Skip to main content
×
Home
    • Aa
    • Aa

Local differences in immunocompetence reflect resistance of sticklebacks against the eye fluke Diplostomum pseudospathaceum

  • M. KALBE (a1) and J. KURTZ (a1) (a2)
Abstract

We investigated population differences in immunological adaptation of three-spined sticklebacks (Gasterosteus aculeatus) to one of their most abundant macroparasites, the eye fluke Diplostomum pseudospathaceum. We compared infection success in lab-bred fish of 2 populations in northern Germany, from a lake, where eye flukes are prevalent, and a river, where these parasites do not occur. In order to discriminate between protection through innate and acquired immunity, we exposed fish either only once or repeatedly. Lake fish were significantly less susceptible than river sticklebacks already after a single exposure, indicating that in sympatric hosts innate immunity plays the major role in the defence against this helminth infection. In both habitat types, previous exposures only marginally decreased infection rates within 12 weeks. Lake fish showed higher immunocompentence by means of respiratory burst activity and spleen size, regardless of the infection status. Furthermore, they were in a better energy status than river fish, as indicated by a higher hepatosomatic index and haematocrit value. Interestingly, F1 hybrid fish of both populations ranged between the pure habitat types in parasite susceptibility as well as in immunological and condition parameters. Our results suggest that sticklebacks from lakes are better adapted to cope with higher parasite abundance in this habitat.

Copyright
Corresponding author
Tel: +49 4522 763 256. Fax: +49 4522 763 310. E-mail: kalbe@mpil-ploen.mpg.de
References
Hide All

