Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation

Abstract

Many parasites modify their host behaviour to improve their own transmission and survival, but the proximate mechanisms remain poorly understood. An original model consists of the parasitoid Dinocampus coccinellae and its coccinellid host, Coleomegilla maculata; during the behaviour manipulation, the parasitoid is not in contact with its host anymore. We report herein the discovery and characterization of a new RNA virus of the parasitoid (D. coccinellae paralysis virus, DcPV). Using a combination of RT-qPCR and transmission electron microscopy, we demonstrate that DcPV is stored in the oviduct of parasitoid females, replicates in parasitoid larvae and is transmitted to the host during larval development. Next, DcPV replication in the host's nervous tissue induces a severe neuropathy and antiviral immune response that correlate with the paralytic symptoms characterizing the behaviour manipulation. Remarkably, virus clearance correlates with recovery of normal coccinellid behaviour. These results provide evidence that changes in ladybeetle behaviour most likely result from DcPV replication in the cerebral ganglia rather than by manipulation by the parasitoid. This offers stimulating prospects for research on parasitic manipulation by suggesting for the first time that behaviour manipulation could be symbiont-mediated.

Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

“…The virus (DcPV) may be responsible for the paralysis, as evidence suggests it causes lysis of glia cells and thus neuropathy of the cerebral ganglion. Crucially, the wasp injects DcPV with the eggs into the beetle (Dheilly et al, 2015). Here we can see the mutualistic relationship the wasp and DcPV share.…”

“…The only scenario that has empirical support for symbiont-mediated manipulation is the relationship between a macro-parasite and the viruses that use it as a vector. Essentially, the macroparasite harnesses the virus' manipulative abilities, while the virus uses the macro-parasites as delivery device (Dheilly et al, 2015). Let us look at the ladybeetle-wasp host-parasite system: the best and (currently) only empirically confirmed example of symbiont-mediated manipulation.…”

“…Note, however, that parasites can interact with the hosts' brain on a structural level as well, destroying areas of the brain (Lafferty and Shaw, 2013;Libersat and Gal, 2013), but in the interest of remaining cohesive the major focus here will be on micro-level manipulation via molecular mechanisms. Symbiont-mediated behavioral manipulation could also be another potential major pathway for parasite behavioral manipulation, but research on this phenomenon is still in its infancy currently (Dheilly et al, 2015).…”

The parasitic wasp Cotesia congregata uses multiple mechanisms to control host (Manduca sexta) behaviour

“…Other parasitic wasps have been shown to affect the central nervous systems of their hosts (e.g. Dheilly et al, 2015;Shi et al, 2015). Therefore, C. congregata wasps appear to use complex, multifactorial mechanisms to alter host behaviour ( Table 1).…”

Predators and parasitoids of the harlequin ladybird, Harmonia axyridis, in its native range and invaded areas

“…This virus, after transmission from the parasitoid larva to the host ladybird nervous system, replicates in the cerebral ganglia causing paralysis of the ladybird. This enables the emerging larva to spin a cocoon between the host's legs and consequently gain protection beneath the aposematically coloured and chemically defended host body (Dheilly et al 2015). The virus-induced paralysis is temporary and ladybirds can sometimes recover and even resume their reproductive activity (Triltsch 1996;Maure et al 2014).…”