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Do parasites live in extreme environments? Constructing hostile niches and living in them

Published online by Cambridge University Press:  16 October 2009

C. Combes*
Affiliation:
Laboratoire de Biologie Animale, UMR 5555 CNRS, Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Unirersité de Perpignan, Avenue de Villeneuve, F-66860 Perpignan Cedex, France
S. Morand
Affiliation:
Laboratoire de Biologie Animale, UMR 5555 CNRS, Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Unirersité de Perpignan, Avenue de Villeneuve, F-66860 Perpignan Cedex, France
*
* Corresponding author. Tel: 33 4 68 66 21 81; Fax: 33 4 68 66 22 81. E-mail: [email protected]

Summary

We develop the hypothesis that parasites do not invade extreme environments, i.e. hostile hosts, but rather ‘create’ them. We argue that parasites may have driven the evolution of the constitutive and adaptive immune system. This leads to several implications. First, parasites respond to ‘genes to kill’ by ‘genes to survive’ and this triggers an indefinite selection of measures and counter-measures. Second, these revolutionary arms races may lead to local adaptation, in which parasite populations perform better on local hosts. Third, the evolution of the immune system, whose responses are predictable, may allow parasites to specialize, to evade and even to manipulate. Finally we show that the correlations between the increase in the antibody repertoire, the expansion of MHC loci and parasite pressures support our hypothesis that both host complexity and parasite pressures can be invoked to explain the diversity of antibodies, T-receptors and MHC molecules.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1999

