Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-26T09:20:31.588Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  13 September 2005

M. KALBE  and
J. KURTZ
M. KALBE
Affiliation:
Max Planck Institute for Limnology, Department of Evolutionary Ecology, August-Thienemann-Strasse 2, D-24306 Plön, Germany
J. KURTZ
Affiliation:
Max Planck Institute for Limnology, Department of Evolutionary Ecology, August-Thienemann-Strasse 2, D-24306 Plön, Germany Present address: Experimental Ecology, Universitätsstrasse 16, ETH-Zentrum, CHN JR.1, CH-8092 Zürich, Switzerland.
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

parasite-host coevolutionlocal adaptationfishinnate immunityrespiratory burstacquired immunityhybridhabitat
Type
Research Article
Information
Parasitology , Volume 132 , Issue 1 , January 2006 , pp. 105 - 116
Copyright
© 2005 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

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, 611–632.Google Scholar
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, 84–90.CrossRefGoogle Scholar
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, 489–493.CrossRefGoogle Scholar
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, 193–195.CrossRefGoogle Scholar
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. 59–86. 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, 775–787.CrossRefGoogle Scholar
Criscione, C. D. and Blouin, M. S. ( 2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198–202.CrossRefGoogle Scholar
Crowden, A. E. and Broom, D. M. ( 1980). Effects of the eyefluke, Diplostomum spathaceum, on the behavior of dace (Leuciscus leuciscus). Animal Behaviour 28, 287–294.CrossRefGoogle Scholar
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, 505–510.CrossRefGoogle Scholar
Ebert, D. ( 1994). Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 1084–1086.CrossRefGoogle Scholar
Ebert, D. and Hamilton, W. D. ( 1996). Sex against virulence: the coevolution of parasitic diseases. Trends in Evolutionary Ecology 11, A79–A82.CrossRefGoogle Scholar
Flajnik, M. F. and DuPasquier, L. ( 2004). Evolution of innate and adaptive immunity: can we draw a line? Trends in Immunology 25, 640–644.Google Scholar
Frischknecht, M. ( 1993). The breeding coloration of male 3-spined sticklebacks (Gasterosteus aculeatus) as an indicator of energy investment in vigor. Evolutionary Ecology 7, 439–450.CrossRefGoogle Scholar
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, 491–498.Google Scholar
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, 595–600.CrossRefGoogle Scholar
Höglund, J. and Thuvander, A. ( 1990). Indications of nonspecific protective mechanisms in rainbow-trout Oncorhynchus mykiss with diplostomosis. Diseases of Aquatic Organisms 8, 91–97.CrossRefGoogle Scholar
Imhoof, B. and Schmid-Hempel, P. ( 1998). Patterns of local adaptation of a protozoan parasite to its bumblebee host. Oikos 82, 59–65.CrossRefGoogle Scholar
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, 1529–1542.CrossRefGoogle Scholar
Kaltz, O. and Shykoff, J. A. ( 1998). Local adaptation in host-parasite systems. Heredity 81, 361–370.CrossRefGoogle Scholar
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, 850–860.CrossRefGoogle Scholar
Karvonen, A., Paukku, S., Seppälä, O. and Valtonen, E. T. ( 2005). Resistance against eye flukes: naive versus previously infected fish. Parasitology Research 95, 55–59.CrossRefGoogle Scholar
Kennedy, C. R. ( 1984). The use of frequency-distributions in an attempt to detect host mortality induced by infections of diplostomatid metacercariae. Parasitology 89, 209–220.CrossRefGoogle Scholar
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, 619–633.CrossRefGoogle Scholar
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, 107–116.Google Scholar
Kurtz, J. ( 2005). Specific memory within innate immune systems. Trends in Immunology 26, 186–192.CrossRefGoogle Scholar
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, 197–204.CrossRefGoogle Scholar
Kurtz, J., Klappert, K., Schneider, W. and Reinhold, K. ( 2002). Immune defence, dispersal and local adaptation. Evolutionary Ecology Research 4, 431–439.Google Scholar
Lajeunesse, M. J. and Forbes, M. R. ( 2002). Host range and local parasite adaptation. Proceedings of the Royal Society of London, Series B 269, 703–710.CrossRefGoogle Scholar
Lester, R. J. G. ( 1977). Estimate of mortality in a population of Perca flavescens owing to trematode Diplostomum adamsi. Canadian Journal of Zoology 55, 288–292.CrossRefGoogle Scholar
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, 1513–1519.CrossRefGoogle Scholar
Lively, C. M. ( 1989). Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43, 1663–1671.CrossRefGoogle Scholar
Lively, C. M. and Dybdahl, M. F. ( 2000). Parasite adaptation to locally common host genotypes. Nature, London 405, 679–681.CrossRefGoogle Scholar
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, 169–173.CrossRefGoogle Scholar
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, 441–456.Google Scholar
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, 377–380.Google Scholar
Mutikainen, P., Salonen, V., Puustinen, S. and Koskela, T. ( 2000). Local adaptation, resistance, and virulence in a hemiparasitic plant-host plant interaction. Evolution 54, 433–440.Google Scholar
Niewiadomska, K. ( 1984). Present status of Diplostomum spathaceum (Rudolphi, 1819) and differentiation of Diplostomum pseudospathaceum nom-nov (Trematoda, Diplostomatidae). Sytematic Parasitology 6, 81–86.CrossRefGoogle Scholar
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, 951–955.CrossRefGoogle Scholar
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, 803–806.Google Scholar
Pechhold, K., Pohl, T. and Kabelitz, D. ( 1994). Rapid quantification of lymphocyte subsets in heterogeneous cell-populations by flow-cytometry. Cytometry 16, 152–159.CrossRefGoogle Scholar
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, 389–406.CrossRefGoogle Scholar
Press, C. M. and Evensen, O. ( 1999). The morphology of the immune system in teleost fishes. Fish and Shellfish Immunology 9, 309–318.CrossRefGoogle Scholar
Ratanarat-Brockelmann, C. ( 1974). Migration of Diplostomum spathaceum (Trematoda) in fish intermediate host. Zeitschrift für Parasitenkunde 43, 123–134.CrossRefGoogle Scholar
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, 1069–1075.CrossRefGoogle Scholar
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, 2435–2445.CrossRefGoogle Scholar
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, 141–150.CrossRefGoogle Scholar
Scott, A. L. and Klesius, P. H. ( 1981). Chemiluminescence: a novel analysis of phagocytosis in fish. Development of Biological Standards 49, 243–254.Google Scholar
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, 257–263.CrossRefGoogle Scholar
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, 3668–3674.CrossRefGoogle Scholar
Sweeting, R. A. ( 1974). Investigations into natural and experimental infections of freshwater fish by common eye-fluke Diplostomum spathaceum Rud. Parasitology 69, 291–300.CrossRefGoogle Scholar
Thrall, P. H., Burdon, J. J. and Bever, J. D. ( 2002). Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution 56, 1340–1351.Google Scholar
Van Valen, L. ( 1973). A new evolutionary law. Evolutionary Theory 1, 1–30.Google Scholar
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, 224–232.Google Scholar
Wegner, K. M., Kalbe, M., Kurtz, J., Reusch, T. B. H. and Milinski, M. ( 2003 b). Parasite selection for immunogenetic optimality. Science 301, 1343.Google Scholar
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, 185–190.CrossRefGoogle Scholar
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, 333–345.CrossRefGoogle Scholar
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, 169–178.CrossRefGoogle Scholar