Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-26T21:32:31.500Z Has data issue: false hasContentIssue false
  • English
  • Français

The influence of clonal diversity and intensity-dependence on trematode infections in an amphipod

Published online by Cambridge University Press:  21 January 2009

D. B. KEENEY ,
K. BRYAN-WALKER ,
N. KHAN ,
T. M. KING  and
R. POULIN
D. B. KEENEY
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin9054, New Zealand Department of Biological Sciences, Le Moyne College, 1419 Salt Springs Road, Syracuse, NY13214-1301, USA
K. BRYAN-WALKER
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin9054, New Zealand
N. KHAN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin9054, New Zealand
T. M. KING
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin9054, New Zealand
R. POULIN*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin9054, New Zealand
*
*Corresponding author: Department of Zoology, University of Otago, P.O. Box 56, Dunedin9054, New Zealand. Tel: +64 3 479 7983. Fax: +64 3 479 7584. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Individual animals are often infected not only by different parasite species, but also by multiple genotypes of the same parasite species. Genetic relatedness among parasites sharing a host is expected to modulate their strategies of resource exploitation, growth and virulence. We experimentally examined the effects that genetic diversity and infection intensity had on host mortality, infectivity and growth of the marine trematode Maritrema novaezealandensis in amphipod hosts. The presence of 2 versus 1 parasite genotype during infection did not influence subsequent host mortality, had different effects on infectivity among genotypes and did not influence growth or variation in parasite growth. Density-dependent growth reductions revealed that the number of parasites infecting a host was more important than their genetic relatedness. Temperature, host size, and host sex influenced the degree to which density-dependent factors affected parasite growth. Our results suggest that the effects of parasite relatedness vary among parasite genotypes in this trematode species, and reveal that many factors play an important role during parasite development and transmission.

Keywords

amphipodsclonalitygrowthMaritrema novaezealandensismicrosatellites
Type
Research Article
Information
Parasitology , Volume 136 , Issue 3 , March 2009 , pp. 339 - 348
Copyright
Copyright © 2009 Cambridge University Press

