Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-28T02:21:14.864Z Has data issue: false hasContentIssue false

Clone-specific immune reactions in a trematode-crustacean system

Published online by Cambridge University Press:  14 October 2011

ANSON V. KOEHLER*
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand
ROBERT POULIN
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand
*
*Corresponding author: Tel: +64 03 479 5848; Fax: +64 03 479 7584; E-mail: ansonkoehler@gmail.com

Summary

Variability of immune responses is an essential aspect of ecological immunology, yet how much of this variability is due to differences among parasite genotypes remains unknown. Here, variation in immune response of the crab, Macrophthalmus hirtipes, is examined as a function of experimental exposure to 10 clonal cercarial lineages of the trematode Maritrema novaezealandensis. Our goals were (1) to assess the variability of the host immune reaction elicited by 10 parasite clones, (2) to test if the heterozygosity–fitness correlation, whereby organisms with higher heterozygosities achieve a higher fitness than those with lower heterozygosities, applies to heterozygous parasites eliciting weak immune responses, and (3) to see how concomitant infections by other macroparasites influence the crab's immune response to cercariae. Parasite clones were distinguished and heterozygosities calculated using 20 microsatellite markers. We found that exposure to cercariae resulted in increased haemocyte counts, and that although interclonal differences in immune response elicited were detected, parasite heterozygosity did not correlate with host immune response. Additionally, the presence of other pre-existing parasites in hosts did not influence their immune response following experimental exposure to cercariae. Overall, the existence of variability in immune response elicited by different parasite clones is promising for future ecological immunology studies using this system.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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