REFERENCES

Altizer, S. M. ( 2001). Migratory behaviour and host-parasite co-evolution in natural populations of monarch butterflies infected with a protozoan parasite. Evolutionary Ecology Research 3, 611632.
Ballabeni, P. and Ward, P. I. ( 1993). Local adaptation of the tremadote Diplostomum phoxini to the European minnow Phoxinus phoxinus, its 2nd intermediate host. Functional Ecology 7, 8490.
Brassard, P., Rau, M. E. and Curtis, M. A. ( 1982). Infection dynamics of Diplostomum spathaceum cercariae and parasite-induced mortality of fish hosts. Parasitology 85, 489493.
Briles, W. E., Stone, H. A. and Cole, R. K. ( 1977). Mareks-disease – effects of B-histocompatibility alloalleles in resistant and susceptible chicken lines. Science 195, 193195.
Chappell, L. H., Hardie, L. J. and Secombes, C. J. ( 1994). Diplostomiasis: the disease and host-parasite interactions. In Parasitic Diseases in Fish ( ed. Pike, A. W. and Lewis, J. W.), pp. 5986. Samara Publishing Limited, Dyfed, Wales.
Chellappa, S., Huntingford, F. A., Strang, R. C. H. and Thomson, R. Y. ( 1995). Condition factor and hepatosomatic index as estimates of energy status in male 3-spined stickleback. Journal of Fish Biololgy 47, 775787.
Criscione, C. D. and Blouin, M. S. ( 2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198202.
Crowden, A. E. and Broom, D. M. ( 1980). Effects of the eyefluke, Diplostomum spathaceum, on the behavior of dace (Leuciscus leuciscus). Animal Behaviour 28, 287294.
Dufva, R. ( 1996). Sympatric and allopatric combinations of hen fleas and great tits: a test of the local adaptation hypothesis. Journal of Evolutionary Biology 9, 505510.
Ebert, D. ( 1994). Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 10841086.
Ebert, D. and Hamilton, W. D. ( 1996). Sex against virulence: the coevolution of parasitic diseases. Trends in Evolutionary Ecology 11, A79A82.
Flajnik, M. F. and DuPasquier, L. ( 2004). Evolution of innate and adaptive immunity: can we draw a line? Trends in Immunology 25, 640644.
Frischknecht, M. ( 1993). The breeding coloration of male 3-spined sticklebacks (Gasterosteus aculeatus) as an indicator of energy investment in vigor. Evolutionary Ecology 7, 439450.
Godot, V., Harraga, S., Beurton, I., Tiberghien, P., Sarciron, E., Gottstein, B. and Vuitton, D. A. ( 2000). Resistance/susceptibility to Echinococcus multilocularis infection and cytokine profile in humans. II. Influence of the HLA B8, DR3, DQ2 haplotype. Clinical and Experimental Immunology 121, 491498.
Hill, A. V. S., Allsopp, C. E. M., Kwiatkowski, D., Anstey, N. M., Twumasi, P., Rowe, P. A., Bennett, S., Brewster, B., McMichael, A. J. and Greenwood, B. M. ( 1991). Common west African HLA antigens are associated with protection from severe malaria. Nature, London 352, 595600.
Höglund, J. and Thuvander, A. ( 1990). Indications of nonspecific protective mechanisms in rainbow-trout Oncorhynchus mykiss with diplostomosis. Diseases of Aquatic Organisms 8, 9197.
Imhoof, B. and Schmid-Hempel, P. ( 1998). Patterns of local adaptation of a protozoan parasite to its bumblebee host. Oikos 82, 5965.
Janeway, C. A., Travers, P., Walport, M. and Capra, J. D. ( 1999). Immunobiology: the Immune System in Health and Disease. Current Biology Publications, London.
Kalbe, M., Wegner, K. M. and Reusch, T. B. H. ( 2002). Dispersion patterns of parasites in 0+ year three-spined sticklebacks: a cross population comparison. Journal of Fish Biology 60, 15291542.
Kaltz, O. and Shykoff, J. A. ( 1998). Local adaptation in host-parasite systems. Heredity 81, 361370.
Kaltz, O. and Shykoff, J. A. ( 2002). Within- and among-population variation in infectivity, latency and spore production in a host-pathogen system. Journal of Evolutionary Biology 15, 850860.
Karvonen, A., Paukku, S., Seppälä, O. and Valtonen, E. T. ( 2005). Resistance against eye flukes: naive versus previously infected fish. Parasitology Research 95, 5559.
Kennedy, C. R. ( 1984). The use of frequency-distributions in an attempt to detect host mortality induced by infections of diplostomatid metacercariae. Parasitology 89, 209220.
Kennedy, C. R. and Burrough, R. ( 1977). Population biology of 2 species of eyefluke, Diplostomum gasterostei and Tylodelphys clavata, in perch. Journal of Fish Biology 6, 619633.
Klein, J. ( 1986). Natural History of the Major Histocompatibility Complex. New York, Wiley.
Kraaijeveld, A. R. and Godfray, H. C. J. ( 2001). Is there local adaptation in Drosophila-parasitoid interactions? Evolutionary Ecology Research 3, 107116.
Kurtz, J. ( 2005). Specific memory within innate immune systems. Trends in Immunology 26, 186192.
Kurtz, J., Kalbe, M., Aeschlimann, P. B., Häberli, M. A., Wegner, K. M., Reusch, T. B. H. and Milinski, M. ( 2004). Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proceedings of the Royal Society of London, Series B 271, 197204.
Kurtz, J., Klappert, K., Schneider, W. and Reinhold, K. ( 2002). Immune defence, dispersal and local adaptation. Evolutionary Ecology Research 4, 431439.
Lajeunesse, M. J. and Forbes, M. R. ( 2002). Host range and local parasite adaptation. Proceedings of the Royal Society of London, Series B 269, 703710.
Lester, R. J. G. ( 1977). Estimate of mortality in a population of Perca flavescens owing to trematode Diplostomum adamsi. Canadian Journal of Zoology 55, 288292.
