Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-17T14:08:31.627Z Has data issue: false hasContentIssue false
  • English
  • Français

The evolution of parasite manipulation of host behaviour: a theoretical analysis

Published online by Cambridge University Press:  16 March 2011

R. Poulin
R. Poulin
Affiliation:
Department of Zoology, University of Otago, P. O. Box 56, Dunedin, New Zealand.
Get access Rights & Permissions [Opens in a new window]

Summary

Parasite-induced modifications of host behaviour are known from a wide range of host-parasite associations. In many cases, these behavioural changes are thought to be adaptive and. benefit the parasite by increasing its probability of successful transmission. However, in many cases, energy spent on host manipulation will not be available for other functions, such as growth. These trade-offs suggest that in the absence of other constraints, natural selection will optimize, and not maximize, the influence of parasites on host behaviour. This argument is developed and expanded into theoretical considerations of the evolution of host behaviour manipulation by parasites. Among populations of the same parasite species or among closely-related species, the optimal investment into manipulation, or optimal manipulative effort (ME*), of individual parasites is predicted to increase as (1) typical infrapopulation size decreases, (2) prevalence increases, (3) the longevity of the infected host, or of the parasite in its host, decreases, (4) passive transmission rates decrease, and (5) parasite fecundity decreases. This evolutionary analysis indicates that ecological and life history variables may have played an important role in the evolution of manipulation of host behaviour by parasites.

