Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-23T22:39:13.326Z Has data issue: false hasContentIssue false
  • English
  • Français

Resistance against heterogeneous sequential infections: experimental studies with a tapeworm and its copepod host

Published online by Cambridge University Press:  12 April 2024

J. Kurtz  and
K. Hammerschmidt
J. Kurtz*
Affiliation:
Department of Evolutionary Ecology, Max Planck Institute of Limnology, August-Thienemann-Str. 2, 24306 Plön, Germany
K. Hammerschmidt
Affiliation:
Department of Evolutionary Ecology, Max Planck Institute of Limnology, August-Thienemann-Str. 2, 24306 Plön, Germany
*
*Address for correspondence: ETH Zürich Ecology and Evolution, ETH-Zentrum, CHN J12.1, Universitätsstr. 16, CH-8092 Zürich, Switzerland Fax: +41 44 63 21 271 E-mail: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Parasite heterogeneity is thought to be an important factor influencing the likelihood and the dynamics of infection. Previous studies have demonstrated that simultaneous exposure of hosts to a heterogeneous mixture of parasites might increase infection success. Here this view is extended towards the effect of parasite heterogeneity on subsequent infections. Using a system of the tapeworm Schistocephalus solidus and its copepod intermediate host, heterogeneity of the tapeworm surface carbohydrates is investigated, i.e. structures that are potentially recognized by the invertebrate host's immune system. With lectin labelling, a significant proportion of variation in surface carbohydrates is related to differences in worm sibships (i.e. families). Tapeworm sibships were used for experimental exposure of copepods to either homogeneous combinations of tapeworm larvae, i.e. worms derived from the same sibship or heterogeneous mixtures of larvae, and copepods were subsequently challenged with an unrelated larva to study re-infection. Contrary to expectation, neither an effect of parasite heterogeneity on the current infection, nor on re-infection were found. The effect of parasitic heterogeneity on host immunity is therefore complex, potentially involving increased cross-protection on the one hand, with higher costs of raising a more heterogeneous immune response on the other.

Type
Research Article
Information
Journal of Helminthology , Volume 80 , Issue 2 , June 2006 , pp. 199 - 206
Copyright
Copyright © Cambridge University Press 2006

