ReviewParasitic manipulation: where are we and where should we go?
Section snippets
Adaptive versus non-adaptive changes: is the debate clear?
It is now accepted that phenotypic changes in infected hosts are not necessarily ‘true’ parasitic (or host) adaptations, they may be ‘by-products’ of infection or ancestral legacies. Although we agree with the evolutionary relevance of these distinctions, we believe that a discussion is needed, at least to recall the limitations of the definitions and of the methods originally chosen to decide whether a change is adaptive or not.
Adaptation is a complex concept with several possible definitions
How does the presence of a parasite alter host behaviour ?
Parasites can use both direct and indirect mechanisms to alter host behaviour. Parasites can alter host behaviour directly by interacting with the host's nervous system or muscle. For example, a parasite may secrete/excrete a neuroactive substance resulting in changes in host behaviour. Parasites can have indirect effects on host behaviour by affecting host tissues other than neurons and muscles, resulting in host-mediated changes in behaviour. For example, the presence of a parasite can
Mafia-like strategy of manipulation: an understudied hypothesis?
The complexity of the interactions between host and parasite suggest that we may not yet know all the ways in which parasites and hosts interact. For example, it has been recently suggested that parasites may select for collaborative behaviour in their host by imposing extra fitness costs in the absence of compliance. This interaction has been called a mafia-like strategy. This process was initially proposed as a possible explanation for why several bird species accept cuckoo eggs and nestlings
Considering manipulated hosts within ecosystems
Many studies of parasitic manipulation have been performed without considering the ecological context in which they occur. This is unfortunate, for it compromises both our understanding of the evolution of parasitic manipulation and our understanding of the ecological consequences of manipulation within ecosystems.
A full understanding of the evolution of parasitic manipulation requires knowledge of the selective pressures experienced by both the host and the parasite. Conditions used in
How complex are ‘parasitically modified organisms’?
A full understanding of the manipulation processes requires the study of other phenotypic traits in hosts in addition to the most obviously altered behaviours. Indeed, there are several reasons to think that we have until now only studied the visible part of the iceberg, manipulated hosts being probably more complex than traditionally viewed.
Studies on phenotypic plasticity and evolution have shown how a single phenotypic change (for instance induced by a minor genetic mutation) can result
Multiple parasites within manipulated hosts
Recently there has been a growing interest in studying the influence of manipulative parasitic species on the evolution of sympatric parasite species. Lafferty et al. (2000) have proposed a series of predictions about transmission strategies that should be favored by natural selection depending on the ecology of the co-occurring parasite species in the manipulated host. For instance, when manipulation is costly to achieve and when non-manipulative and manipulative parasites have shared
Determining the causes of intraspecific variation in manipulative processes
It is common to find substantial variation in the intensity of the phenotypic changes displayed by infected hosts, even when they are collected in the same environment and at the same time. As pointed out by Perrot-Minnot (2004), the analysis of the intraspecific variability in these patterns is nonetheless essential to an understanding of their evolution. When a character is variable for both genetic and environmental reasons, two individuals may differ because they differ in genotype, because
Concluding remarks
In the year 2000, Poulin published a paper entitled “Manipulation of host behaviour by parasites: a weakening paradigm?” (Poulin, 2000). Although some of Poulin's concerns are well justified, we find that on the whole, the study of manipulation is far from being weak. If anything, it is moving into a new era, characterized by challenging questions that demand interdisciplinary approaches. These little worms, tiny protozoa and viruses are on the brink of accomplishing what has eluded large
References (118)
Evidence for adaptive changes in egg-laying in crickets exposed to bacteria and parasites
Anim. Behav.
(1999)- et al.
Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species
Int. J. Parasitol.
(2000) - et al.
Usurpation of host behaviour by a parasitic wasp
Anim. Behav.
(1994) - et al.
Characterisation of global protein expression by two-dimensional electrophoresis and mass spectrometry: proteomics of Toxoplasma gondii
Int. J. Parasitol.
(2002) Parasite transmission in the intertidal zone: vertical migrations, infective stages and snail trails
J. Exp. Mar Biol. Ecol.
(1993)- et al.
Species associations among larval helminths in an amphipod intermediate host
Int. J. Parasitol.