Keywords

Parasitismmanipulationhost behaviourtrade-offsinfrapopulationtransmission success.
Type
Research Article
Information
Parasitology , Volume 109 , supplement S1: Parasites and behaviour , 1994 , pp. S109 - S118
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Baudoin, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335–52.CrossRefGoogle ScholarPubMed
Baylis, H. A. (1943). Notes on the distribution of hairworms (Nematomorpha: Gordiidae) in the British Isles. Proceedings of the Zoological Society of London (Series B) 113, 193–7.Google Scholar
Bethel, W. M. & Holmes, J. C. (1974). Correlation of development of altered evasive behaviour in Gammarus lacustris (Amphipoda) harboring cystacanths of Polymorphus paradoxus (Acanthocephala) with infectivity to the definitive host. Journal of Parasitology 60, 272–4.CrossRefGoogle Scholar
Croll, N. A. (1966). Ecology of Parasites. Cambridge, Mass: Harvard University Press.Google Scholar
Curtis, L. A. (1987). Vertical distribution of an estuarine snail altered by a parasite. Science 235, 1509–11.Google ScholarPubMed
Dawkins, R. (1990). Parasites, desiderata lists and the paradox of the organism. Parasitology 100 (Suppl.), S63–S73.CrossRefGoogle ScholarPubMed
Dobson, A. P. (1988). The population biology of parasiteinduced changes in host behaviour. Quarterly Review of Biology 63, 139–65.CrossRefGoogle Scholar
Dobson, A. P. & Keymer, A. E. (1985). Life history models. In Biology of the Acanthocephala (ed. Crompton, D. W. T. & Nickol, B. B.), pp. 347–84. Cambridge: Cambridge University Press.Google Scholar
Dobson, A. P. & Merenlender, A. (1991). Coevolution of macroparasites and their hosts. In Parasite-Host Associations: Coexistence or Conflict? (ed. Toft, C. A., Aeschlimann, A. & Bolis, L.), pp. 83–101. Oxford: Oxford University Press.CrossRefGoogle Scholar
Endler, J. A. (1983). Natural selection on color patterns in poeciliid fishes. Environmental Biology of Fishes 9, 173–90.CrossRefGoogle Scholar
Forbes, M. R. L. (1993). Parasitism and host reproductive effort. Oikos 67, 444–50.CrossRefGoogle Scholar
Fraser, D. F. & Gilliam, J. F. (1987). Feeding under predation hazard: response of the guppy and Hart's rivulus from sites with contrasting predation hazard. Behavioural Ecology and Sociobiology 21, 203–9.CrossRefGoogle Scholar
Hagen, D. W. & Gilbertson, L. G. (1972). Geographic variation and environmental selection in Gasterosteus aculeatus L. in the Pacific Northwest, America. Evolution 26, 32–51.CrossRefGoogle ScholarPubMed
Hamilton, W. D. (1964). The genetical evolution of social behaviour, I & II. Journal of Theoretical Biology 7, 1–52.CrossRefGoogle ScholarPubMed
Harvey, P. H. & Pagel, M. D. (1991). The Comparative Method in Evolutionary Biology. Oxford: Oxford University Press.CrossRefGoogle Scholar
Helluy, S. & Holmes, J. C. (1990). Serotonin, octopamine, and the clinging behaviour induced by the parasite Polymorphus paradoxus (Acanthocephala) in Gammarus lacustris (Crustacea). Canadian Journal of Zoology 68, 1214–20.CrossRefGoogle Scholar
Holmes, J. C. & Bethel, W. M. (1972). Modification of intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. U. & Wright, C. A.), pp. 123–49. London: Academic Press.Google Scholar
Holmes, J. C. & Zohar, S. (1990). Pathology and host behaviour. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.), pp. 34–64. London: Taylor and Francis.Google Scholar
Hurd, H. (1990). Physiological and behavioural interactions between parasites and invertebrate hosts. Advances in Parasitology 29, 271–318.Google ScholarPubMed
Hurd, H. & Fogo, S. (1991). Changes induced by Hymenolepis diminuta (Cestoda) in the behaviour of the intermediate host Tenebrio molitor (Coleoptera). Canadian Journal of Zoology 69, 2291–4.CrossRefGoogle Scholar
Lafferty, K. D. (1992). Foraging on prey that are modified by parasites. American Naturalist 140, 854–67.CrossRefGoogle Scholar
Lloyd, M. (1967). Mean crowding. Journal of Animal Ecology 36, 1–30.CrossRefGoogle Scholar
Lobue, C. P. & Bell, M. A. (1993). Phenotypic manipulation by the cestode parasite Schistocephalus solidus of its intermediate host, Gasterosteus aculeatus, the threespine stickleback. American Naturalist 142, 725–35.CrossRefGoogle ScholarPubMed
Lozano, G. A. (1991). Optimal foraging theory: a possible role for parasites. Oikos 60, 391–5.CrossRefGoogle Scholar
Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M. & Schad, G. A. (1982). The use of ecological terms in parasitology (Report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology 68, 131–3.CrossRefGoogle Scholar
MaynardSmith, J. Smith, J. (1982). Evolution and the Theory of Games. Cambridge: Cambridge University Press.Google Scholar
Minchella, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–16.CrossRefGoogle Scholar
Moore, J. (1984). Altered behavioural responses in intermediate hosts: an acanthocephalan parasite strategy. American Naturalist 123, 572–7.CrossRefGoogle Scholar
Moore, J. & Gotelli, N. J. (1990). A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.), pp. 193–233. London: Taylor and Francis.Google Scholar
Oetinger, D. F. & Nickol, B. B. (1982). Spectrophotometric characterization of integumental pigments from uninfected and Acanthocephalus dirus - infected Asellus intermedius. Journal of Parasitology 68, 270–5.CrossRefGoogle Scholar
Poinar, G. O. Jr. (1991 a). Hairworm (Nematomorpha: Gordioidea) parasites of New Zealand wetas (Orthoptera: Stenopelmatidae). Canadian Journal of Zoology 69, 1592–9.CrossRefGoogle Scholar
Poinar, G. O. Jr. (1991 b). Nematoda and Nematomorpha. In Ecology and Classification of North American Freshwater Invertebrates (ed. Thorp, J. H. & Covich, A. P.), pp. 249–83. New York: Academic Press.Google Scholar
Poulin, R. (1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937–44.CrossRefGoogle Scholar
Poulin, R. (in press). Meta-analysis of parasite-induced behavioural changes. Animal Behaviour.Google Scholar
Poulin, R., Brodeur, J. & Moore, J. (in press). Parasite manipulation of host behaviour: should hosts always lose? Oikos.Google Scholar
Poulin, R., Curtis, M. A. & Rau, M. E. (1992). Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105, 265–71.Google Scholar
Reimchen, T. E. (1989). Loss of nuptial color in threespine sticklebacks (Gasterosteus aculeatus). Evolution 43, 450–60.Google ScholarPubMed
Seghers, B. H. (1974). Geographic variation in the responses of guppies (Poecilia reticulata) to aerial predators. Oecologia 14, 93–8.CrossRefGoogle Scholar
Smith Trail, D. R. (1980). Behavioural interactions between parasites and hosts: host suicide and the evolution of complex life cycles. American Naturalist 116, 77–91.Google Scholar
Stearns, S. C. (1989). Trade-offs in life-history evolution. Functional Ecology 3, 259–68.CrossRefGoogle Scholar
Szidat, L. (1969). Structure, development, and behaviour of new strigeatoid metacercariae from subtropical fishes of South America. Journal of the Fisheries Research Board of Canada 26, 753–86.CrossRefGoogle Scholar
Taugbøl, T., Skurdal, J. & Andersen, R. (1988). Ecological significance of differences in frequency of white fin margins among four brown trout (Salmo trutta) populations. Canadian Journal of Fisheries and Aquatic Sciences 45, 1304–9.CrossRefGoogle Scholar
Thompson, S. N. & Kavaliers, M. (1994). Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109 (Suppl.), S119–S138.CrossRefGoogle ScholarPubMed
Tierney, J. F., Huntingford, F. A. & Crompton, D. W. T. (1993). The relationship between infectivity of Schistocephalus solidus (Cestoda) and anti-predator behaviour of its intermediate host, the three-spined stickleback, Gasterosteus aculeatus. Animal Behaviour 46, 603–5.CrossRefGoogle Scholar
Wickler, W. (1976). Evolution-oriented ethology, kin selection, and altruistic parasites. Zeitschrift für Tierpsychologie 42, 206–14.CrossRefGoogle ScholarPubMed