References

Adema, C.M., Hertel, L.A., Miller, R.D. & Loker, E.S. (1997) A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proceedings of the National Academy of Sciences of the United States of America 94, 8691–8696.CrossRefGoogle ScholarPubMed
Ahmed, R. & Gray, D. (1996) Immunological memory and protective immunity: understanding their relation. Science 272, 54–60.CrossRefGoogle ScholarPubMed
Armitage, S.A.O., Thompson, J.J.W., Rolff, J. & Siva-Jothy, M.T. (2003) Examining costs of induced and constitutive immune investment in Tenebrio molitor. Journal of Evolutionary Biology 16, 1038–1044.CrossRefGoogle ScholarPubMed
Buchner, A., Faul, F. & Erdfelder, E. (1997) G Power: a priori, post-hoc, and compromise power analyses for the Macintosh (Version 2.1.2). Computer program, University of Trier, Trier, Germany.Google Scholar
Carius, H.J., Little, T.J. & Ebert, D. (2001) Genetic variation in a host–parasite association: potential for coevolution and frequency-dependent selection. Evolution 55, 1136–1145.Google Scholar
Christen, M. & Milinski, M. (2003) The consequences of self-fertilzation and outcrossing of the cestode Schistocephalus solidus in its second intermediate host. Parasitology 126, 369–378.CrossRefGoogle ScholarPubMed
Christen, M., Kurtz, J. & Milinski, M. (2002) Outcrossing increases infection success and competitive ability: experimental evidence from a hermaphrodite parasite. Evolution 56, 2243–2251.Google ScholarPubMed
Davies, C.M., Fairbrother, E. & Webster, J.P. (2002) Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124, 31–38.CrossRefGoogle ScholarPubMed
De Roode, J.C., Read, A.F., Chan, B.H.K. & Mackinnon, M.J. (2003) Rodent malaria parasites suffer from the presence of conspecific clones in three-clone Plasmodium chabaudi infections. Parasitology 127, 411–418.CrossRefGoogle ScholarPubMed
Dubinina, M.N. (1957) Experimental study of the life cycle of Schistocephalus solidus (Cestoda: Pseudophyllidea). Zoologichesky Zhurnal 36, 1647–1658.Google Scholar
Dubinina, M.N. (1966) Tapeworms (Cestoda, Ligulidae) of the Fauna of the USSR – Remnetsy (Cestoda, Ligulidae) Fauny SSSR (translated from Russian and published for the National Marine Fisheries Service, Amerind Publ., New Delhi, 1980). Moscow, Leningrad, Nauka Publishers.Google Scholar
Ebert, D. (1998) Evolution–experimental evolution of parasites. Science 282, 1432–1435.CrossRefGoogle Scholar
Ebert, D., Zschokke-Rohringer, C.D. & Carius, H.J. (1998) Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proceedings of the Royal Society of London, Series B: Biological Sciences 265, 2127–2134.CrossRefGoogle Scholar
Edwards, S.V. & Hedrick, P.W. (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends in Ecology and Evolution 13, 305–311.CrossRefGoogle ScholarPubMed
Faulhaber, L.M. & Karp, R.D. (1992) A diphasic immune response against bacteria in the American cockroach. Immunology 75, 378–381.Google ScholarPubMed
Frank, S.A. (2000) Specific and non-specific defense against parasitic attack. Journal of Theoretical Biology 202, 283–304.CrossRefGoogle ScholarPubMed
Frank, S.A. (2002) Immunology and evolution of infectious disease. 348 pp. Princeton, New Jersey, Princeton University Press.Google ScholarPubMed
George, A.J.T. (2002) Is the number of genes we possess limited by the presence of an adaptive immune system? Trends in Immunology 23, 351–355.CrossRefGoogle Scholar
Hammerschmidt, K. & Kurtz, J. (2005a) Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle. Proceedings of the Royal Society of London, Series B: Biological Sciences 272, 2511–2518.Google Scholar
Hammerschmidt, K. & Kurtz, J. (2005b) Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: individual variation and fitness consequences. International Journal for Parasitology 35, 1499–1507.CrossRefGoogle ScholarPubMed
Hughes, W.O.H., Petersen, K.S., Ugelvig, L.V., Pedersen, D., Thomsen, L., Poulsen, M. & Boomsma, J.J. (2004) Density-dependence and within-host competition in a semelparous parasite of leaf-cutting ants. BMC Evolutionary Biology 4, 45.CrossRefGoogle Scholar
Imhoof, B. & Schmid-Hempel, P. (1998) Single-clone and mixed-clone infections versus host environment in Crithidia bombi infecting bumblebees. Parasitology 117, 331–336.CrossRefGoogle ScholarPubMed
Jacobson, R.L. & Doyle, R.J. (1996) Lectin–parasite interactions. Parasitology Today 12, 55–61.CrossRefGoogle ScholarPubMed
Jacot, A., Scheuber, H., Kurtz, J. & Brinkhof, M.W.G. (2005) Juvenile immune system activation induces a costly upregulation of adult immunity in field crickets Gryllus campestris. Proceedings of the Royal Society of London, Series B: Biological Sciences 272, 63–69.Google ScholarPubMed
Janeway, C.A., Travers, P., Walport, M. & Capra, J.D. (1999) Immunobiology: the immune system in health and disease. 635 pp. London, Current Biology Publications.Google Scholar
