Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-07T08:33:41.406Z Has data issue: false hasContentIssue false
  • English
  • Français

The evolution of inducible defence

Published online by Cambridge University Press:  06 April 2009

C. D. Harvell
C. D. Harvell
Affiliation:
Section of Ecology and Systematics, Corson Hall, Cornell University, Ithaca, N. Y. 14853
Get access Rights & Permissions [Opens in a new window]

Summary

Defences against parasites are characterized by inducible, amplifiable responses, often with a memory component. Inducible defences with similar properties are common in a variety of other types of interactions, for example many aquatic invertebrates produce inducible structural defences against their predators and competitors. Most inducible defences have the following properties: (1) a threshold of activation; (2) an amplification of response with increasing stimulus; (3) a memory component. Specificity, amplification and memory are the basis for defining a defence as ‘immune’ (Klein, 1982), and these properties are present in both the vertebrate and invertebrate internal defence responses to pathogens. Invertebrates differ in the absence of immunoglobulins and therefore in reduced specificity. Although the reduced specificity of invertebrate internal defence systems is often viewed as proof of their ‘primitiveness’, the differences in defence systems of vertebrates and invertebrates may be more related to their respective selection regimes than to phylogeny. The syngeneic recognition system of vertebrates functions to recognize small departures from self, such as would arise from neoplasia. Are vertebrates under more intense selection from neoplasia, perhaps due to a greater incidence of hormonal imbalance or hypersensitivity reactions? The invertebrate internal defence systems are all less discriminating than the vertebrate, but there are marked differences in degree of discrimination depending on whether the group is colonial or not. Even the phyla of colonial animals with quite simple body plans, the sponges and cnidarians, have a more discriminating recognition system than the phyla of solitary animals with more complex body plans, such as the molluscs and arthropods. The primary effectors of all invertebrate responses to parasites are encapsulation and phagocytosis, although in some phyla there are specific antibacterial proteins that can also be induced. A primary effector of the vertebrate immune system is also based on phagocytosis, but is mediated largely by immunoglobulins. Although memory is a widespread property of inducible defence systems, the mechanisms, underlying memory components are unknown except in the vertebrate immune response. The function and adaptiveness of many of these accelerated or amplified second-set responses remain unclear, although it is tempting to conclude that a memory component is a beneficial adaptation to multiple, intermittent stimuli. From this review I conclude that the conditions that favour the evolution of inducible defences include: (1) an intermittent, unpredictable selective regime; (2) selection for a ‘camouflaged’ defence, to slow parasite counter-adaptation; (3) reliable cues and (4) high costs of defence.

Keywords

inducible defencememoryimmune mechanismevolution
Type
Research Article
Information
Parasitology , Volume 100 , Issue S1: Symposia of the British Society for Parasitology Volume 27:The evolutionary biology of parasitism , June 1990 , pp. S53 - S61
Copyright
Copyright © Cambridge University Press 1990