Bordes, F. and Morand, S. (2009). Coevolution between multiple helminth infestations and basal immune investment in mammals: cumulative effects of polyparasitism? Parasitology Research 106, 3337.CrossRefGoogle ScholarPubMed
Brownstein, M. J., Carpten, J. D. and Smith, J. R. (1996). Modulation of non-templated nucleotide addition by tag DNA polymerase: Primer modifications that facilitate genotyping. BioTechniques 20, 10041010.CrossRefGoogle Scholar
Bryan-Walker, K., Leung, T. L. F. and Poulin, R. (2007). Local adaptation of immunity against a trematode parasite in marine amphipod populations. Marine Biology 152, 687695.CrossRefGoogle Scholar
Carius, H. J., Little, T. J. and Ebert, D. (2001). Genetic variation in a host-parasite association: Potential for coevolution and frequency-dependent selection. Evolution 55, 11361145.Google Scholar
Chapman, J. R., Nakagawa, S., Coltman, D. W., Slate, J. and Sheldon, B. C. (2009). A quantitative review of heterozygosity-fitness correlations in animal populations. Molecular Ecology 18, 27462765.CrossRefGoogle ScholarPubMed
Cornet, S., Franceschi, N., Bauer, A., Rigaud, T. and Moret, Y. (2009). 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, 221229.CrossRefGoogle ScholarPubMed
Cox, F. E. G. (2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl.) S2338.CrossRefGoogle ScholarPubMed
de Roode, J. C. and Altizer, S. (2010). Host-parasite genetic interactions and virulence transmission relationships in natural populations of monarch butterflies. Evolution 64, 502514.CrossRefGoogle ScholarPubMed
Dittmer, J. (2010). The influence of parasites as an environmental factor on the immune response and haemolymph bacterial loads in New Zealand shore crabs. Unpublished Master's thesis. Université de Poitiers, Poitiers, France.Google Scholar
Dittmer, J., Koehler, A. V., Richard, F., Poulin, R. and Sicard, M. (2011). Parasitic pressure as a source of immune variation among populations of New Zealand shore crabs. Parasitology Research 109, 759767.CrossRefGoogle Scholar
Eslin, P. and Prévost, G. (1998). Hemocyte load and immune resistance to Asobara tabida are correlated in species of the Drosophila melanogaster subgroup. Journal of Insect Physiology 44, 807816.CrossRefGoogle 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, 253265.CrossRefGoogle Scholar
Goyal, P. K. and Wakelin, D. (1993). Influence of variation in host strain and parasite isolate on inflammatory and antibody responses to Trichinella spiralis in mice. Parasitology 106, 371378.CrossRefGoogle ScholarPubMed
Hansson, B. and Westerberg, L. (2002). On the correlation between heterozygosity and fitness in natural populations. Molecular Ecology 11, 24672474.CrossRefGoogle ScholarPubMed
Hawley, D. M. and Altizer, S. M. (2010). Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25, 4860.CrossRefGoogle Scholar
Hay, K. B., Fredensborg, B. L. and Poulin, R. (2005). Trematode-induced alterations in shell shape of the mud snail Zeacumantus subcarinatus (Prosobranchia : Batillariidae). Journal of the Marine Biological Association of the United Kingdom 85, 989992.CrossRefGoogle Scholar
Hayden, M. J., Nguyen, T. M., Waterman, A., McMichael, G. L. and Chalmers, K. J. (2008). Application of multiplex-ready PCR for fluorescence-based SSR genotyping in barley and wheat. Molecular Breeding 21, 271281.CrossRefGoogle Scholar
Hillyer, J. F., Schmidt, S. L., Fuchs, J. F., Boyle, J. P. and Christensen, B. M. (2005). Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cellular Microbiology 7, 3951.CrossRefGoogle ScholarPubMed
Jiravanichpaisal, P., Lee, B. L. and Söderhäll, K. (2006). Cell-mediated immunity in arthropods: Hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211, 213236.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, 10421044.CrossRefGoogle Scholar
Koehler, A. V., Gonchar, A. G. and Poulin, R. (2011 a). Genetic and environmental determinants of host use in the trematode Maritrema novaezealandensis (Microphallidae). Parasitology 138, 100106.CrossRefGoogle ScholarPubMed
Koehler, A. V. and Poulin, R. (2010). Host partitioning by parasites in an intertidal crustacean community. Journal of Parasitology 96, 862868.CrossRefGoogle Scholar
Koehler, A. V., Springer, Y. P., Keeney, D. B. and Poulin, R. (2011 b). Intra- and inter-clonal phenotypic and genetic variability of the trematode Maritrema novaezealandensis. Biological Journal of the Linnean Society 103, 106116.CrossRefGoogle Scholar
Kostadinova, A. and Mavrodieva, R. S. (2005). Microphallids in Gammarus insensibilis Stock, 1966 from a Black Sea lagoon: host response to infection. Parasitology 131, 347354.CrossRefGoogle Scholar
Kraaijeveld, A. R., Limentani, E. C. and Godfray, H. C. J. (2001). Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proceedings of the Royal Society of London, B 268, 259261.Google ScholarPubMed
Kurtz, J. (2002). Phagocytosis by invertebrate hemocytes: Causes of individual variation in Panorpa vulgaris scorpionflies. Microscopy Research and Technique 57, 456468.CrossRefGoogle ScholarPubMed
Lazzaro and Little, T. (2009). Immunity in a variable world. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 1526.Google Scholar
