Variation in the reversibility of evolution

Article metrics

Abstract

How reversible is adaptive evolution1,2,3,4,5,6? Studies of microbes give mixed answers to this question6,7,8,9,10,11. Reverse evolution has been little studied in sexual populations12,13,14, even though the population genetics of sexual populations may be quite different. In the present study, 25 diverged replicated populations of Drosophila melanogaster are returned to a common ancestral environment for 50 generations. Here we show that reverse evolution back to the ancestral state occurs, but is not universal, instead depending on previous evolutionary history and the character studied. Hybrid populations showed no greater tendency to undergo successful reverse evolution, suggesting that insufficient genetic variation was not the factor limiting reverse evolution. Adaptive reverse evolution is a contingent process which occurs with only 50 generations of sexual reproduction.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Laboratory radiation due to five selection treatments.
Figure 2: Reverse evolution during 50 generations.
Figure 3: Reverse evolutionary rates as a function of differentiation at the start of the study.

References

  1. 1

    Muller, H. J. Reversibility in evolution considered from the standpoint of genetics. Biol. Rev. 14, 261–280 (1939).

  2. 2

    Simpson, G. G. The Major Features of Evolution (Columbia Univ. Press, New York, 1953).

  3. 3

    Wright, S. Evolution and the Genetics of Populations. Vol 3 Experimental Results and Evolutionary Deductions (Univ. Chicago Press, Chicago, 1977).

  4. 4

    Bull, J. J. & Charnov, E. L. On irreversible evolution. Evolution 39, 1149–1155 (1985).

  5. 5

    Gayon, J. Darwinism's Struggle for Survival: Heredity and the Hypothesis of Natural Selection (Cambridge Univ. Press, Cambridge and New York, 1998).

  6. 6

    Crill, W. D., Wichman, H. A. & Bull, J. J. Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154, 27–37 (2000).

  7. 7

    Lenski, R. E. Experimental studies of pleiotropy and epistasis in Escherichia coli. II. Compensation for maladaptive effects associated with resistance to virus T4. Evolution 42, 433–440 (1988).

  8. 8

    Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998).

  9. 9

    Burch, C. L. & Chao, L. Evolution by small steps and rugged landscapes in the RNA virus φ6. Genetics 151, 921–927 (1999).

  10. 10

    Moore, F. B.-G., Rozen, D. E. & Lenski, R. E. Pervasive compensatory adaptation in Escherichia coli. Proc. R. Soc. Lond. B 267, 515–522 (2000).

  11. 11

    Levin, B. L., Perrot, V. & Walker, N. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in Bacteria. Genetics 154, 985–997 (2000).

  12. 12

    Clarke, C. A., Mani, G. S. & Wynne, G. Evolution in reverse: clean air and the peppered moth. Biol. J. Linn. Soc. 26, 189–199 (1985).

  13. 13

    Service, P. M., Hutchison, E. W. & Rose, M. R. Multiple genetic mechanisms for the evolution of senescence in Drosophila melanogaster. Evolution 42, 708–716 (1988).

  14. 14

    Cook, L. M., Dennis, R. L. & Mani, G. S. Melanic morph frequency in the peppered moth in the Manchester area. Proc. R. Soc. Lond. B 266, 293–297 (1999).

  15. 15

    Rose, M. R. Laboratory evolution of postponed senescence in Drosophila melanogaster. Evolution 38, 1004–1010 (1984).

  16. 16

    Graves, J. L., Toolson, E. C., Jeong, C., Vu, L. N. & Rose, M. R. Desiccation, flight, glycogen, and postponed senescence in Drosophila melanogaster. Physiol. Zool. 65, 268–286 (1992).

  17. 17

    Rose, M. R., Vu, L. N., Park, S. U. & Graves, J. L. Selection on stress resistance increased longevity in Drosophila melanogaster. Exp. Gerontol. 27, 241–250 (1992).

  18. 18

    Fleming, J. E., Spicer, G. S., Garrison, R. C. & Rose, M. R. Two-dimensional protein electrophoretic analysis of postponed aging in Drosophila. Genetica 91, 183–198 (1993).

  19. 19

    Tyler, R. H. et al. The effect of superoxide dismutase alleles on aging in Drosophila. Genetica 91, 143–149 (1993).

  20. 20

    Leroi, A. M., Chippindale, A. K. & Rose, M. R. Long-term laboratory evolution of a genetic life-history trade-off in Drosophila melanogaster. 1. The role of genotype-by-environment interaction. Evolution 48, 1244–1257 (1994).

  21. 21

    Chippindale, A. K., Alipaz, J. A., Chen, H.-W. & Rose, M. R. Experimental evolution of accelerated development in Drosophila. 1. Development speed and larval survival. Evolution 51, 1536–1551 (1997).

  22. 22

    Fisher, R. A. The Genetical Theory of Natural Selection (Dover, New York, 1958).

  23. 23

    Reznick, D. N., Bryga, H. & Endler, J. A. Experimentally induced life-history evolution in a natural population. Nature 346, 357–359 (1990).

  24. 24

    Coyne, J. A., Barton, N. H. & Turelli, M. Perspective: a critique of Sewall Wright's shifting balance theory of evolution. Evolution 51, 643–671 (1997).

  25. 25

    Losos, J. B., Jackman, T. R., Larson, A., de Queiroz, K. & Rodriguez-Schettino, L. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279, 2115–2117 (1998).

  26. 26

    Cohan, F. M. & Hoffmann, A. A. Uniform selection as a diversifying force in evolution: evidence from Drosophila. Am. Nat. 134, 613–637 (1989).

  27. 27

    Travisano, M., Mongold, J. A., Bennet, A. F. & Lenski, R. E. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267, 87–90 (1995).

  28. 28

    SPSS, I. SigmaPlot 5.0. Programming Guide (SPSS Inc., Chicago, 1998).

  29. 29

    Glantz, S. A. & Slinker, B. K. Primer of Applied Regression and Analysis of Variance (McGraw-Hill Health Professions Division, New York, 1990).

  30. 30

    Zar, J. H. Biostatistical Analysis (Prentice Hall, Upper Saddle River, 1996).

Download references

Acknowledgements

We thank P. Beldade, A. K. Chippindale, L. D. Mueller, E. Sucena and particularly M. Matos for advice throughout the project and for comments on the manuscript. H.T. was supported by the Gulbenkian Foundation and Program PRAXIS XXI/FCT under the “Programa Gulbenkian de Doutoramento em Biologia e Medicina”.

Author information

Correspondence to Henrique Teotónio.

Rights and permissions

Reprints and Permissions

About this article

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.