels or were exclusively identified in the Tb-On strain. These combined results indicated that virulence factors in Tb-On strain might be linked to lipid metabolism or more venom is required to inhibit O. nipae pupa’s melanotic encapsulation upon its parasitism. Altogether, our data reveal that venom composition can quickly evolve and respond to host selection, mainly through rapid changes in regulation of protein abundance and/or the emergence of multigenic families by gene duplication. Our data additionally provide invaluable data for further functional analysis of parasitoid venoms.

Project description:Background: Eusociality is widely considered to evolve through kin selection, where the reproductive success of an individual’s close relative is favored at the expense of its own. High genetic relatedness is thus considered a prerequisite for eusociality. While ants are textbook examples of eusocial animals, not all ants form colonies of closely related individuals. One such example is the ectatommine ant Rhytidoponera metallica, which predominantly forms predominantly queen-less colonies that have such a low intra-colony relatedness that they have been proposed to represent a transient, unstable form of eusociality. However, R. metallica is among the most abundant and widespread ants on the Australian continent. This apparent contrast provides an example of how inclusive fitness may not by itself explain the maintenance of eusociality and raises the question of what other selective advantages maintain their eusocial lifestyle. Results: We provide a comprehensive portrait of the venom of R. metallica and show that the colony-wide venom consists of a, for an ant, exceptionally high diversity of functionally distinct toxins. These toxins have evolved under strong positive selection, which is normally expected to reduce genetic variance. Yet, R. metallica exhibits remarkable intra-colony variation, with workers sharing only a relatively small proportion of toxins in their venoms. We also find that this variation is not due to the presence of chemical castes, but that it has a genetic foundation that is at least in part explained by toxin allelic diversity. Conclusions: Taken together, our results suggest that the toxin diversity contained in R. metallica colonies may be maintained by a form of group selection, which selects for colonies that can exploit more resources and defend against a wider range of predators. We propose that increased intra-colony genetic variance resulting from low kinship may itself provide a selective advantage in the form of an expanded pharmacological venom repertoire. These findings provide an example of how group selection on adaptive phenotypes may contribute to maintaining eusociality where a prerequisite for kin selection is diminished.

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