Le Moullac, G. and Haffner, P. (2000). Environmental factors affecting immune responses in Crustacea. Aquaculture 191, 121131.CrossRefGoogle Scholar
Lorenzon, S., de Guarrini, S., Smith, V. J. and Ferrero, E. A. (1999). Effects of LPS injection on circulating haemocytes in crustaceans in vivo. Fish & Shellfish Immunology 9, 3150.CrossRefGoogle Scholar
Molecular Ecology Resources Primer Development Consortium. (2009). Permanent genetic resources added to Molecular Ecology Resources database 1 January 2009–30 April 2009. Molecular Ecology Resources 9, 13751379.CrossRefGoogle Scholar
Nappi, A. J. (1981). Cellular immune response of Drosophila melanogaster against Asobara tabida. Parasitology 83, 319324.CrossRefGoogle Scholar
Paterson, S. (2005). No evidence for specificity between host and parasite genotypes in experimental Strongyloides ratti (Nematoda) infections. International Journal for Parasitology 35, 15391545.CrossRefGoogle ScholarPubMed
Persson, M., Cerenius, L. and Soderhall, K. (1987). The influence of haemocyte number on the resistance of the freshwater crayfish, Pacifastacus leniusculus Dana, to the parasitic fungus Aphanomyces astaci. Journal of Fish Diseases 10, 471477.CrossRefGoogle Scholar
Poulin, R. (2001). Interactions between species and the structure of helminth communities. Parasitology 122 (Suppl.) S311.CrossRefGoogle ScholarPubMed
R Development Core Team. (2010). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rauch, G., Kalbe, M. and Reusch, T. B. H. (2006). One day is enough: rapid and specific host–parasite interactions in a stickleback-trematode system. Biology Letters 2, 382384.CrossRefGoogle Scholar
Read, A. and Viney, M. (1996). Helminth immunogenetics: Why bother? Parasitology Today 12, 337343.CrossRefGoogle ScholarPubMed
Rigaud, T. and Moret, Y. (2003). Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression? Parasitology 127, 571577.CrossRefGoogle ScholarPubMed
Rodriguez, J., Boulo, V., Mialhe, E. and Bachere, E. (1995). Characterisation of shrimp haemocytes and plasma components by monoclonal antibodies. Journal of Cell Science 108, 10431050.CrossRefGoogle ScholarPubMed
Rolff, J. and Siva-Jothy, M. T. (2003). Invertebrate ecological immunology. Science 301, 472475.CrossRefGoogle ScholarPubMed
Sadd, B. M. and Schmid-Hempel, P. (2009). Principles of ecological immunology. Evolutionary Applications 2, 113121.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P. and Ebert, D. (2003). On the evolutionary ecology of specific immune defence. Trends in Ecology & Evolution 18, 2732.CrossRefGoogle Scholar
Scholtz, G., Braband, A., Tolley, L., Reimann, A., Mittmann, B., Lukhaup, C., Steuerwald, F. and Vogt, G. (2003). Ecology: Parthenogenesis in an outsider crayfish. Nature, London 421, 806806.CrossRefGoogle Scholar
Schuelke, M. (2000). An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18, 233234.CrossRefGoogle ScholarPubMed
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2007). Phenotypic variation in infectivity of Diplostomum spathaceum cercariae within a population. Journal of Parasitology 93, 12441246.CrossRefGoogle ScholarPubMed
Seppälä, O., Karvonen, A., Valtonen, E. T. and Jokela, J. (2009). Interactions among co-infecting parasite species: a mechanism maintaining genetic variation in parasites? Proceedings of the Royal Society of London, B 276, 691697.Google ScholarPubMed
Sequeira, T., Tavares, D. and Arala-Chaves, M. R. (1996). Evidence for circulating hemocyte proliferation in the shrimp Penaeus japonicus. Developmental & Comparative Immunology 20, 97104.CrossRefGoogle ScholarPubMed
Sicard, M., Chevalier, F., De Vlechouver, M., Bouchon, D., Greve, P. and Braquart-Varnier, C. (2010). Variations of immune parameters in terrestrial isopods: a matter of gender, aging and Wolbachia. Naturwissenschaften 97, 819826.CrossRefGoogle ScholarPubMed
Söderhäll, I., Bangyeekhum, E., Mayo, S. and Söderhäll, K. (2003). Hemocyte production and maturation in an invertebrate animal; proliferation and gene expression in hematopoietic stem cells of Pacifastacus leniusculus. Developmental and Comparative Immunology 27, 661672.CrossRefGoogle Scholar
Söderhäll, K. and Cerenius, L. (1998). Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology 10, 2328.CrossRefGoogle ScholarPubMed
Thomas, F., Guldner, E. and Renaud, F. (2000). Differential parasite (Trematoda) encapsulation in Gammarus aequicauda (Amphipoda). The Journal of Parasitology 86, 650654.CrossRefGoogle ScholarPubMed
Thomas, F., Renaud, F., Rousset, F., Cezilly, F. and de Meeûs, T. (1995). Differential mortality of two closely related host species induced by one parasite. Proceedings of the Royal Society of London, B 260, 349352.Google Scholar
Thomas, M. B., Watson, E. L. and Valverde-Garcia, P. (2003). Mixed infections and insect–pathogen interactions. Ecology Letters 6, 183188.CrossRefGoogle Scholar
Vardo-Zalik, A. M. (2009). Clonal diversity of a malaria parasite, Plasmodium mexicanum, and its transmission success from its vertebrate-to-insect host. International Journal for Parasitology 39, 15731579.CrossRefGoogle ScholarPubMed
Walsh, P. S., Metzger, D. A. and Higuchi, R. (1991). Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10, 506513.Google ScholarPubMed