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Density-dependent effects on parasite growth and parasite-induced host immunodepression in the larval helminth Pomphorhynchus laevis

Published online by Cambridge University Press:  10 August 2010

STEPHANE CORNET
STEPHANE CORNET*
Affiliation:
Université de Bourgogne, UMR CNRS 5561 Biogéosciences, Dijon, France Génétique et Evolution des Maladies Infectieuses, UMR CNRS-IRD 2724, Montpellier, France Centre d'Ecologie Fonctionnelle et Evolutive, UMR CNRS 5175, Montpellier, France
*
*Corresponding author: Génétique et Evolution des Maladies Infectieuses, UMR CNRS-IRD 2724, Centre de Recherche IRD, 911 av. Agropolis, BP 64501, 34394 Montpellier cedex 5, France. Tel: +33 4 67 41 63 73. Fax: +33 4 67 41 62 99. E-mail: Stephane.Cornet@ird.fr
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Summary

Larval helminths exploit the physiology of their intermediate hosts: first, as a resource for energy and space and second by altering the immune system activity to ensure their survival. Whereas the growth pattern under parasite competition has been investigated, the effect of multiple infections on the level of parasite-induced immunodepression in a trophically transmitted helminth has been neglected. In this study, amphipods Gammarus pulex were infected in the laboratory by the acanthocephalan Pomphorhynchus laevis to investigate how parasite density in the intermediate host affected (i) cystacanth growth and (ii) the level of parasite-induced alterations of the host immune defences, two traits strongly linked to host exploitation. The study highlights that sharing a host is costly. As parasite intensity increases, competition for resources translates into a reduction in cystacanth volume. Immune manipulation is also modulated by density. Interestingly, immunodepression is higher in double-infected hosts compared to hosts with a single infection, suggesting an opportunity for cooperative immune manipulation. However, in higher multiple infections, parasites do not further down-regulate the host immune response, possibly to avoid additional costs that may outweigh the benefits of immunodepression.

Keywords

acanthocephalancompetitionexploitationimmunodepressionlarval helminth growthparasite intensityphenoloxidase

