Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

Invertebrate immunity and the limits of mechanistic immunology

Nature Immunology volume 6, pages 651–654 (2005)Cite this article

Abstract

Rapid progress is being made in elucidating the molecular mechanisms involved in invertebrate immunity. This search for molecules runs the risk of missing important phenomena. In vertebrates, acquired protection and pathogen-specific responses were demonstrated experimentally long before the mechanisms responsible were elucidated. Without analogous experiments, mechanism-driven work may not demonstrate the full richness of invertebrate immunity.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: How to determine what an invertebrate immune system can do.
Figure 2: How to determine the level of genetic specificity in an invertebrate host-pathogen interaction.

Similar content being viewed by others

References

  1. Kurtz, J. Memory in the innate and adaptive immune systems. Microbes Infect. 6, 1410–1417 (2004).

    Article  Google Scholar 

  2. Christophides, G.K. et al. Immunity-related genes and gene families in Anopheles gambiae. Science 298, 159–165 (2002).

    Article  CAS  Google Scholar 

  3. Choe, K.M., Werner, T., Stoven, S., Hultmark, D. & Anderson, K.V. Requirement for a peptidoglycan recognition protein (PGRP) in relish activation and antibacterial immune responses in Drosophila. Science 296, 359–362 (2002).

    Article  CAS  Google Scholar 

  4. Hoffman, J.A. Primitive immune systems. Immunol. Rev. 198, 5–9 (2004).

    Article  Google Scholar 

  5. Hoffmann, J.A., Kafatos, F.C., Janeway, C.A. & Ezekowitz, R.A.B. Phylogenetic perspectives in innate immunity. Science, 1313–1318 (1999).

  6. Kush, R.S., Leulier, F.L. & Lemaitre, B. Pathogen Surveillance- the flies have it. Science 296, 273–275 (2002).

    Article  Google Scholar 

  7. Tzou, P., De Gregorio, E. & Lemaitre, B. How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Curr. Opin. Microbiol. 5, 102–110 (2002).

    Article  CAS  Google Scholar 

  8. Cooper, E.L. & Roch, P. Second-set allograft responses in the earthworm Lumbricu terrestris. Transplantation 4, 514–520 (1986).

    Article  Google Scholar 

  9. Hartman, R.S. & Karp, R.D. Short-term immunologic memory in the allograft response of the American cockroach, Periplaneta americana. Transplantation 37, 478–484 (1989).

    Google Scholar 

  10. Hildemann, W.H., Johnson, I.S. & Jokiel, P.L. Immunocompetence in the lowest metazoan phylum–transplantation immunity in sponges. Science 204, 420–422 (1979).

    Article  CAS  Google Scholar 

  11. Hildemann, W.H. et al. Immunological specificity and memory in a scleractinian coral. Nature 270, 219–223 (1977).

    Article  CAS  Google Scholar 

  12. Smith, V.J., Brown, J.H. & Hauton, C. Immunostimulation in crustaceans: does it really protect against infection? Fish Shellfish Immunol. 15, 71–90 (2003).

    Article  Google Scholar 

  13. Moret, Y. & Siva-Jothy, M.T. Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc. Roy. Soc. Lond. B 270, 2475–2780 (2003).

    Article  CAS  Google Scholar 

  14. Huang, C.-C. & Song, Y.-L. Maternal transmission of immunity to white spot syndrome associated virus (WSSD) in shrimp (Penaeus monodon). Dev. Comp. Immunol. 23, 545–552 (1999).

    Article  CAS  Google Scholar 

  15. Moret, Y. & Schmid-Hempel, P. Immune defence in bumble-bee offspring. Nature 414, 506–506 (2001).

    Article  CAS  Google Scholar 

  16. Rahman, M.M., Roberts, H.L.S., Sarjan, M., Asgari, S. & Schmidt, O. Induction and transmission of Bacillus thuringiensis tolerance in the flour moth Ephestia kuehniella. Proc. Natl. Acad. Sci. USA 101, 2696–2699 (2004).

    Article  CAS  Google Scholar 

  17. Rosengaus, R.B., Traniello, J.F.A., Chen, T., Brown, J.J. & Karp, R.D. Immunity in a social insect. Naturwissenschaften 86, 588–591 (1999).