Lindström, K. M., Foufopoulos, J., Parn, H. and Wikelski, M. ( 2004). Immunological investments reflect parasite abundance in island populations of Darwin's finches. Proceedings of the Royal Society of London, Series B 271, 15131519.
Lively, C. M. ( 1989). Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43, 16631671.
Lively, C. M. and Dybdahl, M. F. ( 2000). Parasite adaptation to locally common host genotypes. Nature, London 405, 679681.
Lyholt, H. C. K. and Buchmann, K. ( 1996). Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Diseases of Aquatic Organisms 25, 169173.
McCoy, K. D., Boulinier, T., Schjørring, S. and Michalakis, Y. ( 2002). Local adaptation of the ectoparasite Ixodes uriae to its seabird host. Evolutionary Ecology Research 4, 441456.
McKeown, C. A. and Irwin, S. W. B. ( 1997). Accumulation of Diplostomum spp. (Digenea: Diplostomatidae) metacercariae in the eyes of 0+ and 1+ roach (Rutilus rutilus). International Journal for Parasitology 27, 377380.
Mutikainen, P., Salonen, V., Puustinen, S. and Koskela, T. ( 2000). Local adaptation, resistance, and virulence in a hemiparasitic plant-host plant interaction. Evolution 54, 433440.
Niewiadomska, K. ( 1984). Present status of Diplostomum spathaceum (Rudolphi, 1819) and differentiation of Diplostomum pseudospathaceum nom-nov (Trematoda, Diplostomatidae). Sytematic Parasitology 6, 8186.
Oppliger, A., Vernet, R. and Baez, M. ( 1999). Parasite local maladaptation in the Canarian lizard Gallotia galloti (Reptilia: Lacertidae) parasitized by haemogregarian blood parasite. Journal of Evolutionary Biology 12, 951955.
Owen, S. F., Barber, I. and Hart, P. J. B. ( 1993). Low-level infection by eye fluke, Diplostomum spp., affects the vision of 3-spined sticklebacks, Gasterosteus aculeatus. Journal of Fish Biology 42, 803806.
Pechhold, K., Pohl, T. and Kabelitz, D. ( 1994). Rapid quantification of lymphocyte subsets in heterogeneous cell-populations by flow-cytometry. Cytometry 16, 152159.
Pennycuick, L. ( 1971). Frequency distributions of parasites in a population of 3-spined sticklebacks, Gasterosteus aculeatus L, with particular reference to negative binomial distribution. Parasitology 63, 389406.
Press, C. M. and Evensen, O. ( 1999). The morphology of the immune system in teleost fishes. Fish and Shellfish Immunology 9, 309318.
Ratanarat-Brockelmann, C. ( 1974). Migration of Diplostomum spathaceum (Trematoda) in fish intermediate host. Zeitschrift für Parasitenkunde 43, 123134.
Rauch, G., Kalbe, M. and Reusch, T. B. H. ( 2005). How a complex life cycle can improve a parasite's sex life. Journal of Evolutionary Biology 18, 10691075.
Reusch, T. B. H., Wegner, K. M. and Kalbe, M. ( 2001). Rapid genetic divergence in postglacial populations of threespine stickleback (Gasterosteus aculeatus): the role of habitat type, drainage and geographical proximity. Molecular Ecology 10, 24352445.
Scharsack, J. P., Kalbe, M., Derner, R., Kurtz, J. and Milinski, M. ( 2004). Modulation of granulocyte responses in three-spined sticklebacks Gasterosteus aculeatus infected with the tapeworm Schistocephalus solidus. Diseases of Aquatic Organisms 59, 141150.
Scott, A. L. and Klesius, P. H. ( 1981). Chemiluminescence: a novel analysis of phagocytosis in fish. Development of Biological Standards 49, 243254.
Seppälä, O., Karvonen, A. and Valtonen, E. T. ( 2004). Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke – fish interaction. Animal Behaviour 68, 257263.
Sinyakov, M. S., Dror, M., Zhevelev, H. M., Margel, S. and Avtalion, R. R. ( 2002). Natural antibodies and their significance in active immunization and protection against a defined pathogen in fish. Vaccine 20, 36683674.
Sweeting, R. A. ( 1974). Investigations into natural and experimental infections of freshwater fish by common eye-fluke Diplostomum spathaceum Rud. Parasitology 69, 291300.
Thrall, P. H., Burdon, J. J. and Bever, J. D. ( 2002). Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution 56, 13401351.
Van Valen, L. ( 1973). A new evolutionary law. Evolutionary Theory 1, 130.
Wegner, K. M., Reusch, T. B. H. and Kalbe, M. ( 2003 a). Multiple parasites are driving major histocompatibility complex polymorphism in the wild. Journal of Evolutionary Biology 16, 224232.
Wegner, K. M., Kalbe, M., Kurtz, J., Reusch, T. B. H. and Milinski, M. ( 2003 b). Parasite selection for immunogenetic optimality. Science 301, 1343.
Whyte, S. K., Allan, J. C., Secombes, C. J. and Chappell, L. H. ( 1987). Cercariae and diplostomules of Diplostomum spathaceum (Digenea) elicit an immune-response in rainbow trout, Salmo gairdneri Richardson. Journal of Fish Biology 31, 185190.
Whyte, S. K., Chappell, L. H. and Secombes, C. J. ( 1989). Cytotoxic reactions of rainbow trout, Salmo gairdneri Richardson, macrophages for larvae of the eye fluke Diplostomum spathaceum (Digenea). Journal of Fish Biology 35, 333345.
Whyte, S. K., Secombes, C. J. and Chappell, L. H. ( 1991). Studies on the infectivity of Diplostomum spathaceum in rainbow trout (Oncorhynchus mykiss). Journal of Helminthology 65, 169178.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 4
Total number of PDF views: 42 *
Loading metrics...

Abstract views

Total abstract views: 177 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 21st October 2017. This data will be updated every 24 hours.