Prevalence of a virus inducing behavioural manipulation near species range border

Abstract

The densities of conspecific individuals may vary through space, especially at the edge of species range. This variation in density is predicted to influence the diffusion of species-specific horizontally transmitted symbionts. However, to date there is very little data on how parasite prevalence varies around the border of a host species. Using a molecular epidemiology approach, we studied the prevalence of a vertically and horizontally transmitted virus at the edge of the geographic range of its insect host, the Drosophila parasitoid wasp Leptopilina boulardi. L. boulardi is a Mediterranean parasitoid species showing a recent range expansion to the north (in France). The LbFV virus manipulates the behaviour of females, increasing their tendency to lay additional eggs in already parasitized Drosophila larvae (superparasitism). This is beneficial for the virus because it allows the virus to be horizontally transferred during superparasitism. We show that LbFV prevalence is very high in central populations, intermediate in marginal populations and almost absent from newly established peripheral populations of L. boulardi. We failed to detect any influence of temperature and diapause on viral transmission efficiency but we observed a clear relationship between prevalence and parasitoid density, and between parasitoid density and the occurrence of superparasitism, as predicted by our epidemiological model. Viral strains were all efficient at inducing the behavioural manipulation and viral gene sequencing revealed very low sequence variation. We conclude that the prevalence reached by the virus critically depends on density-dependent factors, i.e. superparasitism, underlying the selective pressures acting on the virus to manipulate the behaviour of the parasitoid.

Seasonal and regional presence of hymenopteran parasitoids of Drosophila in Switzerland and their ability to parasitize the invasive Drosophila suzukii

“…), however, it was not retrieved from any of the samples from northern Switzerland. Like Central France, Switzerland seems to be at the northern geographic limit of L. boulardi , a species native to the Mediterranean region that is currently expanding its distribution range northwards30. Previous studies have shown that developmental success of L. heterotoma is reduced in the presence of L. boulardi , but not vice versa and in cage experiments L. boulardi outcompeted L. heterotoma 31.…”

Genome Sequencing of the Behavior Manipulating Virus LbFV Reveals a Possible New Virus Family

“…Accordingly, by a theoretical approach, we showed that the virus is always selected to increase the natural tendency of the wasp to superparasitize, which indicates a conflict of interest on this trait, and shows that this is a case of behavior manipulation (Gandon et al 2006). In addition to horizontal transmission under superparasitism, the virus is vertically transmitted (from mother to offspring) with very high efficiency and reaches high prevalence (∼95%) in some natural populations (Patot et al 2010). The effect of the virus is mostly restricted to superparasitism.…”

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

“…The parasitoid L. boulardi is often infected by a maternally-transmitted DNA virus called LbFV ( Leptopilina boulardi Filamentous Virus), whose prevalence may exceed 90% in some locations [33]. This virus manipulates the behavior of adult females in a way that favours its own transmission [34].…”