    Article  CAS  Google Scholar 

  18. Kurtz, J. & Franz, K. Evidence for memory in invertebrate immunity. Nature 425, 37–38 (2003).

    Article  CAS  Google Scholar 

  19. Little, T.J., O'Connor, B., Colegrave, N., Watt, K. & Read, A.F. Maternal transfer of strain-specific immunity in an invertebrate. Curr. Biol. 13, 489–492 (2003).

    Article  CAS  Google Scholar 

  20. Witteveldt, J., Cifuentes, C.C., Vlak, J.M. & Van Hulten, M.C.W. Protection of Panaeus monodon against white spot syndrom virus by oral vaccination. J. Virol. 78, 2057–2061 (2004).

    Article  CAS  Google Scholar 

  21. Rosengaus, R.B., Jordan, C., Lefebvre, M.L. & Traniello, J.F.A. Pathogen alarm behavior in a termite: A new form of communication in social insects. Naturwissenschaften 86, 544–548 (1999).

    Article  CAS  Google Scholar 

  22. Elliot, S.L., Blanford, S., Horton, C.M. & Thomas, M.B. Fever and phenotype: transgenerational effect of disease on desert locust phase state. Ecol. Lett. 6, 830–836 (2003).

    Article  Google Scholar 

  23. Traniello, J.F.A., Rosengaus, R.B. & Savoie, K. The development of immunity in a social insect: Evidence for the group facilitation of disease resistance. Proc. Natl. Acad. Sci. USA 99, 6838–6842 (2002).

    Article  CAS  Google Scholar 

  24. Barnes, A.I. & Siva-Jothy, M.T. Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L-(Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proc. Roy. Soc. Lond. B 267, 177–182 (2000).

    Article  CAS  Google Scholar 

  25. Little, T.J. & Kraaijeveld, A.R. The ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol. Evol. 19, 58–60 (2004).

    Article  Google Scholar 

  26. SchmidHempel, P., Puhr, K., Kruger, N., Reber, C. & SchmidHempel, R. Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution 53, 426–434 (1999).

    Article  Google Scholar 

  27. Carius, H.-J., Little, T.J. & Ebert, D. Genetic variation in a host–parasite association: Potential for coevolution and frequency dependent selection. Evolution 55, 1136–1145 (2001).

    Article  CAS  Google Scholar 

  28. Wedekind, C. & Ruetschi, A. Parasite heterogeneity affects infection success and the occurrence of within-host competition: An experimental study with a cestode. Evol. Ecol. Res. 2, 1031–1043 (2000).

    Google Scholar 

  29. Decaestecker, E., Vergote, A., Ebert, D. & De Meester, L. Evidence for strong host-clone-parasite species interactions in the Daphnia microparasite system. Evolution 57, 784–792 (2003).

    Article  Google Scholar 

  30. Schmid-Hempel, P. & Ebert, D. On the evolutionary ecology of specific immune defence. Trends Ecol. Evol. 18, 27–32 (2003).

    Article  Google Scholar 

  31. Klein, J. Homology between immune responses in vertebrates and invertebrates: Does it exist? Scand. J. Immunol. 46, 558–564 (1997).

    Article  CAS  Google Scholar 

  32. Michel, T., Reichhart, J.-M., Hoffmann, J.A. & Royet, J. Drosophila Toll is activated by Gram-positive bacteria through a circulating peptidoglycan recognition protein. Nature 414, 756–759 (2001).

    Article  CAS  Google Scholar 

  33. Vivier, E. & Malissen, B. Innate and adaptive immunity: specificities and signalling heirarchies revisited. Nat. Immunol. 6, 17–21 (2004).

    Article  Google Scholar 

  34. Hultmark, D. Drosophila immunity: paths and patterns. Curr. Opin. Immunol. 15, 12–19 (2003).

    Article  CAS  Google Scholar 

  35. Thompson, J.N. & Burdon, J.J. Gene-for-gene coevolution between plants and parasites. Nature 360, 121–125 (1992).

    Article  Google Scholar 

  36. Dangle, J.L. & Jones, J.D.G. Plant pathogens and integrated defence in plants. Nature 411, 826–833 (2001).

    Article  Google Scholar 

  37. Bergelson, J., Kreitman, M., Stahl, E.A. & Tian, D.C. Evolutionary dynamics of plant R-genes. Science 292, 2281–2285 (2001).