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

Anderson, R. M. (1986). Genetic variability in resistance to parasitic invasion: population implications for invertebrate host species. Symposium of the Zoological Society London 56, 239–74.Google Scholar
Anderson, R. M. & Crombie, J. A. (1985). Experimental studies of age-intensity and age-prevalence profiles of infection: Schistosoma mansoni in snails and mice. In Ecology and Genetics of Host—Parasite Interactions (ed. Rollinson, N. A. & Anderson, R. M.) London: Academic Press.Google Scholar
Appleton, R. & Palmer, R. A. (1988). Waterborne stimuli released by predatory crabs and damaged prey induce more predator-resistant shells in marine gastropods. Proceedings of the National Academy of Sciences, USA 85, 4387–91.CrossRefGoogle Scholar
Baldwin, I. T. (1990). Costs of inducible alkaloid production in Nicotiana. Ecology, (in the Press).Google Scholar
Bazzaz, F. A., Chiarella, N. A., Coley, P. D. & Pitelka, L. F. (1987). Allocating resources to reproduction and defence. Bioscience 37, 58–67.CrossRefGoogle Scholar
Bigger, C. H., Jokiel, P. L. & Hildemann, W. H. (1983). Cytotoxic transplantation immunity in the sponge Toxidocia violacea. Transplantation 35, 239–43.CrossRefGoogle ScholarPubMed
Bigger, C. H., Jokiel, P. L., Hildemann, W. H. & Johnston, L. S. (1982). Characterization of alloimmune memory in a sponge. Journal of Immunology 192, 1570–2.CrossRefGoogle Scholar
Brehelin, M. (1986). Immunity in Invertebrates: Cells, Molecules and Defence Reactions. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Brindley, P. J. & Dobson, C. (1981). Genetic control of liability to infection with Nematospiroides dubius in mice: selection of refractory and liable populations of mice. Parasitology 83, 51–65.CrossRefGoogle ScholarPubMed
Burnet, M. (1970). Immunological Surveillance. Sydney: Pergamon Press.CrossRefGoogle ScholarPubMed
Buss, L. W. (1982). Somatic cell parasitism and the evolution of somatic tissue compatibility. Proceedings of the National Academy of Sciences, USA 79, 5337–41.CrossRefGoogle ScholarPubMed
Buss, L. W. (1983). Evolution, development, and the units of selection. Proceedings of the National Academy of Sciences, USA 80, 1387–91.CrossRefGoogle ScholarPubMed
Buss, L. W. (1987). The Evolution of Individuality. Princeton, N. J.: Princeton University Press.Google Scholar
Buss, L. W., McFadden, C. S. & Keene, D. R. (1984). Biology of Hydractiniid hydroids. 2. Histocompatibility effector system mediated by nematocyst discharge. Biological Bulletin 167, 131–58.CrossRefGoogle Scholar
Chornesky, E. A. (1983). Induced development of sweeper tentacles on the reef coral Agaricia agaricites: a response to direct competition. Biological Bulletin 165, 569–81.CrossRefGoogle ScholarPubMed
Coley, P. D. (1986). Costs and benefits of defence by tannins in a neotropical tree. Oecologia 70, 238–41.CrossRefGoogle Scholar
Dunn, P. E. (1986). Biochemical aspects of insect immunity. Annual Review of Entomology 31, 321–39.CrossRefGoogle Scholar
Evans, C. W., Kerr, J. & Curtis, A. S. G. (1980). Graft rejection and immune memory in marine sponges. In Phylogeny of Immune Memory (ed. Manning, M. J.), pp. 27–34. Amsterdam: Elsevier Biomedical Press.Google Scholar
Francis, L., (1988). Clonal anemones and the evolution of aggression. Biological Bulletin 174, 241–53.CrossRefGoogle Scholar
Freeman, G. (1964). The role of blood cells in the process of asexual reproduction in the tunicate Perophora viridis. Journal of Experimental Zoology 156, 157–84.CrossRefGoogle ScholarPubMed
Futuyma, D. & Statkin, M. (1983). Coevolution. New York: Sinauer Press.Google Scholar
Gilbert, J. J. (1966). Rotifer ecology and embryological induction. Science 151, 1234–7.CrossRefGoogle ScholarPubMed
Grosberg, R. K. (1988). The evolution of allorecognition specificity in clonal invertebrates. Quarterly Review of Biology 63, 377–412.CrossRefGoogle Scholar
Grosberg, R. K., Hedgecock, D. & Nelson, K. (1988). Invertebrate Historecognition. New York: Plenum Press.CrossRefGoogle Scholar
Grosberg, R. K. & Quinn, J. (1989). The evolution of selective aggression conditioned on allorecognition specificity. Evolution 43, 504–15.CrossRefGoogle ScholarPubMed
Harvell, C. D. (1984). Predator-induced defense in a marine bryozoan. Science 224, 1357–9.CrossRefGoogle Scholar
Harvell, C. D. (1986). The ecology and evolution of inducible defenses in a marine bryozoan: cues, costs, and consequences. American Naturalist 128, 810–23.CrossRefGoogle Scholar
Harvell, C. D. (1990). The ecology and evolution of inducible defences. Quarterly Review of Biology (in the Press).CrossRefGoogle Scholar
Harvell, C. D. & Padilla, D. (1990). Competitor-induced stolons in a marine bryozoan. Proceedings of the National Academy of Sciences, USA (in the Press).Google Scholar
Havel, J. (1987). Predator-induced defenses: a review. In Predation: Direct and Indirect Impacts on Aquatic Communities (ed. Kerfoot, W. C. & Sih, A.), pp. 263–278. Hanover, New Hampshire: University Press of New England.Google Scholar
Hildemann, W. H., Bigger, C. H., Jokiel, P. L. & Johnson, I. S. (1980). Characteristics of immune memory in invertebrates. In Phylogeny of Immunological Memory (ed. Manning, M. J.), pp. 9–15. Amsterdam: Elsevier Biomedical Press.Google Scholar
Hildemann, W. H., Raison, R. L., Cheung, O., Hull, C. J., Akaka, L. & Okamoto, J. (1977). Immunospecificity and memory in a scleractinian coral. Nature, London 270, 219–23.CrossRefGoogle Scholar
Ivker, F. (1972). A hierarchy of histo-incompatability in Hydractinia echinata. Biological Bulletin 143, 162–74.CrossRefGoogle Scholar
Klein, J. (1982). Immunology: the Science of Self-non-self Discrimination. New York: Wiley Interscience.Google Scholar
Lackie, A. M. (1986 a). Immune Mechanisms in Invertebrate Vectors (ed. Lackie, A. M.). Oxford: Clarendon Press.Google Scholar
Lackie, A. M. (1986 b). Evasion of insect immunity by helminth larvae. Symposium of the Zoological Society London 56, 161–78.Google Scholar
Lie, K. J. & Heyneman, D. (1979). Acquired resistance to echinostomes in four Biomphalaria glabrata strains. International Journal for Parasitology 9, 533–7.CrossRefGoogle ScholarPubMed
Lie, K. J., Heyneman, D. & Richards, C. S. (1979). Specificity of natural resistance to trematode infections in Biomphalaria glabrata. International Journal for Parasitology 9, 529–31.CrossRefGoogle ScholarPubMed
Lie, K. J., Jeong, K. H. & Heyneman, D. (1980). Inducement of miracidia-immobilizing substance in the hemolymph of Biomphalaria glabrata. International Journal for Parasitology 10, 183–8.CrossRefGoogle ScholarPubMed
Lie, K. J., Jeong, K. H. & Heyneman, D. (1982). Further characterization of acquired resistance in Biomophalaria glabrata. Journal of Parasitology 68, 529–31.CrossRefGoogle Scholar
Lively, C. M. (1986). Canalization versus developmental conversion in a spatially variable environment. American Naturalist 128, 561–72.CrossRefGoogle Scholar
Loker, E. S. & Bayne, C. J. (1986). Immunity to trematode larvae in the snail Biomphalaria. Symposium of the Zoological Society London 56, 199–220.Google Scholar
Smith, Maynard J. (1982). Evolution and the Theory of Games. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Mitchison, N. A. (1990). The evolution of acquired immunity in parasites. Parasitology 100 (Suppl.), S27–S34.CrossRefGoogle ScholarPubMed
Neigel, J. E. & Avise, J. C. (1985). The precision of histocompatibility response in clonal recognition in tropical marine sponges. Evolution 39, 724–34.CrossRefGoogle ScholarPubMed
Osborne, S. (1984). Bryozoan interactions: observations on stolonal interactions. Australian Journal of Marine and Freshwater Research 35, 453–62.CrossRefGoogle Scholar
Rinkevich, B. & Weissman, I. (1987). Chimeras in colonial invertebrates: an aggregation symbiosis or somatic and germ-cell parasitism? Symbiosis 4, 117–34.Google Scholar
Rowley, A. F., Rhodes, C. P. & Ratcliffe, N. A. (1984). Protochordate leucocytes: a review. Zoological Journal of the Linnean Society 80, 283–95.CrossRefGoogle Scholar
Sabbadin, A. (1982). Formal genetics of ascidians. American Zoologist 22, 765–73.CrossRefGoogle Scholar
Salt, G. (1970). The Cellular Defence Reactions of Insects. Cambridge: Cambridge University PressCrossRefGoogle Scholar
Sauer, K. P., Muller, M. & Weber, M. (1986). Alloimmune memory for glycoproteid recognition molecules in sea anemones competing for space. Marine Biology 92, 73–9.CrossRefGoogle Scholar
Sebens, K. & Miles, J. (1988). Sweeper tentacles in a gorgonian octocoral: morphological modifications for interference competition. Biological Bulletin 175, 378–87.CrossRefGoogle Scholar
Simms, E. L. & Rauscher, M. D. (1987). Costs and benefits of plant resistance to herbivory. American Naturalist 130, 570–81.CrossRefGoogle Scholar
Sminia, T., Van Der Knaap, W. P. W. & Edelenbosch, P. (1979). The role of serum factors in phagocytosis of foreign particles by blood cells of the freshwater snail Lymnaea stagnalis. Developmental and Comparative Immunology 3, 37–44.CrossRefGoogle ScholarPubMed
Smith, L. C. (1988). The role of sponge mesophyl cells in sponge allograft rejections. In Invertebrate Historecognition (ed. Grosberg, R. K., Hedgecock, D. & Nelson, K.), pp. 15–31. New York: Plenum Press.CrossRefGoogle Scholar
Sullivan, J. T., Richards, C. S., Lie, K. J. & Heyneman, D. (1982). Ribeiroia marini: irradiated miracidia and induction of acquired resistance in Biomphalaria glabrata. Experimental Parasitology 53, 17–25.CrossRefGoogle ScholarPubMed
Tallamy, D. W. & Krischik, V. A. (1989). Variation and function of cucurbitacins: an examination of current hypotheses. American Naturalist 133, 766–86.CrossRefGoogle Scholar
Knaap, van Der W. P. W. & Meuleman, E. A. (1986). Interaction between the immune system of lymnaeid snails and trematode parasites. Symposium of the Zoological Society London 56, 179–98.Google Scholar
Vyver, van de G. (1983). Absence of alloimmune memory in the freshwater sponge Ephydatia fluviatilis. Developmental and Comparative Immunology 7, 609–12.CrossRefGoogle Scholar
Vyver, van de G. (1988). Histocompatibility responses in freshwater sponges: a model for studies of cell-cell interactions in natural populations and experimental systems. In Invertebrate Historecognition (ed. Grosberg, R. K., Hedgecock, D. & Nelson, K.), pp. 1–14. New York: Plenum Press.Google Scholar
Wakelin, D. (1984). Immunity to Parasites: How Animals Control Parasitic Infections. London: Edward Arnold.Google Scholar