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Test of synergistic interactions among deleterious mutations in bacteria

Nature volume 390, pages 395–398 (1997)Cite this article

Abstract

Identifying the forces responsible for the origin and maintenance of sexuality remains one of the greatest unsolved problems in biology1,2,3,4,5,6. The mutational deterministic hypothesis postulates that sex is an adaptation that allows deleterious mutations to be purged from the genome; it requires synergistic interactions, which means that two mutations would be more harmful together than expected from their separate effects4,5. We generated 225 genotypes of Escherichia coli carrying one, two or three successive mutations and measured their fitness relative to an unmutated competitor. The relationship between mutation number and average fitness is nearly log-linear. We also constructed 27 recombinant genotypes having pairs of mutations whose separate and combined effects on fitness were determined. Several pairs exhibit significant interactions for fitness, but they are antagonistic as often as they are synergistic. These results do not support the mutational deterministic hypothesis for the evolution of sex.

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Figure 1: Hypothetical effects of increasing numbers of deleterious mutations on fitness.
Figure 2: Observed effect of increasing the number of deleterious mutations on fitness in the bacterium, E.coli .
Figure 3: Distribution of observed minus expected fitness values for 27 different double mutants.

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References

  1. Williams, G. C. Sex and Evolution(Princeton Univ. Press, Princeton, (1975)).

    Google Scholar 

  2. Maynard Smith, J. The Evolution of Sex(Cambridge Univ. Press, Cambridge, MA, (1978)).

    Google Scholar 

  3. Bell, G. The Masterpiece of Nature(Univ. California Press, Berkeley, (1982)).

  4. Kondrashov, A. S. Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440 (1988).

    Article  ADS  CAS  Google Scholar 

  5. Kondrashov, A. S. Classification of hypotheses on the advantage of amphimixis. J. Hered. 84, 372–387 (1993).

    Article  CAS  Google Scholar 

  6. Hurst, L. D. & Peck, J. R. Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol. Evol. 11, 46–52 (1996).

    Article  CAS  Google Scholar 

  7. Muller, H. J. The relation of recombination to mutational advantage. Mut. Res. 1, 2–9 (1964).

    Article  Google Scholar 

  8. Haigh, J. The accumulation of deleterious genes in a population: Muller's ratchet. Theor. Popul. Biol. 14, 251–267 (1978).

    Article  MathSciNet  CAS  Google Scholar 

  9. Kimura, M. & Maruyama, T. The mutational load with epistatic gene interactions in fitness. Genetics 54, 1337–1351 (1966).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Crow, J. F. in Genetic Loads and the Cost of Natural Selection(ed. Kojima, K. I.) 128–177 (Springer, New York, (1970)).

    Google Scholar 

  11. Redfield, R. J., Schrag, M. R. & Dean, A. M. The evolution of bacterial transformation: sex with poor relations. Genetics 146, 27–38 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Spassky, B., Dobzhansky, Th. & Anderson, W. W. Genetics of natural populations. XXXVI. Epistatic interactions of the components of the genetic load in Drosophila pseudoobscura . Genetics 52, 653–664 (1965).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Kitigawa, O. Interactions in fitness between lethal genes in heterozygous condition in Drosophila melanogaster . Genetics 57, 809–820 (1969).

    Google Scholar 

  14. Mukai, T. The genetic structure of natural populations of Drosophila melanogaster . VII. Synergistic interaction of spontaneous mutant polygenes controlling viability. Genetics 61, 749–761 (1969).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Chao, L. Evolution of sex in RNA viruses. J. Theor. Biol. 133, 99–112 (1988).

    Article  CAS  Google Scholar 

  16. De Visser, J. A. G. M., Hoekstra, R. F. & van den Ende, H. The effect of sex and deleterious mutations on fitness in Chlamydomonas . Proc. R. Soc. Lond. B 263, 193–200 (1996).

    Article  ADS  Google Scholar 

  17. De Visser, J. A. G. M., Hoekstra, R. F. & van den Ende, H. Test of interaction between genetic markers that affect fitness in Aspergillus niger . Evolution(in the press).

  18. Willis, J. H. Effects of different levels of inbreeding on fitness components in Mimulus guttatus . Evolution 47, 864–876 (1993).

    Article  Google Scholar 

  19. Zeyl, C. & Bell, G. The advantage of sex in evolving yeast populations. Nature 388, 465–468 (1997).

    Article  ADS  CAS  Google Scholar 

  20. Lenski, R. E. & Travisano, M. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc. Natl Acad. Sci. USA 91, 6808–6814 (1994).

    Article  ADS  CAS  Google Scholar 

  21. Kleckner, N., Bender, J. & Gottesman, S. Uses of transposons with emphasis on Tn 10 . Methods Enzymol. 204, 139–181 (1991).

    Article  CAS  Google Scholar 

  22. Sokal, R. R. & Rohlf, F. J. Biometry(Freeman, New York, (1981)).

    MATH  Google Scholar 

  23. Sniegowski, P. D., Gerrish, P. J. & Lenski, R. E. Evolution of high mutation rates in experimental populations of Escherichia coli . Nature 387, 703–705 (1997).

    Article  ADS  CAS  Google Scholar 

  24. Charlesworth, B. Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet. Res. 55, 199–221 (1990).

    Article  CAS  Google Scholar 

  25. Kibota, T. T. & Lynch, M. Estimate of the genomic mutation rate deleterious to overall fitness in E. coli . Nature 381, 694–696 (1996).

    Article  ADS  CAS  Google Scholar 

  26. Otto, S. P. & Feldman, M. W. Deleterious mutations, variable epistatic interactions, and the evolution of recombination. Theor. Popul. Biol. 51, 134–147 (1997).

    Article  CAS  Google Scholar 

  27. Rice, W. R. Analyzing tables of statistical tests. Evolution 43, 223–225 (1989).

    Article  Google Scholar 

  28. Elena, S. F., Ekunwe, L., Hajela, N., Oden, S. A. & Lenski, R. E. Distribution of fitness effects caused by random insertion mutations in Escherichia coli . Genetica(in the press).

  29. Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli . I. Adaptation and divergence during 2,000 generations. Am. Nat. 138, 1315–1341 (1991).

    Article  Google Scholar 

  30. Zyskind, J. W. & Bernstein, S. I. Recombinant DNA Laboratory Manual(Academic, San Diego, (1989)).

    Google Scholar 

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Acknowledgements

We thank V. de Lorenzo, L. Forney, J. Peck and O. Schabenberger for advice and encouragement; L. Ekunwe and N. Hajela for technical support; and A. de Visser, J. Mongold, P.Moore, S.Otto, B. Rice, D. Rozen and C. Zeyl for valuable comments. This work was supported by a fellowship from the Spanish MEC to S.F.E. and a grant from the NSF to R.E.L.

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  1. Center for Microbial Ecology, Michigan State University, East Lansing, 48824, Michigan, USA

    Santiago F. Elena & Richard E. Lenski

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  1. Santiago F. Elena
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  2. Richard E. Lenski
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Correspondence to Santiago F. Elena.

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Elena, S., Lenski, R. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390, 395–398 (1997). https://doi.org/10.1038/37108

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