Information

Type
Research Article
Information
Parasitology , Volume 138 , Issue 2 , February 2011 , pp. 257 - 265
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Ball, M. A., Parker, G. A. and Chubb, J. C. (2008). The evolution of complex life cycles when parasite mortality is size- or time-dependent. Journal of Theoretical Biology 253, 202–214.CrossRefGoogle ScholarPubMed
Bollache, L., Rigaud, T. and Cézilly, F. (2002). Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). Journal of Invertebrate Pathology 79, 102–110.CrossRefGoogle ScholarPubMed
Brown, S. P. (1999). Cooperation and conflict in host-manipulating parasites. Proceedings of the Royal Society of London, B 266, 1899–1904.CrossRefGoogle 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
Cerenius, L., Bangyeekhun, E., Keyser, P., Soderhall, I. and Soderhall, K. (2003). Host prophenoloxidase expression in freshwater crayfish is linked to increased resistance to the crayfish plague fungus, Aphanomyces astaci. Cellular Microbiology 5, 353–357.CrossRefGoogle Scholar
Cerenius, L., Lee, B. L. and Söderhäll, K. (2008). The proPO-system: pros and cons for its role in invertebrate immunity. Trends in Immunology 29, 263–271.CrossRefGoogle ScholarPubMed
Cerenius, L. and Söderhäll, K. (2004). The prophenoloxidase-activating system in invertebrates. Immunological Reviews 198, 116–126.CrossRefGoogle ScholarPubMed
Cornet, S., Franceschi, N., Bauer, A., Rigaud, T. and Moret, Y. (2009 a). Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: consequences for the risk of super-infection and links with host behavioural manipulation. International Journal for Parasitology 39, 221–229.CrossRefGoogle ScholarPubMed
Cornet, S., Franceschi, N., Bollache, L., Rigaud, T. and Sorci, G. (2009 b). Variation and covariation in infectivity, virulence and immunodepression in the host-parasite association Gammarus pulex-Pomphorhynchus laevis. Proceedings of the Royal Society of London, B 276, 4229–4236.Google ScholarPubMed
Cornet, S. and Sorci, G. (2010). Parasite virulence when the infection reduces the host immune response. Proceedings of the Royal Society of London, B 277, 1929–1935.Google ScholarPubMed
Dezfuli, B. S., Giari, L. and Poulin, R. (2001). Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths. Parasitology 122, 483–489.CrossRefGoogle ScholarPubMed
Dezfuli, B. S., Lui, A., Giovinazzo, G. and Giari, L. (2008). Effect of Acanthocephala infection on the reproductive potential of crustacean intermediate hosts. Journal of Invertebrate Pathology 98, 116–119.CrossRefGoogle ScholarPubMed
Dezfuli, B. S., Rossetti, E., Bellettato, C. M. and Maynard, B. J. (1999). Pomphorhynchus laevis in its intermediate host Echinogammarus stammeri in the River Brenta, Italy. Journal of Helminthology 73, 95–102.CrossRefGoogle Scholar
Duclos, L. M., Danner, B. J. and Nickol, B. B. (2006). Virulence of Corynosoma constrictum (Acanthocephala : Polymorphidae) in Hyalella azteca (Amphipoda) throughout parasite ontogeny. Journal of Parasitology 92, 749–755.CrossRefGoogle ScholarPubMed
Franceschi, N., Bauer, A., Bollache, L. and Rigaud, T. (2008). The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. International Journal for Parasitology 38, 1161–1170.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Guillou, F., Roger, E., Mone, Y., Rognon, A., Grunau, C., Theron, A., Mitta, G., Coustau, C. and Gourbal, B. E. F. (2007). Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Molecular and Biochemical Parasitology 155, 45–56.CrossRefGoogle ScholarPubMed
Hanington, P. J., Lun, C.-M., Adema, C. M. and Loker, E. S. (2010). Time series analysis of transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei. International Journal for Parasitology 40, 819–831.CrossRefGoogle ScholarPubMed
Heins, D. C., Baker, J. A. and Martin, H. C. (2002). The “crowding effect” in the cestode Schistocephalus solidus: density-dependent effetcs on plerocercoid size and infectivity. Journal of Parasitology 88, 302–307.Google Scholar
Hewitson, J. P., Grainger, J. R. and Maizels, R. M. (2009). Helminth immunoregulation: The role of parasite secreted proteins in modulating host immunity. Molecular and Biochemical Parasitology 167, 1–11.CrossRefGoogle ScholarPubMed
Humbert, E. and Coustau, C. (2001). Refractoriness of host haemocytes to parasites immunosuppressive factors as a putative resistance mechanism in the Biomphlaria glabrata-Echinostoma caproni system. Parasitology 122, 651–660.CrossRefGoogle Scholar
Labbé, P. and Little, T. J. (2009). ProPhenolOxidase in Daphnia magna: cDNA sequencing and expression in relation to resistance to pathogens. Developmental & Comparative Immunology 33, 674–680.CrossRefGoogle ScholarPubMed
Lagrue, C. and Poulin, R. (2008). Intra- and interspecific competition among helminth parasites: Effects on Coitocaecum parvum life history strategy, size and fecundity. International Journal for Parasitology 38, 1435–1444.CrossRefGoogle ScholarPubMed
Loker, E. S. (1994). On being a parasite in an invertebrate host: a short survival course. Journal of Parasitology 80, 728–747.CrossRefGoogle Scholar
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. (2004). Helminth parasites – masters of regulation. Immunological Reviews 201, 89–116.CrossRefGoogle ScholarPubMed
Michaud, M., Milinski, M., Parker, G. A. and Chubb, J. C. (2006). Competitive growth strategies in intermediate hosts: Experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evolutionary Ecology 20, 39–57.CrossRefGoogle Scholar
Outreman, Y., Bollache, L., Plaistow, S. and Cézilly, F. (2002). Patterns of intermediate host use and levels of association between two conflicting manipulative parasites. International Journal for Parasitology 32, 15–20.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Poulin, R. (1994). The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109, 109–118.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Quinn, G. P. and Keough, M. J. (2002). Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P. (2008). Parasite immune evasion: a momentous molecular war. Trends in Ecology & Evolution 23, 318–326.CrossRefGoogle ScholarPubMed
Steinauer, M. L. and Nickol, B. B. (2003). Effect of cystacanth body size on adult success. Journal of Parasitology 89, 251–254.CrossRefGoogle ScholarPubMed
Taraschewski, H. (2000). Host-parasite interactions in Acanthocephala: a morphological approach. Advances in Parasitology 46, 1–179.CrossRefGoogle ScholarPubMed
Volkmann, A. (1991). Localization of phenoloxidase in the midgut of Periplaneta americana parasitized by larvae of Moniliformis moniliformis (Acanthocephala). Parasitology Research 77, 616–621.CrossRefGoogle ScholarPubMed