Influence of the Virus LbFV and of Wolbachia in a Host-Parasitoid Interaction

Symbionts are widespread and might have a substantial effect on the outcome of interactions between species, such as in host-parasitoid systems. Here, we studied the effects of symbionts on the outcome of host-parasitoid interactions in a four-partner system, consisting of the parasitoid wasp Leptopilina boulardi, its two hosts Drosophila melanogaster and D. simulans, the wasp virus LbFV, and the endosymbiotic bacterium Wolbachia. The virus is known to manipulate the superparasitism behavior of the parasitoid whereas some Wolbachia strains can reproductively manipulate and/or confer pathogen protection to Drosophila hosts. We used two nuclear backgrounds for both Drosophila species, infected with or cured of their respective Wolbachia strains, and offered them to L. boulardi of one nuclear background, either infected or uninfected by the virus. The main defence mechanism against parasitoids, i.e. encapsulation, and other important traits of the interaction were measured. The results showed that virus-infected parasitoids are less frequently encapsulated than uninfected ones. Further experiments showed that this viral effect involved both a direct protective effect against encapsulation and an indirect effect of superparasitism. Additionally, the Wolbachia strain wAu affected the encapsulation ability of its Drosophila host but the direction of this effect was strongly dependent on the presence/absence of LbFV. Our results confirmed the importance of heritable symbionts in the outcome of antagonistic interactions.Peer reviewe

Deciphering the behaviour manipulation imposed by a virus on its parasitoid host: insights from a dual transcriptomic approach

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Heritable variation in an extended phenotype: the case of a parasitoid manipulated by a virus.

International audienceIn host-symbiont interactions, the genes of both host and symbiont can influence phenotypic traits. In the context of a conflict of interest, fitness-related traits are subjected to opposing selective pressures in the genomes of the partners. In the Drosophila parasitoid Leptopilina boulardi, females usually avoid laying eggs into already parasitized larvae. However, when infected by the virus LbFV, they readily lay additional eggs into parasitized larvae. Inducing superparasitism allows the virus to colonize uninfected parasitoid lineages but is usually maladaptive for the parasitoid. We tested for the presence of resistance genes to this behavioural manipulation in the parasitoid genotype by sampling 30 lines from five populations with contrasting viral prevalence, after infecting them with a reference viral isolate. No geographical differentiation was observed although some genotypes underwent less manipulation than others, and these differences were heritable across generations. The viral titre was not correlated with these differences although fecundity differed between extreme lines

Virus manipulateurs du comportement des insectes (prévalence et influence sur la structure des communautés hôtes)

Les symbioses eucaryotes/micro-organismes constituent une importante source d innovation évolutive et de diversité écologique. Ces associations sont très répandues chez les insectes, en particulier chez les insectes parasitoïdes (insectes parasites d autres insectes) qui hébergent en particulier une grande diversité de virus transmis verticalement. Leurs effets directs sur les parasitoïdes ainsi que les effets indirects sur la structure des communautés sont à l heure actuelle mal compris. Nous avons abordé ces questions au travers l étude d un virus héritable (LbFV) ayant la particularité de manipuler le comportement de superparasitisme de son hôte, l hyménoptère parasitoïde de drosophiles Leptopilina boulardi. La mise au point d un outil moléculaire diagnostic de l infection nous a permis de montrer que ce virus, spécifique à L. boulardi, peut atteindre de fortes prévalences dans les populations d hôtes. Nous avons également mis en évidence un effet de la présence du virus sur les interactions compétitives interspécifiques au sein de la communauté des parasitoïdes de drosophiles. L approche intégrée de ce travail constitue une étape importante dans la connaissance du rôle des virus héritables sur l écologie et l évolution de leurs hôtesEukaryots/microorganisms symbiosis is an important source of evolutionary novelty and ecological diversification. These associations are widespread in insects, particularly in parasitoids (insects that parasitize other insects) where a broad diversity of vertically transmitted viruses are found. However, their direct and indirect effects on host community are poorly understood. In this thesis, we used a system involving a Drosophila parasitoid, Leptopilina boulardi and a heritable virus LbFV that manipulates the behaviour of the parasitoid by increasing its tendency to lay eggs in a host that is already parasitized (superparasitism). Using a viral molecular marker developed in this work, we showed very high prevalences of the virus in L. boulardi populations. Additionally, we found a strong effect of the virus on interspecific competition in the Drosophila parasitoid community. The integrative approach of this work is an important step in understanding the role of heritable viruses in parasitoid ecology and evolutionLYON1-BU.Sciences (692662101) / SudocSudocFranceF

introgression

Table of superparasitism measurements in parasitoid females from the different generation of introgression. The first row correspond to designation of the different variables. "generation" indicates the generation of introgression. "Population" stands for the population of origin of the introgressed genotypes. "Line" is the name of the different introgressed genotypes. "female" gives the number of each tested female. "l1-l3" stands for the three dissected Drosophila larvae per parasitoid female. "Parasitism" is the mean number of parasitoid eggs per Drosophila larvae. "superparasitism" is the mean number of parasitoid eggs per parasitized drosophila larvae

PCRQBC2

Table of the viral titer in the four extreme lines Av3, Av8, Go16 and Sf12 at generation BC2. The first row corresponds to designations of the different variables. "line" is the name of the extreme lines. "virus" indicates the gene copy number for the viral molecular marker. "insect" indicates the gene copy number for the insect molecular marker. "ratio" indicates the ratio between the viral and the insect gene copy numbers

expGQ

Table of superparasitism measurements in parasitoid females from the crossing experiment between “extreme” lines. The first row corresponds to designations of the different variables. "line" is the name of the different cross combinations. "mother" indicates the mother of tested females in each cross combination. "female" gives the number of each tested female. "l1-l3" stands for the three dissected Drosophila larvae per parasitoid female. "superparasitism" is the mean number of parasitoid eggs per parasitized drosophila larvae

Superparasitism evolution: adaptation or manipulation?

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