Sex increases the efficacy of natural selection in experimental yeast populations

Abstract

Why sex evolved and persists is a problem for evolutionary biology, because sex disrupts favourable gene combinations and requires an expenditure of time and energy1. Further, in organisms with unequal-sized gametes, the female transmits her genes at only half the rate of an asexual equivalent (the twofold cost of sex)2. Many modern theories that provide an explanation for the advantage of sex incorporate an idea originally proposed by Weismann more than 100 years ago: sex allows natural selection to proceed more effectively because it increases genetic variation3,4,5. Here we test this hypothesis, which still lacks robust empirical support, with the use of experiments on yeast populations. Capitalizing on recent advances in the molecular biology of recombination in yeast, we produced by genetic manipulation strains that differed only in their capacity for sexual reproduction. We show that, as predicted by the theory, sex increases the rate of adaptation to a new harsh environment but has no measurable effect on fitness in a new benign environment where there is little selection.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: The change in natural logarithm of fitness of asexual and sexual populations of yeast in benign and harsh environments.

References

  1. 1

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

    Google Scholar 

  2. 2

    Michod, R. E. & Levin, B. R. The Evolution of Sex: An Examination of Current Ideas (Sinauer, Sunderland, Massachusetts, 1988)

    Google Scholar 

  3. 3

    Weismann, A. The Evolution Theory (Edward Arnold, London, 1904)

    Google Scholar 

  4. 4

    Barton, N. H. & Charlesworth, B. Why sex and recombination? Science 281, 1986–1990 (1998)

    CAS  Article  Google Scholar 

  5. 5

    Burt, A. Sex, recombination, and the efficacy of selection—was Weismann right? Evolution 54, 337–351 (2000)

    CAS  PubMed  Google Scholar 

  6. 6

    Bruggeman, J., Debets, A. J. M., Wijngaarden, P. J., deVisser, J. A. G. M. & Hoekstra, R. F. Sex slows down the accumulation of deleterious mutations in the homothallic fungus Aspergillus nidulans . Genetics 164, 479–485 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  7. 7

    Otto, S. P. & Lenormand, T. Resolving the paradox of sex and recombination. Nature Rev. Genet. 3, 252–261 (2002)

    CAS  Article  Google Scholar 

  8. 8

    Birdsell, J. & Wills, C. Significant competitive advantage conferred by meiosis and syngamy in the yeast Saccharomyces cerevisiae . Proc. Natl Acad. Sci. USA 93, 908–912 (1996)

    ADS  CAS  Article  Google Scholar 

  9. 9

    Greig, D., Borts, R. H. & Louis, E. J. The effect of sex on adaptation to high temperature in heterozygous and homozygous yeast. Proc. R. Soc. Lond. B 265, 1017–1023 (1998)

    CAS  Article  Google Scholar 

  10. 10

    Colegrave, N. Sex releases the speed limit on evolution. Nature 420, 664–666 (2002)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Kaltz, O. & Bell, G. The ecology and genetics of fitness in Chlamydomonas. XII. Repeated sexual episodes increase the rates of adaptation to novel environments. Evolution 56, 1743–1753 (2002)

    Article  Google Scholar 

  12. 12

    Rice, W. R. Experimental effects of the adaptive significance of sexual recombination. Nature Rev. Genet. 3, 241–251 (2002)

    CAS  Article  Google Scholar 

  13. 13

    Rice, W. R. & Chippindale, A. K. Sexual recombination and the power of natural selection. Science 294, 555–559 (2001)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Goho, S. & Bell, G. Mild environmental stress elicits mutations affecting fitness in Chlamydomonas . Proc. R. Soc. Lond. B 267, 123–129 (2000)

    CAS  Article  Google Scholar 

  15. 15

    Marini, A., Matmati, N. & Morpurgo, G. Starvation in yeast increases non-adaptive mutation. Curr. Genet. 35, 77–81 (1999)

    CAS  Article  Google Scholar 

  16. 16

    Berry, D. R. The Biology of Yeasts (Edward Arnold, London, 1982)

    Google Scholar 

  17. 17

    Grewal, N. S. & Miller, J. J. Formation of asci with two diploid spores by diploid cells of Saccharomyces . Can. J. Microbiol. 18, 1897–1905 (1972)

    CAS  Article  Google Scholar 

  18. 18

    Klapholz, S., Waddell, C. S. & Esposito, R. E. The role of the SPO11 gene in meiotic recombination in yeast. Genetics 110, 187–216 (1985)

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 19

    Shonn, M. A., McCarroll, R. & Murray, A. W. Spo13 protects meiotic cohesin at centromeres in meiosis I. Genes Dev. 16, 1659–1671 (2002)

    CAS  Article  Google Scholar 

  20. 20

    Wang, H., Frackman, S., Kowalisyn, J., Esposito, R. E. & Elder, R. Developmental regulation of SPO13, a gene required for separation of homologous chromosomes at meiosis I. Mol. Cell. Biol. 7, 1425–1435 (1987)

    CAS  Article  Google Scholar 

  21. 21

    Steele, D. F., Morris, M. E. & Jinks-Robertson, S. Allelic and ectopic interactions in recombination-defective yeast strains. Genetics 127, 53–60 (1991)

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22

    Wach, A. et al. PCR-based gene targeting in S. cerevisiae . Methods Microbiol. 26, 67–81 (1998)

    CAS  Article  Google Scholar 

  23. 23

    Baganz, F., Hayes, A., Marren, D., Gardner, D. C. J. & Oliver, S. G. Suitability of replacement markers for functional analysis studies in Saccharomyces cerevisiae . Yeast 13, 1536–1573 (1997)

    Article  Google Scholar 

  24. 24

    Burke, D., Dawson, D. & Stearns, T. Methods in Yeast Genetics. A Cold Spring Harbor Laboratory Course Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2000)

    Google Scholar 

  25. 25

    Pinheiro, J. C. & Bates, D. M. Mixed-effects Models in S and S-PLUS (Springer, New York, 2000)

    Google Scholar 

  26. 26

    Zeyl, C. & DeVisser, J. A. G. M. Estimates of the rate and distribution of fitness effects of spontaneous mutation in Saccharomyces cerevisiae . Genetics 157, 53–61 (2001)

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27

    Burt, A. The evolution of fitness. Evolution 49, 1–8 (1995)

    PubMed  Google Scholar 

  28. 28

    Muller, H. J. Some genetic aspects of sex. Am. Nat. 66, 118–138 (1932)

    Article  Google Scholar 

  29. 29

    Barton, N. A general model for the evolution of recombination. Genet. Res. 65, 123–144 (1995)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank M. Rees for comments on statistical analyses. This work was supported by the UK Natural Environment Research Council (NERC).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Matthew R. Goddard.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Methods

This file contains more detailed descriptions of the methods used in this study. (DOC 37 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Goddard, M., Godfray, H. & Burt, A. Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434, 636–640 (2005). https://doi.org/10.1038/nature03405

Download citation

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.