Rapid and differential evolution of the venom composition of a parasitoid wasp depending on the host strain

Abstract

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 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 parasitoid lines. The venom composition of individuals was characterized by a semi-automatic analysis of 1D SDS-PAGE protein profiles whose accuracy was checked by Western blot analysis of wellcharacterized venom proteins. Results evidenced 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. Key Contribution:The venom protein composition of parasitoid wasps can evolve rapidly and differently depending on the host strain. Studying this evolution can help identify new venom proteins possibly involved in parasitism success on a given host.

Quantitative trait loci involved in the reproductive success of a parasitoid wasp

“…In all QTLs, except in the QTL3‐PS, we found genes associated with venom components, whose role in host adaptation was widely studied (Cavigliasso et al., 2019). In polydnavirus‐associated parasitoids, polydnavirus is considered as the main virulence factor.…”

Prior adaptation of parasitoids improves biological control of symbiont‐protected pests

“…Possible reasons include temporally variable selection in the face of trade‐offs with resistance, weak selection as a consequence of spatial structuring, and importantly, coevolutionary dynamics (Holt & Hochberg, 1997). Parasitoids and predators exhibit genetic variation as well and are thus able to evolve counter‐resistance (Cavigliasso et al, 2019; Kraaijeveld, Hutcheson, Limentani, & Godfray, 2001), highlighting the opportunity for genetic improvement of biocontrol agents (Kruitwagen, Beukeboom, & Wertheim, 2018; Lommen, de Jong, & Pannebakker, 2017). Nevertheless, biological control is not immune to resistance evolution, as shown, for example, by the increasing resistance of Argentine stem weevils to the introduced parasitoid Microctonus hyperodae in New Zealand (Tomasetto, Tylianakis, Reale, Wratten, & Goldson, 2017).…”

A chromosome‐level genome assembly of the parasitoid wasp Pteromalus puparum

“…(2016). To adapt to different hosts, parasitoid wasp venom compositions turnover and evolve quickly, making parasitoid wasp venom an excellent system for studying gene function evolution (Cavigliasso et al., 2019; Colinet et al., 2013; Goecks et al., 2013; Martinson et al, 2017). In contrast to the classic duplication and neofunctionalization model of venom evolution described in some venomous animals, such as snakes (Wong & Belov, 2012), the mechanism of new venom gene evolution in parasitoids often involves single‐copy genes acquiring a venom function, either by ‘moonlighting’ (i.e., when a protein evolves to perform more than one function) (Jeffery, 1999) or by co‐option (i.e., shifting to a new function), through rapid cis ‐regulatory expression evolution (Martinson et al, 2017).…”