    Article  CAS  Google Scholar 

  38. Rathjen, J.P. & Moffett, P. Early signal transduction events in specific plant disease resistance. Curr. Opin. Plant Biol. 6, 300–306 (2003).

    Article  CAS  Google Scholar 

  39. Allen, R.L. et al. Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306, 1957–1960 (2004).

    Article  CAS  Google Scholar 

  40. Basset, A., Tzou, P., Lemaitre, B. & Boccard, F. A single gene that promotes interaction of a phytopathogenic bacterium with its insect vector, Drosophila melanogaster. EMBO Rep. 4, 205–209 (2003).

    Article  CAS  Google Scholar 

  41. Lambrechts, L., Halbert, J., Durand, P., Gouagna, L.C. & Koella, J.C. Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malar. J. 4, 3 (2005).

    Article  Google Scholar 

  42. Christophides, G.K., Vlachou, D. & Kafatos, F.C. Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol. Rev. 198, 127–148 (2004).

    Article  CAS  Google Scholar 

  43. Brandt, S.M. et al. Secreted bacterial effectors and host-produced eiger/TNF drive death in a Salmonella-infected fruit fly. PLoS. Biol. 2, 2067–2075 (2004).

    Article  CAS  Google Scholar 

  44. Pancer, Z. et al. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 420, 174–180 (2004).

    Article  Google Scholar 

  45. Zhang, S.M., Adema, C.M., Kepler, T.B. & Loker, E.S. Diversification of Ig superfamily genes in an invertebrate. Science 305, 251–254 (2004).

    Article  CAS  Google Scholar 

  46. Little, T.J., Colbourne, J.K. & Crease, T.J. Molecular evolution of Daphnia immunity genes: polymorphism in a Gram negative binding protein and an α-2-macroglobulin. J. Mol. Evol. 59, 498–506 (2004).

    Article  CAS  Google Scholar 

  47. Lazzaro, B.P., Sceurman, B.K. & Clark, A.G. Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science 303, 1873–1876 (2004).

    Article  CAS  Google Scholar 

  48. Schlenke, T.A. & Begun, D.J. Natural selection drives Drosophila immune system evolution. Genetics 164, 1471–1480 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Levashina, E.A. et al. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104, 709–718 (2001).

    Article  CAS  Google Scholar 

  50. Osta, M.A., Christophides, G.K. & Kafatos, F.C. Effects of mosquito genes on Plasmosium development. Science 303, 2030–2032 (2004).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank A. Graham, A. Hayward and L. Råberg for comments. Supported by the University of Edinburgh School of Biological Sciences, Wellcome Trust and Natural Environment Research Council (T.L.); the Swedish Research Council, Swedish Cancer Society, Swedish Foundation for Strategic Research and Wallenberg Consortium North (D.H.); and the Wellcome Trust and Biotechnology and Biological Sciences Research Council (A.R.).

Author information

Authors and Affiliations

  1. Institute of Evolutionary Biology,

    Tom J Little & Dan Hultmark

  2. Institute of Immunology and Infection Research, School of Biology, University of Edinburgh, Kings Buildings, Edinburgh, EH9 3JT, UK

    Tom J Little & Dan Hultmark

  3. Umeå Center for Molecular Pathogenesis, Umeå University, Umeå, S-90187, Sweden

    Andrew F Read

Authors
  1. Tom J Little
    View author publications

    Search author on:PubMed Google Scholar

  2. Dan Hultmark
    View author publications

    Search author on:PubMed Google Scholar

  3. Andrew F Read
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Tom J Little.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Little, T., Hultmark, D. & Read, A. Invertebrate immunity and the limits of mechanistic immunology. Nat Immunol 6, 651–654 (2005). https://doi.org/10.1038/ni1219

Download citation

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/ni1219

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing