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Prisoner's dilemma in an RNA virus

Abstract

The evolution of competitive interactions among viruses1 was studied in the RNA phage φ6 at high and low multiplicities of infection (that is, at high and low ratios of infecting phage to host cells). At high multiplicities, many phage infect and reproduce in the same host cell, whereas at low multiplicities the viruses reproduce mainly as clones. An unexpected result of this study1 was that phage grown at high rates of co-infection increased in fitness initially, but then evolved lowered fitness. Here we show that the fitness of the high-multiplicity phage relative to their ancestors generates a pay-off matrix conforming to the prisoner's dilemma strategy of game theory2,3. In this strategy, defection (selfishness) evolves, despite the greater fitness pay-off that would result if all players were to cooperate. Viral cooperation and defection can be defined as, respectively, the manufacturing and sequestering of diffusible (shared) intracellular products. Because the low-multiplicity phage did not evolve lowered fitness, we attribute the evolution of selfishness to the lack of clonal structure and the mixing of unrelated genotypes at high multiplicity4,5,6.

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Figure 1: Expected and observed fitness values for a game in which opponents use conflicting strategies of cooperation and defection.
Figure 2: The fitness of derived high MOI phage relative to the ancestor is a decreasing function of initial frequency in competition.

References

  1. Turner, P. E. & Chao, L. Sex and the evolution of intrahost competition in RNA virus φ6. Genetics 150, 523–532 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981).

    ADS  MathSciNet  CAS  Article  Google Scholar 

  3. Maynard-Smith, J. Evolution and the Theory of Games(Cambridge Univ. Press, Cambridge, (1982)).

    Book  Google Scholar 

  4. Hamilton, W. D. Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3, 193–232 (1972).

    Article  Google Scholar 

  5. Frank, S. A. Akin selection model for the evolution of virulence. Proc. R. Soc. Lond. B 250, 195–197 (1992).

    ADS  CAS  Article  Google Scholar 

  6. Nowak, M. A. & May, R. M. Superinfection and the evolution of parasite virulence. Proc. R. Soc. Lond. B 255, 81–89 (1994).

    ADS  CAS  Article  Google Scholar 

  7. Craig, J. L. Are communal pukeko caught in a Prisoner's Dilemma? Behav. Ecol. Sociobiol. 14, 147–150 (1984).

    Article  Google Scholar 

  8. Fischer, E. A. Simultaneous hermaphroditism, Tit for Tat, and the evolutionary stability of social systems. Ethol. Sociobiol. 9, 119–136 (1988).

    Article  Google Scholar 

  9. Chao, L. Evolution of polyandry in a communal breeding system. Behav. Ecol. 8, 668–674 (1997).

    Article  Google Scholar 

  10. Dugatkin, L. A. Cooperation Among Animals: an Evolutionary Perspective(Oxford Univ. Press, Oxford, (1997)).

    Google Scholar 

  11. von Magnus, P. Incomplete forms of influenza virus. Adv. Virus Res. 2, 59–79 (1954).

    CAS  Article  Google Scholar 

  12. Lewontin, R. C. The units of selection. Annu. Rev. Ecol. Syst. 1, 1–18 (1970).

    Article  Google Scholar 

  13. Bonhoeffer, S. & Nowak, M. A. Intra-host and inter-host selection: viral evolution of immune function impairment. Proc. Natl Acad. Sci. USA 91, 8062–8066 (1994).

    ADS  CAS  Article  Google Scholar 

  14. Huang, A. S. & Baltimore, D. Defective viral particles and viral disease processes. Nature 226, 325–327 (1970).

    ADS  CAS  Article  Google Scholar 

  15. Holland, J. Fundamental Virology 2nd edn(eds Fields, B. & Knipe, D.) 151–165 (Raven, New York, (1991)).

    Google Scholar 

  16. Chao, L. The Evolutionary Biology of Viruses(ed. Morse, S. S.) 233–250 (Raven, New York, (1994)).

    Google Scholar 

  17. Mindich, L., Cohen, J. & Weisburd, M. Isolation of nonsense suppressor mutants in Pseudomonas. J.Bact. 126, 177–182 (1976).

    CAS  PubMed  Google Scholar 

  18. Stent, G. Molecular Biology of Bacterial Viruses(Freeman, San Francisco, (1963)).

    Google Scholar 

  19. Nowak, M. & May, R. Evolutionary games and spatial chaos. Nature 359, 826–829 (1992).

    ADS  Article  Google Scholar 

  20. Herre, E. A. Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 1442–1445 (1993).

    ADS  CAS  Article  Google Scholar 

  21. Frank, S. A. Models of parasite virulence. Q. Rev. Biol. 71, 37–78 (1996).

    CAS  Article  Google Scholar 

  22. Hamilton, W. D. The genetical evolution of social behavior: I and II. J. Theor. Biol. 7, 1–52 (1964).

    CAS  Article  Google Scholar 

  23. Bremermann, H. J. & Pickering, J. Agame-theoretical model of parasite virulence. J. Theor. Biol. 100, 411–426 (1983).

    CAS  Article  Google Scholar 

  24. Knolle, H. Host density and the evolution of parasite virulence. J. Theor. Biol. 136, 199–207 (1989).

    ADS  MathSciNet  CAS  Article  Google Scholar 

  25. Fisher, R. A. The Genetical Theory of Natural Selection(Clarendon, Oxford, (1930)).

    Book  Google Scholar 

  26. Sinclair, J. F., Cohen, J. & Mindich, L. The isolation of suppressible nonsense mutants of bacteriophage φ6. Virology 75, 198–208 (1976).

    CAS  Article  Google Scholar 

  27. Vidaver, K. A., Koski, R. K. & Van Etten, J. L. Bacteriophage φ6: a lipid-containing virus of Pseudomonas phaseolicola. J. Virol. 11, 799–805 (1973).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank C. Burch, K. Hanley, S. Lance, U. Mueller, J. Smale and G. Wilkinson for useful comments and enlightening discussion. This work was supported by fellowships from the NSF and University of Maryland to P.E.T.

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Correspondence to Paul E. Turner.

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Turner, P., Chao, L. Prisoner's dilemma in an RNA virus. Nature 398, 441–443 (1999). https://doi.org/10.1038/18913

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