Inequalities in body size among mermithid nematodes parasitizing earwigs.

Variation among body sizes of adult parasitic worms determines the relative genetic contribution of individuals to the next generation as it affects the effective parasite population size. Here, we investigate inequalities in body size and how they are affected by intensity of infection in Mermis nigrescens (Mermithidae: Nematoda) parasitizing the European earwig Forficula auricularia in New Zealand. Among a population of pre-adult worms prior to their emergence from the host, we observed only modest inequalities in body length; however, among worms sharing the same individual host, inequalities in body sizes decreased with increasing intensity of infection. Thus, the more worms occurred in a host, the more the second-longest, third-longest and even fourth-longest worms approached the longest worm in body length. This pattern, also known from another mermithid species, suggests that worms sharing the same host may have infected it roughly simultaneously, when the host encountered a clump of eggs in the environment. Thus, the life history and mode of infection of the parasite may explain the modest inequalities in the sizes achieved by pre-adult worms, which are lower than those reported for endoparasitic helminths of vertebrates.

Host Manipulation by Parasites: A Look Back Before Moving Forward.

The ability to manipulate host behaviour is among the most fascinating and best-studied adaptations of parasites. In this opinion article, we highlight trends and biases in the study of this phenomenon that may cloud or limit our understanding of its evolution. For instance, reviews and theoretical studies have shown a disproportionately sharp increase in the past decade relative to empirical studies. We also discuss taxonomic biases in the host-parasite systems investigated, as well as recent declines in the use of experimental infections and in the proportion of these systems in which fitness benefits for the parasites have been confirmed. We finish this opinion article by offering recommendations for the continued success of research in this area.

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

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.

Bodyguard manipulation in a multipredator context: different processes, same effect.

Parasites have evolved various strategies to exploit hosts to their own advantage. Bodyguard manipulations consist of usurping the behaviour of the host to confer some protection to the parasite and/or its offspring. Dinocampus coccinellae Schrank is a solitary endoparasitoid of the spotted lady beetle Coleomegilla maculata lengi Timberlake. The parasitoid larva grows inside the host until mature, then egresses and spins a cocoon between the ladybird's legs. Unlike most parasitoids, D. coccinellae does not kill its host during development, but keeps the coccinellid partially paralysed on top of the cocoon, where it acts as a bodyguard against natural enemies. As recently shown, the presence of a living ladybird on the parasitoid cocoon provides efficient protection against a predator, lacewing larvae. In the present study, we used predators with different foraging behaviours--jumping spiders and crickets--to explore the relevance of the bodyguard strategy for D. coccinellae in a multipredator context. Although the manner of the protection differs among the different tested predators, the presence of the ladybird always enhances parasitoid survival, even when it first increases detection of the cocoon-ladybird complex, as is the case with jumping spiders. Furthermore, although a dead bodyguard is sufficient to passively defend parasitoid cocoons against crickets, it provides only partial protection against jumping spiders. Altogether, these results support the bodyguard hypothesis in a multipredator context, since the presence of a living coccinellid significantly reduces cocoon predation by predators having different prey specificities, morphologies, and hunting behaviours.

Diversity and evolution of bodyguard manipulation.

Among the different strategies used by parasites to usurp the behaviour of their host, one of the most fascinating is bodyguard manipulation. While all classic examples of bodyguard manipulation involve insect parasitoids, induced protective behaviours have also evolved in other parasite-host systems, typically as specific dimensions of the total manipulation. For instance, parasites may manipulate the host to reduce host mortality during their development or to avoid predation by non-host predators. This type of host manipulation behaviour is rarely described, probably due to the fact that studies have mainly focused on predation enhancement rather than studying all the dimensions of the manipulation. Here, in addition to the classic cases of bodyguard manipulation, we also review these 'bodyguard dimensions' and propose extending the current definition of bodyguard manipulation to include the latter. We also discuss different evolutionary scenarios under which such manipulations could have evolved.

How much energy should manipulative parasites leave to their hosts to ensure altered behaviours?

Although host manipulation is likely to be costly for parasites, we still have a poor understanding of the energetic aspects underlying this strategy. It is traditionally assumed that physiological costs are inevitably associated with mechanisms evolved by parasites to induce the required changes in host behaviours. While most energetic expenditures of parasites relate primarily to bringing about the altered behaviours, manipulative parasites also have to consider the condition of their host during the manipulation. Here, we suggest that because of this trade-off, the energy required to accomplish parasite-induced behaviours may represent a key energetic constraint for parasites. Depending on the energetic expenditures specific to each type of manipulation, parasites should undergo selection to secure resources for their host to allow them to perform manipulated behaviours.

The cost of a bodyguard.

Host manipulation by parasites not only captures the imagination but has important epidemiological implications. The conventional view is that parasites face a trade-off between the benefits of host manipulation and their costs to fitness-related traits, such as longevity and fecundity. However, this trade-off hypothesis remains to be tested. Dinocampus coccinellae is a common parasitic wasp of the spotted lady beetle Coleomegilla maculata. Females deposit a single egg in the haemocoel of the host, and during larval development the parasitoid feeds on host tissues. At the prepupal stage, the parasitoid egresses from its host by forcing its way through the coccinellid's abdominal segments and begins spinning a cocoon between the ladybird's legs. Remarkably, D. coccinellae does not kill its host during its development, an atypical feature for parasitoids. We first showed under laboratory conditions that parasitoid cocoons that were attended by a living and manipulated ladybird suffered less predation than did cocoons alone or cocoons under dead ladybirds. We then demonstrated that the length of the manipulation period is negatively correlated with parasitoid fecundity but not with longevity. In addition to documenting an original case of bodyguard manipulation, our study provides the first evidence of a cost required for manipulating host behaviour.

Intraspecific variability in host manipulation by parasites.

Manipulative parasites have the capacity to alter a broad range of phenotypic traits in their hosts, extending from colour, morphology and behaviour. While significant attention has been devoted to describing the diversity of host manipulation among parasite clades, and testing the adaptive value of phenotypic traits that can be manipulated, there is increasing evidence that variation exists in the frequency and intensity of the changes displayed by parasitized individuals within single host-manipulative parasite systems. Such variability occurs within individuals, between individuals of a same population, and across populations. Here we review the non-genetic (i.e. environmental) and genetic causes of variability in host behaviour manipulation, discuss its evolutionary significance, and propose directions for further researches.

Experimental evidence of size/age-biased infection of Biomphalaria glabrata (Pulmonata: Planorbidae) by an incompatible parasite species: consequences for biological control.

Because the digenetic trematode Plagiorchis elegans can elicit a rapid, severe and permanent suppression of the reproductive output in the snail Biomphalaria glabrata, it is considered as a potential biological control agent of human schistosomiasis. This assumption however is derived from laboratory experiments that are poor approximations of what occurs in a natural ecosystem. In order to recreate conditions that resemble those found in nature, we exposed B. glabrata as individual populations composed of a young, juvenile and adult snails to various concentrations of P. elegans eggs to assess the probability of encountering the parasite eggs by the different snail sizes/age groups. We demonstrated that within populations composed of different size/age classes, larger/older snails displayed the negative effects typical of exposure to P. elegans, whereas smaller individuals appeared relatively unaffected, particularly at lower levels of exposure. These findings coupled with the difficulty of producing large quantities of parasite eggs suggest that P. elegans has limited efficiency as a biological control agent of human schistosomiasis.