Klein, J. (1989) Are invertebrates capable of anticipatory immune responses? Scandinavian Journal of Immunology 29, 499–505.CrossRefGoogle ScholarPubMed
Kurtz, J. (2003) Sex, parasites and resistance–an evolutionary approach. Zoology 106, 327–339.CrossRefGoogle ScholarPubMed
Kurtz, J. (2004) Memory in the innate and adaptive immune systems. Microbes and Infection 6, 1410–1417.CrossRefGoogle ScholarPubMed
Kurtz, J. (2005) Specific memory within innate immune systems. Trends in Immunology 26, 186–192.CrossRefGoogle ScholarPubMed
Kurtz, J. & Franz, K. (2003) Evidence for memory in invertebrate immunity. Nature 425, 37–38.CrossRefGoogle ScholarPubMed
Kurtz, J., van der Veen, I.T. & Christen, M. (2002) Fluorescent vital labeling to track cestodes in a copepod intermediate host. Experimental Parasitology 100, 36–43.CrossRefGoogle Scholar
Little, T.J. & Kraaijeveld, A.R. (2004) Ecological and evolutionary implications of immunological priming in invertebrates. Trends in Ecology and Evolution 19, 58–60.CrossRefGoogle ScholarPubMed
Mallon, E.B., Loosli, R. & Schmid-Hempel, P. (2003) Specific versus nonspecific immune defense in the bumblebee, Bombus terrestris L. Evolution 57, 1444–1447.Google ScholarPubMed
Moret, Y. (2003) Explaining variable costs of the immune response: selection for specific versus non-specific immunity and facultative life history change. Oikos 102, 213–216.CrossRefGoogle Scholar
Moret, Y. & Schmid-Hempel, P. (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 1166–1168.CrossRefGoogle Scholar
Nyame, A.K., Kawar, Z.S. & Cummings, R.D. (2004) Antigenic glycans in parasitic infections: implications for vaccines and diagnostics. Archives of Biochemistry and Biophysics 426, 182–200.CrossRefGoogle ScholarPubMed
Råberg, L., Vestberg, M., Hasselquist, D., Holmdahl, R., Svensson, E., Nilsson, J.-A. (2002) Basal metabolic rate and the evolution of the adaptive immune system. Proceedings of the Royal Society of London, Series B: Biological Sciences 269, 817–821.CrossRefGoogle ScholarPubMed
Read, A.F. & Taylor, L.H. (2001) The ecology of genetically diverse infections. Science 292, 1099–1102.CrossRefGoogle ScholarPubMed
Rolff, J. & Siva-Jothy, M.T. (2003) Ecological immunology: an invertebrate perspective. Science 301, 472–475.CrossRefGoogle Scholar
Schärer, L. & Wedekind, C. (1999) Lifetime reproductive output in a hermaphrodite cestode when reproducing alone or in pairs: a time cost of pairing. Evolutionary Ecology 13, 381–394.CrossRefGoogle Scholar
Schjørring, S. (2004) Delayed selfing in relation to the availability of a mating partner in the cestode Schistocephalus solidus. Evolution 58, 2591–2596.Google Scholar
Schmid-Hempel, P. (2003) Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London, Series B: Biological Sciences 270, 357–366.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P. & Ebert, D. (2003) On the evolutionary ecology of specific immune defence. Trends in Ecology and Evolution 18, 27–32.CrossRefGoogle Scholar
Sheldon, B.C. & Verhulst, S. (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.CrossRefGoogle ScholarPubMed
Smyth, J.D. (1946) Studies on tapeworm physiology. 1. The cultivation of Schistocephalus solidus in vitro. Journal of Experimental Biology 23, 47–70.CrossRefGoogle ScholarPubMed
Taylor, L.H., Walliker, D. & Read, A.F. (1997) Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitology 115, 121–132.CrossRefGoogle ScholarPubMed
Taylor, L.H., Welburn, S.C. & Woolhouse, M.E.J. (2002) Theileria annulata: virulence and transmission from single and mixed clone infections in cattle. Experimental Parasitology 100, 186–195.CrossRefGoogle ScholarPubMed
van der Veen, I.T. & Kurtz, J. (2002) To avoid or eliminate: cestode infections in copepods. Parasitology 124, 465–474.CrossRefGoogle ScholarPubMed
van Valen, L.M. (1973) A new evolutionary law. Evolutionary Theory 1, 1–30.Google Scholar
Wedekind, C. (1997) The infectivity, growth, and virulence of the cestode Schistocephalus solidus in its first intermediate host, the copepod Macrocyclops albidus. Parasitology 115, 317–324.CrossRefGoogle ScholarPubMed
Wedekind, C. & Ruetschi, A. (2000) Parasite heterogeneity affects infection success and the occurrence of within-host competition: an experimental study with a cestode. Evolutionary Ecology Research 2, 1031–1043.Google Scholar
Williams, G.C. & Nesse, R.M. (1991) The dawn of Darwinian medicine. Quarterly Review of Biology 66, 1–22.CrossRefGoogle ScholarPubMed
Zhang, S.-M., Adema, C.M., Kepler, T.B. & Loker, E.S. (2004) Diversification of Ig superfamily genes in an invertebrate. Science 305, 251–254.CrossRefGoogle Scholar
Zinkernagel, R.M., Bachmann, M.F., Kundig, T.M., Oehen, S., Pirchet, H. & Hengartner, H. (1996) On immunological memory. Annual Review of Immunology 14, 333–367.CrossRefGoogle ScholarPubMed
Zuk, M. & Stoehr, A.M. (2002) Immune defense and host life history. American Naturalist 160, S9–S22.CrossRefGoogle ScholarPubMed