Evolutionary Ecology

, Volume 21, Issue 4, pp 473–483 | Cite as

Innate versus adaptive immunity in sticklebacks: evidence for trade-offs from a selection experiment

  • K. Mathias Wegner
  • Martin Kalbe
  • Thorsten B. H. Reusch
Original Paper

Abstract

In vertebrates, the immune system consists of two arms of different characteristics: the innate and the acquired immune response. Parasites that are only shortly exposed to the immune system are most efficiently attacked by fast, constitutive innate immune mechanisms. Here, we experimentally selected within four fish families for high innate resistance versus susceptibility of three-spined sticklebacks (Gasterosteus aculeatus) against infection with the eye-fluke (Diplostomum pseudospathacaeum), a parasite whose metacercariae are protected from the immune system within the eye lens. We predicted that in families with high susceptibility, the adaptive immune system would be upregulated when challenged with infection. In accordance, we found that MHC class IIB expression is increased by approximately 50% in those lines selected for higher parasite load (i.e. low innate response). This suggests extensive genetic correlations between innate and adaptive immune system and/or crosstalk between both lines of defense. An efficient, specific innate immune response might reduce overall activation of the immune system and potentially alleviate associated effects of immunopathology.

Keywords

Major histocompatibility complex (MHC) Ecological immunity Innate resistance Adaptive immunity Gene expression Three-spined stickleback (Gasterosteus aculeatusParasites Artificial selection 

