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Evolution of virulence: triggering host inflammation allows invading pathogens to exclude competitors

  1. Sam P. Brown1,2,*,
  2. Ludovic Le Chat3,
  3. François Taddei4

Article first published online: 16 NOV 2007

DOI: 10.1111/j.1461-0248.2007.01125.x

Issue

Ecology Letters

Ecology Letters

Volume 11, Issue 1, pages 44–51, January 2008

Additional Information

How to Cite

Brown, S. P., Le Chat, L. and Taddei, F. (2008), Evolution of virulence: triggering host inflammation allows invading pathogens to exclude competitors. Ecology Letters, 11: 44–51. doi: 10.1111/j.1461-0248.2007.01125.x

Author Information

  1. 1

    Section of Integrative Biology, University of Texas at Austin, Austin, TX 78712, USA

  2. 2

    Department of Zoology, University of Oxford, South Parks Rd, Oxford OX1 3PS, UK

  3. 3

    London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK

  4. 4

    University of Paris 5, Faculty of Medicine, INSERM, U571, 156 Rue de Vaugirard, F-75730 Paris 15, France

**Correspondence: E-mail: sam.brown@cantab.net

  1. Reuse of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

Publication History

  1. Issue published online: 16 NOV 2007
  2. Article first published online: 16 NOV 2007
  3. Editor, Minus van BaalenManuscript received 19 July 2007First decision made 28 August 2007 Manuscript accepted 2 October 2007