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References

REFERENCES

Arnal, C. & Côté, I. M. (1998). Interactions between cleaning gobies and territorial damseltish on coral reefs. Animal Behaviour 55, 14291442.CrossRefGoogle ScholarPubMed
Bristow, C. M. (1988). What makes a predator specialize? Trends in Ecology imd Evolution 3, 12.CrossRefGoogle Scholar
Combes, C. (1995). Interactions Durables. Ecologie et Evolution du Parasitisme. Paris, Masson.Google Scholar
Combes, C. & Théron, A. (2000). Metazoan parasites and resource heterogeneity: constraints and benefits. International Journal for Parasitology 30, 299304.CrossRefGoogle ScholarPubMed
Davey, B. (1990). Immunology. A Foundation Text. New Jersey, Prentice Hall.Google Scholar
Du Pasquier, L. (1982). Antibody diversity in lower vertebrates why is it so restricted? Nature 296, 311 313.CrossRefGoogle ScholarPubMed
Dupas, S & Boscaro, M. (1999). Geographic variation and evolution of immunosuppressive genes in a Drosophila parasitoid. Ecography 22, 284291.CrossRefGoogle Scholar
Frost, S. D. W (1999). The immune system as an inducible defense. In The Ecology and Evolution of Inducible Defenses (ed. Tollrian, R. & Harvell, C. D.), pp. 104126. Princeton, Princeton University Press.CrossRefGoogle Scholar
Gandon, S., Capowiez, Y., Dubois, Y., Michalakis, Y. & Olivieri, I. (1996). Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society of London, Series B Biological Sciences 263, 10031009.Google Scholar
Grutter, A. S. (1996). Parasite removal rates by the wrasse Labroides dimidiatus. Marine Ecology Progress Series 130, 6170.CrossRefGoogle Scholar
Grutter, A. S. (1999). Cleaner fish do clean. Nature 398, 672673.CrossRefGoogle Scholar
Hamilton, W. D., Axelrod, R. & Tanese, R. (1990). Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences, USA 87, 35663573.CrossRefGoogle ScholarPubMed
Hamilton, W. D. & Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384386.CrossRefGoogle Scholar
Hart, B. L., Hart, L. A. & Mooring, M. S. (1990). Differential foraging of oxpeckers on impala in comparison with sympatric antelope species. African Journal of Ecology 28, 240249.CrossRefGoogle Scholar
Jones, C. G., Lawton, J. H. & Shachak, M. (1994). Organisms as ecosystem engineers. Oikos 69, 373386.CrossRefGoogle Scholar
Jones, C. G., Lawton, J. H. & Shachak, M. (1997). Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78, 19461957.CrossRefGoogle Scholar
Kaltz, O. & Shykoff, J. A. (1998). Local adaptation in host-parasite systems. Heredity 81, 361370.CrossRefGoogle Scholar
Klein, J. (1991). Of HLA, Tryps, and selection: an essay on coevolution of MHC and parasites. Human Immunology 30, 247258.CrossRefGoogle ScholarPubMed
Ladle, R. J. (1992). Parasites and sex: catching the Red Oucen. Trends in Ecology and Evolution 7, 405408.CrossRefGoogle Scholar
Laland, K. N., Odling-Smee, F. J. & Feldmann, M. W. (1996). On the evolutionary consequences of niche construction. Journal of Evolutionary Biology 9, 293316.CrossRefGoogle Scholar
Laland, K. N., Odling-Smee, F. J. & Feldmann, M. W. (2000). Niche construction, biological evolution, and cultural change. Behavioral and Brain Sciences 23, 131175.CrossRefGoogle ScholarPubMed
Lively, C. M. (1989). Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43, 16631671.CrossRefGoogle ScholarPubMed
Lively, C. M. (1999). Migration, virulence, and the geographic mosaic of adaptation by parasites. The American Naturalist 153, S34S47.CrossRefGoogle ScholarPubMed
Moné, H., Mouahid, G. & Mokand, S. (2000). On biogeographical history of Schistosoma bovis Sonsino, 1876 in the light of both intermediate host spectrum and compatibility in the mollusc-parasite association. Advances in Parasitology 44, 99138.CrossRefGoogle Scholar
Morand, S. (2000). Wormy world: comparative tests of theoretical hypotheses on parasite species richness. In Evolutionary Biology of Host-Parasite Relationships: Reality Meets Models (ed. Poulin, R., Skorping, A. & Morand, S.). Elsevier (in press).Google Scholar
Morand, S, Hafner, M. S., Page, R. D. M & Reed, D. L. (2000). Comparative body size relationships in Pocket Gophers and their Chewing Lice. Biological Journal of the Linnean Society 70, 239 249.CrossRefGoogle Scholar
Morand, S., Manning, S. D. & Woolhouse, M. E. J (1996). Parasite-host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proceedings of the Royal Society of London, Series B Biological Sciences 263, 119128.Google ScholarPubMed
Odling-Smee, F. J., Laland, K. N. & Feldmann, M. W. (1996). Niche construction. American Naturalist 147, 641648.CrossRefGoogle Scholar
Paterson, S., Wilson, K. & Pemberton, J. M. (1998). Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proceedings of the National Academy of Sciences, USA 95, 37143719.CrossRefGoogle Scholar
Poulin, R. (1992). Determinants of host-specificity in parasites of freshwater fishes. International Journal for Parasitology 22, 753758.CrossRefGoogle ScholarPubMed
Poulin, R. (1999). The functional importance of parasites in animal communities: many roles at many levels? International Journal for Parasitology 29, 903914.CrossRefGoogle ScholarPubMed
Poulin, R. & Morand, s. (2000). The diversity of parasites. Quarterly Review of Biology (in press).CrossRefGoogle Scholar
Reina-San-Maktin, B., Cosson, A. & Minoprio, p. (2000). Lymphocyte polyclonal activation: a pitfall for vaccination design against infectious agents. Parasitology Today 16, 6267.CrossRefGoogle Scholar
Sasal, P., Desdevises, Y. & Morand, S. (1998). Host-specialization and species diversity in fish parasites: phylogenetic conservatism? Ecography 21, 639645.CrossRefGoogle Scholar
Sukhdeo, M. V. K (1997). Earth's third environment: the worm's eye view. BioScience 47, 141149.Google Scholar
Takahata, N. (1990). A simple genealogical structure of strongly allclic lines and trans-species evolution of polymorphism. Proceedings of the National Academy of Sciences, USA 87, 24192423.CrossRefGoogle ScholarPubMed
Thomas, F., Renaud, F., De Meeüs, T. & Poulin, R.(1998). Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proceedings of the Royal Society of London, Series B Biological Sciences 265, 10911096.CrossRefGoogle Scholar
Van Valen, L. (1973). A new evolutionary law. Evolutionary Theory 1, 130.Google Scholar
Vernon, P., Vannier, G. & Trehen, P. (1998). A comparative approach to the entomological diversity of polar regions. Acta Oecologica 19, 303308.CrossRefGoogle Scholar
Xia, M., Jourdane, J. & Combes, C. (1998). Local adaptation of Schistosoma japonicum in its snail host demonstrated by transplantation of sporocysts. ICOPA IX, Monduzzi Editore (ed. Tada, I., Kojima, S. & Tsuji, M.), pp. 573 576.Google Scholar