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

Brown, S. P. (1999). Cooperation and conflict in host-manipulating parasites. Proceedings of the Royal Society of London, B 266, 1899–1904.Google Scholar
Brown, S. P., Hochberg, M. E. and Grenfell, B. T. (2002). Does multiple infection select for raised virulence? Trends in Microbiology 10, 401–405.Google Scholar
Brown, S. P., de Lorgeril, J., Joly, C. and Thomas, F. (2003). Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis. Journal of Parasitology 89, 668–672.CrossRefGoogle ScholarPubMed
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodal Inference: A Practical Information-Theoretic Approach, 2nd Edn.Springer-Verlag, Berlin, Germany.Google Scholar
Bush, A. O., Fernández, J. C., Esch, G. W. and Seed, J. R. (2001). Parasitism: The Diversity and Ecology of Animal Parasites. Cambridge University Press, Cambridge, UK.Google Scholar
Chao, L., Hanley, K. A., Burch, C. L., Dahlberg, C. and Turner, P. E. (2000). Kin selection and parasite evolution: higher and lower virulence with hard and soft selection. Quarterly Review of Biology 75, 261–275.CrossRefGoogle ScholarPubMed
Chubb, J. C. (1979). Seasonal occurrence of helminthes in freshwater fishes. Part II Trematoda. Advances in Parasitology 17, 141–313.CrossRefGoogle Scholar
Davies, C. M., Fairbrother, E. and Webster, J. P. (2002). Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124, 31–38.CrossRefGoogle ScholarPubMed
Dugatkin, L. A. (1997). Cooperation Among Animals: An Evolutionary Perspective. Oxford University Press, Oxford, UK.Google Scholar
Frank, S. A. (1992). A kin selection model for the evolution of virulence. Proceedings of the Royal Society of London, B 250, 195–197.Google ScholarPubMed
Frank, S. A. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 37–78.Google Scholar
Fredensborg, B. L. and Poulin, R. (2005). Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 1061–1070.Google Scholar
Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2004). Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. Journal of Experimental Marine Biology and Ecology 311, 253–265.Google Scholar
Gower, C. M. and Webster, J. P. (2005). Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution 59, 544–553.Google Scholar
Griffin, A. S. and West, S. A. (2002). Kin selection: fact and fiction. Trends in Ecology and Evolution 17, 15–21.Google Scholar
Hamilton, W. D. (1964). The genetical evolution of social behaviour. Journal of Theoretical Biology 7, 1–52.Google Scholar
Hughes, A. R., Inouye, B. D., Johnson, M. T. J., Underwood, N. and Vellend, M. (2008). Ecological consequences of genetic diversity. Ecology Letters 11, 609–623.Google Scholar
Jager, I. and Schjorring, S. (2006). Multiple infections: relatedness and time between infections affect the establishment and growth of the cestode Schistocephalus solidus in its stickleback host. Evolution 60, 616–622.Google ScholarPubMed
Keymer, A. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573–587.CrossRefGoogle ScholarPubMed
Keeney, D. B., Waters, J. M. and Poulin, R. (2006). Microsatellite loci for the New Zealand trematode Maritrema novaezealandensis. Molecular Ecology Notes 6, 1042–1044.Google Scholar
Keeney, D. B., Waters, J. M. and Poulin, R. (2007 a). Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles. Molecular Ecology 16, 431–439.CrossRefGoogle ScholarPubMed
Keeney, D. B., Waters, J. M. and Poulin, R. (2007 b). Diversity of trematode genetic clones within amphipods and the timing of same-clone infections. International Journal for Parasitology 37, 351–357.Google Scholar
Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M. and Schad, G. A. (1982). The use of ecological terms in parasitology. Journal of Parasitology 68, 131–133.Google Scholar
Martorelli, S. R., Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2004). Description and proposed life cycle of Maritrema novaezealandensis n. sp. (Microphallidae) parasitic in red-billed gulls, Larus novaehollandiae scopulinus, from Otago Harbor, South Island, New Zealand. Journal of Parasitology 90, 272–277.CrossRefGoogle Scholar
Parker, G. A., Chubb, J. C., Roberts, G. N., Michaud, M. and Milinski, M. (2003). Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology 16, 47–54.Google Scholar
Poulin, R. (1996 a). The evolution of life history strategies in parasitic animals. Advances in Parasitology 37, 107–134.Google Scholar
Poulin, R. (1996 b). Sexual inequalities in helminth infections: a cost of being a male? American Naturalist 147, 287–295.CrossRefGoogle Scholar
Poulin, R. (1996 c). Helminth growth in vertebrate hosts: does host sex matter? International Journal for Parasitology 26, 1311–1315.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn.Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Poulin, R. and Latham, A. D. M. (2003). Effects of initial (larval) size and host body temperature on growth in trematodes. Canadian Journal of Zoology 81, 574–581.Google Scholar
Rauch, G., Kalbe, M. and Reusch, T. B. H. (2008). Partitioning average competition and extreme-genotype effects in genetically diverse infections. Oikos 117, 399–405.Google Scholar
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102.Google Scholar
Sandland, G. J. and Goater, C. P. (2000). Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). Journal of Parasitology 86, 1056–1060.Google Scholar
Schalk, G. and Forbes, M. R. (1997). Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78, 67–74.Google Scholar
Sheridan, L. A. D., Poulin, R., Ward, D. F. and Zuk, M. (2000). Sex differences in parasitic infections among arthropod hosts: is there a male bias? Oikos 88, 327–334.Google Scholar
Shostak, A. W. and Scott, M. E. (1993). Detection of density-dependent growth and fecundity of helminths in natural infections. Parasitology 106, 527–539.Google Scholar
Vizoso, D. B. and Ebert, D. (2005). Mixed inoculations of a microsporidian parasite with horizontal and vertical infections. Oecologia 143, 157–166.Google Scholar
Wedekind, C. and 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
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.Google Scholar