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References

  • Alizon, S. (2006). Parasite virulence evolution: insights from embedded models (unpublished thesis). University of Paris 6, Paris, France.
  • Alizon, S. & Van Baalen, M. (2005). Emergence of a convex trade-off between transmission and virulence. Am. Nat., 165, E155–E167.
  • Anderson, R.M. & May, R.M. (1991). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford.
  • Andre, J.B. & Gandon, S. (2006). Vaccination, within-host dynamics, and virulence evolution. Evolution, 60, 13–23.
  • Antia, R., Regoes, R.R., Koella, J.C. & Bergstrom, C.T. (2003). The role of evolution in the emergence of infectious diseases. Nature, 426, 658–661.
  • Van Baalen, M. & Jansen, V.A.A. (2001). Dangerous liaisons: the ecology of private interest and common good. Oikos, 95, 211–224.
    Direct Link:
  • Van Baalen, M. & Sabelis, M.W. (1995). The dynamics of multiple infection and the evolution of virulence. Am. Nat., 146, 881–910.
  • Bae, T., Baba, T., Hiramatsu, K. & Schneewind, O. (2006). Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol. Microbiol., 62, 1035–1047.
    Direct Link:
  • Brown, S.P. & Grenfell, B.T. (2001). An unlikely partnership: parasites, concomitant immunity and host defence. Proc. Biol. Sci., 268, 2543–2549.
  • Brown, S.P. & Taddei, F. (2007). The durability of public goods changes the dynamics and nature of social dilemmas. PLoS ONE, 2, e593.
  • Brown, S.P., Hochberg, M.E. & Grenfell, B.T. (2002). Does multiple infection select for raised virulence? Trends Microbiol., 10, 401–405.
  • Brown, S.P., Le Chat, L., De Paepe, M. & Taddei, F. (2006a). Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare. Curr. Biol., 16, 2048–2052.
  • Brown, S.P., Cornell, S.J., Sheppard, M., Grant, A.J., Maskell, D.J., Grenfell, B.T. et al. (2006b). Intracellular demography and the dynamics of Salmonella enterica infections. PLoS Biol., 4, e349.
  • Bull, J.J. (1994). Perspective: virulence. Evolution, 48, 1423–1437.
  • Czaran, T.L. & Hoekstra, R.F. (2003). Killer-sensitive coexistence in metapopulations of micro-organisms. Proc. Biol. Sci., 270, 1373–1378.
  • Dawkins, R. (1982). The Extended Phenotype. Freeman, San Francisco.
  • Dillon, R.J., Vennard, C.T., Buckling, A. & Charnley, A.K. (2005). Diversity of locust gut bacteria protects against pathogen invasion. Ecol. Lett., 8, 1291–1298.
    Direct Link:
  • Durrett, R. & Levin, S. (1997). Allelopathy in Spatially Distributed Populations. J. Theor. Biol., 185, 165–171.
  • Fitter, A. (2003). Ecology. Making allelopathy respectable. Science, 301, 1337–1338.
  • Frank, S.A. (1994). Spatial polymorphism of bacteriocins and other allelopathic traits. Evol. Ecol., 8, 369–386.
  • Frank, S.A. (1996). Models of Parasite Virulence. Q. Rev. Biol., 71, 37–78.
  • Ganusov, V.V., Bergstrom, C.T. & Antia, R. (2002). Within-host population dynamics and the evolution of microparasites in a heterogeneous host population. Evolution, 56, 213–223.
  • Gilchrist, M.A. & Coombs, D. (2006). Evolution of virulence: interdependence, constraints, and selection using nested models. Theor. Popul. Biol., 69, 145–153.
  • Gordon, D.M. & Riley, M.A. (1999). A theoretical and empirical investigation of the invasion dynamics of colicinogeny. Microbiology, 145, 655–661.
  • Graham, A.L. (2002). When T-helper cells don’t help: immunopathology during concomitant infection. Q. Rev. Biol., 77, 409–434.
  • Graham, A.L., Allen, J.E. & Read, A.F. (2005). Evolutionary causes and consequences of immunopathology. Annu. Rev. Ecol. Evol. Syst., 36, 373–397.
  • Harrison, F., Browning, L.E., Vos, M. & Buckling, A. (2006). Cooperation and virulence in acute Pseudomonas aeruginosa infections. BMC Biol., 4, 21.
  • Hendrix, R.W., Lawrence, J.G., Hatfull, G.F. & Casjens, S. (2000). The origins and ongoing evolution of viruses. Trends Microbiol., 8, 504–508.
  • Hudault, S., Guignot, J. & Servin, A.L. (2001). Escherichia coli strains colonising the gastrointestinal tract protect germfree mice against Salmonella typhimurium infection. Gut, 49, 47–55.
  • Jones, C.G., Lawton, J.H. & Shachak, M. (1994). Organisms as ecosystem engineers. Oikos, 69, 373–386.
  • Kerr, B., Schwilk, D.W., Bergman, A. & Feldman, M.W. (1999). Rekindling an old flame: a haploid model for the evolution and impact of flammability in resprouting plants. Evol. Ecol. Res., 1, 807–833.
  • Kerr, B., Riley, M.A., Feldman, M.W. & Bohannan, B.J. (2002). Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature, 418, 171–174.
  • Kirkup, B. & Riley, M.A. (2004). Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vitro. Nature, 428, 412–414.
  • Lysenko, E.S., Ratner, A.J., Nelson, A.L. & Weiser, J.N. (2005). The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. PLoS Pathog., 1, e1.
  • Nowak, M.A. & May, R.M. (1994). Superinfection and the evolution of parasite virulence. Proc. Biol. Sci., 255, 81–89.
  • Odling-Smee, F.J., Laland, K.N. & Feldman, M.W. (2003). Niche Construction The Neglected Process in Evolution. Princeton University Press, Prineton and Oxford.
  • Ohnishi, M., Kurokawa, K. & Hayashi, T. (2001). Diversification of Escherichia coli genomes: are bacteriophages the major contributors? Trends Microbiol., 9, 481–485.
  • Otto, S.P. & Day, T. (2006). A Biologist’s Guide to Mathematical Modeling in Ecology and Evolution. Princeton University Press, Princeton.
  • Pedersen, A.B. & Fenton, A. (2007). Emphasizing the ecology in parasite community ecology. Trends Ecol. Evol., 22, 133–139.
  • Plunkett, G., Rose, D.J., Durfee, T.J. & Blattner, F.R. (1999). Sequence of Shiga toxin 2 phage 933W from Escherichia coli O157:H7: Shiga toxin as a phage late-gene product. J. Bacteriol., 181, 1767–1778.
  • Poitrineau, K., Brown, S.P. & Hochberg, M.E. (2004). The joint evolution of defence and inducibility against natural enemies. J. Theor. Biol., 231, 389–396.
  • Poulin, R. & Morand, S. (2004). Parasite Biodiversity. Smithsonian Institution Press, Washington, DC.
  • Raberg, L., De Roode, J.C., Bell, A.S., Stamou, P., Gray, D. & Read, A.F. (2006). The role of immune-mediated apparent competition in genetically diverse malaria infections. Am. Nat., 168, 41–53.
  • Riffkin, M., Seow, H.F., Jackson, D., Brown, L. & Wood, P. (1996). Defence against the immune barrage: helminth survival strategies. Immunol. Cell Biol., 74, 564–574.
  • Sansonetti, P.J. & Di Santo, J.P. (2007). Debugging how bacteria manipulate the immune response. Immunity, 26, 149–161.
  • Savage, D.C. (1977). Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol., 31, 107–133.
  • Shafikhani, S.H. & Engel, J. (2006). Pseudomonas aeruginosa type III-secreted toxin ExoT inhibits host-cell division by targeting cytokinesis at multiple steps. Proc. Natl. Acad. Sci. U.S.A., 103, 15605–15610.
  • Sokurenko, E.V., Gomulkiewicz, R. & Dykhuizen, D.E. (2006). Source-sink dynamics of virulence evolution. Nat. Rev. Microbiol., 4, 548–555.
  • Stecher, B., Robbiani, R., Walker, A.W., Westendorf, A.M., Barthel, M., Kremer, M. et al. (2007). Salmonella enterica serovar Typhimurium exploits host inflammation to compete with the intestinal microbiota. PLoS Biol., 5, e244.
  • West, S.A. & Buckling, A. (2003). Cooperation, virulence and siderophore production in bacterial parasites. Proc. Biol. Sci., 270, 37–44.
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