(2000) - et al.
Induction of mosquito hemolymph proteins in response to immune challenge and wounding
Dev. Comp. Immunol.
(1999) - et al.
Metabolic and behavioural alterations in the crab Hemigrapsus crenulatus (Milne-Edwards 1837) induced by its acanthocephalan parasite Profilicollis antarcticus (Zdzitowiecki 1985)
J. Exp. Mar. Biol. Ecol.
(1998) - et al.
The neuropeptide schistosomin and haemolymph from parasitized snails induce similar changes in excitability in neuroendocrine cells controlling reproduction and growth in a freshwater snail
Neurosci. Lett.
(1992) - et al.
Parasites and behaviour: an ethopharmacological analysis and biomedical implications
Neurosc. Biobehav. Rev.
(1999)
Parasite manipulation of the proximate mechanisms that mediate social behaviour in vertebrates
Physiol. Behav.
The evolution of trophic transmission
Parasitol. Today
Ecological effects of larval trematode infestations on littoral invertebrate populations
Int. J. Parasitol.
Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare
Int. J. Parasitol.
Patterns of intermediate host use and levels of association between two conflicting manipulative parasites
Int. J. Parasitol.
Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala)
Int. J. Parasitol.
“Adaptive” change in the behaviour of parasitized animals: a critical review
Int. J. Parasitol.
Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict?
Int. J. Parasitol.
Phenotypic variability induced by parasites: extent and evolutionary implications
Parasitol. Today
Interspecific associations among larval helminthes in fish
Int. J. Parasitol.
Why should parasite resistance be costly?
Trends Parasitol.
Rabies re-examined
Lancet Infect. Dis.
Understanding parasite strategies: a state-dependent approach?
Trends Parasitol.
Modulating the modulators: parasites, neuromodulators and host behavioural change
Brain Behav. Evol.
How parasites alter the behaviour of their insect hosts
The specificity of behavioural fever in the cricket Acheta domesticus
J. Parasitol.
Age and size at maturity of the mosquito Culex pipiens infected by the microsporidian parasite Vavraia culicis
Proc. R. Soc. Lond. B
Infectious Diseases of Humans
Parasitism and Host Behaviour
Mild encephalitis underlying psychiatric disorder—a reconsideration and hypothesis exemplified on Borna disease
Neurol. Psychiatry Brain Res.
Fatal attraction in rats infected with Toxoplasma gondii
Proc. Roy. Soc. Lond. B
Altered evasive behaviour and responses to light in amphipods harboring acanthocephalan cystacanths
J. Parasitol.
Increased vulnerability of amphipods to predation owing to altered behaviour induced by larval acanthocephalans
Can. J. Zool.
Seasonal microhabitat selection by an endoparasitoid through adaptive modification of host behaviour
Science
Conflict between co-occuring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex
Parasitology
Ethological aspect of parasite transmission
Am. Nat.
Parasitism, The Ecology and Evolution of Intimate Interactions
Parasitism and the movements of intertidal gastropod individuals
Biol. Bull.
Vertical distribution of an estuarine snail altered by a parasite
Science
Sickness behaviour: a neuroimmune-based response to infectious disease
The Extended Phenotype
How schistosomes profit from the stress responses of their host
Adv. Parasitol.
Multiple strategies of schistosomes to meet their requirements in the intermediate smail host
Parasitology
Schistosome parasites induce physiological changes in their snail host by interfering with two regulatory systems, the internal defense system and the neuroendocrine system
Parasites flicking the NPY gene on the host's switchboard: why NPY?
FASEB
Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths
Parasitology
Immunosuppression in the definitive and intermediate hosts of the human parasite Schistosoma mansoni by release of immunoactive neuropeptides
Proc. Nat. Acad. Sci. U.S.A.
Spider manipulation by a wasp larva
Nature
Cited by (472)
Why do predators attack parasitized prey? Insights from a probabilistic model and a literature survey
2024, Behavioural ProcessesClockwork intruders: Do parasites manipulate their hostsʼ circadian rhythms?
2024, Current Research in Parasitology and Vector-Borne DiseasesThe impact of climate change and pollution on trematode-bivalve dynamics
2023, Marine Environmental Research