References

  1. Agrawal AF, Lively CM (2002) Infection genetics: gene-for-gene versus matching alleles models and all points in between. Evol Ecol Res 4:79–90Google Scholar
  2. Bernatchez L, Landry C (2003) MHC studies in non-model vertebrates: what have we learned about natural selection in 15 years?. J Evol Biol 16:363–377PubMedCrossRefGoogle Scholar
  3. Bogdan C, Rollinghoff M, Diefenbach A (2000) Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 12:64–67PubMedCrossRefGoogle Scholar
  4. Briles WE, Stone HA, Cole RK (1977) Mareks-Disease—effects of B-histocompatibility alloalleles in resistant and susceptible chicken lines. Science 195(4274):193–195PubMedCrossRefGoogle Scholar
  5. Crowden AE, Broom DM (1980) Effects of the eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus leuciscus). Anim Behav 28:287–294CrossRefGoogle Scholar
  6. Decamposlima PO, Gavioli R, Zhang QJ, Wallace LE, Dolcetti R, Rowe M, Rickinson AB, Masucci MG (1993) Hla-A11 epitope loss isolates of Epstein-Barr-virus from a highly A11+ population. Science 260(5104):98–100CrossRefGoogle Scholar
  7. Dixon B, Stet RJM (2001) The relationship between major histocompatibility receptors and innate immunity in teleost fish. Dev Comp Immunol 25(8–9):683–699PubMedCrossRefGoogle Scholar
  8. Dybdahl MF, Lively CM (1998) Host-parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution 52(4):1057–1066CrossRefGoogle Scholar
  9. Dybdahl MF, Storfer A. (2003) Parasite local adaptation: Red queen versus suicide king. Trends Ecol Evol 18(10):523–530CrossRefGoogle Scholar
  10. Godot V, Harraga S, Beurton I, Tiberghien P, Sarciron E, Gottstein B, Vuitton DA (2000) Resistance/susceptibility to Echinococcus multilocularis infection and cytokine profile in humans. II. Influence of the HLA B8, DR3, DQ2 haplotype. Clin Exp Immunol 121(3):491–498PubMedCrossRefGoogle Scholar
  11. Goldstein DR (2004) Toll-like receptors and other links between innate and acquired alloimmunity. Curr Opin Immunol 16:538–544PubMedCrossRefGoogle Scholar
  12. Grimholt U, Larsen S, Nordmo R, Midtlyng P, Kjoeglum S, Storset A, Saebo S., Stet RJM (2003) MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 55(4):210–219PubMedCrossRefGoogle Scholar
  13. Haldane JBS (1949) Disease and evolution. Ric Sci 19(Suppl):68–75Google Scholar
  14. Hamilton WD, Axelrod R, Tanese R (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proc Natl Acad Sci USA 87(9):3566–3573PubMedCrossRefGoogle Scholar
  15. Harf R, Sommer S (2005) Association between major histocompatibility complex class II DRB alleles and parasite load in the hairy-footed gerbil, Gerbillurus paeba, in the southern Kalahari. Mol Ecol 14(1):85–91PubMedCrossRefGoogle Scholar
  16. Hill AVS, Allsopp CEM, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA, Bennet S, Brewster D, McMichael AJ, Greenwood BM (1991) Common West African HLA antigens are associated with protection from severe malaria. Nature 352:595–600PubMedCrossRefGoogle Scholar
  17. Janeway CA, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216PubMedCrossRefGoogle Scholar
  18. Kalbe M, Kurtz J (2006) Local differences in immunocompetence reflect resistance of sticklebacks against the eye fluke Diplostomum pseudospathaceum. Parasitology 132:1–12CrossRefGoogle Scholar
  19. Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New YorkGoogle Scholar
  20. Kurtz J, Kalbe M, Aeschlimann P, Häberli M, Wegner KM, Reusch TBH, Milinski M (2004) Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc R Soc Lond Ser B Biol Sci 271(1535):197–204CrossRefGoogle Scholar
  21. Kurtz J, Wegner KM, Kalbe M, Reusch TBH, Schaschl H, Hasselquist D, Milinski M (2006) MHC genes and oxidative stress in sticklebacks—an immuno-ecological approach. Proc R Soc Lond Ser B Biol Sci 273:1407–1414CrossRefGoogle Scholar
  22. Langefors Å, Lohm J, Grahn M, Andersen Ö, von Schantz T (2001) Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc R Soc Lond Ser Biol Sci 268:479–485CrossRefGoogle Scholar
  23. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 CT method. Methods 25(4):402–408PubMedCrossRefGoogle Scholar
  24. Medzhitov R, Janeway CA (1997) Innate immunity: impact on the adaptive immune response. Curr Opin Immunol 9(1):4–9PubMedCrossRefGoogle Scholar
  25. Owen SF, Barber I, Hart PJB (1993) Low level infection by eye fluke, Diplostomum ssp., affects the vision of three-spined sticklebacks, Gasterosteus aculeatus. J Fish Biol 42:803–806CrossRefGoogle Scholar
  26. Parham P (2003) Innate immunity: the unsung heroes. Nature 423(6935):20PubMedCrossRefGoogle Scholar
  27. Peichel CL, Nereng KS, Ohgi KA, Cole BLE, Colosimo PF, Buerkle CA, Schluter D, Kingsley DM (2001) The genetic architecture of divergence between threespine stickleback species. Nature 414(6866):901–905PubMedCrossRefGoogle Scholar
  28. Rauch G, Kalbe M, Reusch TBH (2005) How a complex life cycle can improve a parasite’s sex life. J Evol Biol 18(4):1069–1075PubMedCrossRefGoogle Scholar
  29. Rauch G, Kalbe M, Reusch TBH (2006) One day is enough: rapid and specific interactions between stickleback hosts and a trematode parasite. Biol Lett (2):382–384PubMedCrossRefGoogle Scholar
  30. Schmid-Hempel P, Ebert D (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18(1):27–32CrossRefGoogle Scholar
  31. Seppala O, Karvonen A, Valtonen ET (2004) Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Anim Behav 68(2):257–263CrossRefGoogle Scholar
  32. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11(8):317–321CrossRefGoogle Scholar
  33. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman & Co, New YorkGoogle Scholar
  34. Thompson JN, Burdon JJ (1992) Gene-for-gene coevolution between plants and parasites. Nature 360:121–125CrossRefGoogle Scholar
  35. Wegner KM, Kalbe M, Kurtz J, Reusch TBH, Milinski M (2003) Parasite selection for immunogenetic optimality. Science 301:1343PubMedCrossRefGoogle Scholar
  36. Wegner KM, Kalbe M, Rauch G, Kurtz J, Schaschl H, Reusch TBH (2006) Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Mol Ecol 15(4):1153–1164PubMedCrossRefGoogle Scholar
  37. Whyte SK, Allan JC, Secombes CJ, Chappell LH (1987) Cercariae and diplostomules of Diplostomum spathaceum (Digenea) elicit an immune response in rainbow trout, Salmo gairdneri Richardson. J Fish Biol 31:185–190CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • K. Mathias Wegner
    • 1
    • 2
  • Martin Kalbe
    • 1
  • Thorsten B. H. Reusch
    • 1
    • 3
  1. 1.Max-Planck-Institute of LimnologyPlönGermany
  2. 2.Institute of Integrative Biology, Experimental EcologyETH Zürich Universitätstrasse 16 CHN H72ZürichSwitzerland
  3. 3.Institute for Evolution and BiodiversityUniversity of MünsterMünsterGermany

Personalised recommendations