Parasites often induce behavioural changes in their host. However, it is not necessarily easy to determine whether these changes are representative of an adaptation of the parasite (parasite manipulation), an adaptive response of the host or a side-effect of infection. In a solitary parasitoid of Drosophila larvae (Leptopilina boulardi), viral particles (LbFV) modify the host acceptance behaviour of infected females by increasing their tendency to superparasitize. This behavioural alteration allows for the horizontal transmission of the virus within superparasitized Drosophila larvae. To add support for or against the ‘manipulation hypothesis’, we investigated whether other behavioural components of the parasitoid are affected by viral infection, and whether other forms of horizontal transmission exist. Neither the ability of females to locate host kairomones nor their daily rhythm of locomotor activity was affected by viral infection. However, infected females showed a lower rate of locomotor activity, suggesting a physiological cost of infection. The searching paths of females were also unaffected. Males from infected and uninfected lines showed the same ability to locate females'sexual pheromones. Moreover, alternative modes of horizontal transmission (through food consumption and/or contact with the same Drosophila larvae) did not lead to viral contamination of the parasitoid. The overall specificity of behavioural alteration and of viral horizontal transmission is consistent with the hypothesis that the virus manipulates the behaviour of the parasitoid.

Vertically transmitted symbionts can be maintained in a host population only if they do not reduce host fitness, unless they compensate by manipulation of their host's reproduction or have alternative mode of transmission. In Leptopilina boulardi, a parasitoid of Drosophila larvae, some females are infected by viral particles showing both maternal and horizontal transmission. Horizontal transmission occurs when larvae from infected and uninfected individuals of L. boulardi compete in the same host. This situation is facilitated by the increasing tendency to accept already parasitized hosts that viral infection induces in L. boulardi females. Estimation of the adaptive significance of this behavioural modification requires measuring the effect of viral presence on other parasitoid physiological features. Here, we show that viral infection in females imposes no cost on adult survival, a low cost on developmental rate and tibia length, and leads to a strong reduction of locomotor activity. Surprisingly, infected females show higher egg load which could be accounted for by a redirection of energy allocation to egg production. The high intensity of superparasitism in infected females induced a dramatic decrease in pre-imaginal survival of the parasitoid's offspring, representing a potential indirect cost of infection. Low overall pathogeny induced by viral particles appears to be well suited to both transmission modes, both of them requiring females ability to locate and (super)parasitize hosts.