Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Male mutation rates and the cost of sex for females

Abstract

ALTHOUGH we do not know why sex evolved, the twofold cost of meiosis for females provides a standard against which postulated benefits of sex can be evaluated1. The most reliable benefit is sex's ability to reduce the impact of deleterious mutations2,3. But deleterious mutations may themselves generate a large and previously overlooked female-specific cost of sex. DNA sequence comparisons have confirmed Haldane's suggestion that most mutations arise in the male germ line4,5; recent estimates of α, the ratio of male to female mutation rates, are ten, six and two in humans, primates and rodents, respectively6–8. Consequently, male gametes may give progeny more mutations than the associated sexual recombination eliminates. Here I describe computer simulations showing that the cost of male mutations can easily exceed the benefits of recombination, causing females to produce fitter progeny by parthenogenesis than by mating. The persistence of sexual reproduction by females thus becomes even more problematic.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

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

    Google Scholar 

  2. 2

    Kondrashov, A. S. Nature 336, 435–440 (1988).

    ADS  CAS  Article  Google Scholar 

  3. 3

    Charlesworth, B. Genet. Res., Camb. 55, 199–221 (1990).

    CAS  Article  Google Scholar 

  4. 4

    Haldane, J. B. S. Ann. Eugen. 13, 262–271 (1947).

    CAS  Article  Google Scholar 

  5. 5

    Miyata, T., Hayashida, H., Kuma, K., Mitsuyasu, K. & Yasunaga, T. Cold Spring Harb. Symp. quant. Biol. 52, 863–867 (1987).

    CAS  Article  Google Scholar 

  6. 6

    Montandon, A. J. et al. Hum. Genet. 89, 319–322 (1992).

    CAS  Article  Google Scholar 

  7. 7

    Shimmin, L. C., Chang, B. H.-J. & Li, W.-H. Nature 362, 745–747 (1993).

    ADS  CAS  Article  Google Scholar 

  8. 8

    Chang, B. H.-J., Shimmin, L., Shyue, S.-K., Hewett-Emmett, D. & Li, W.-H. Proc. natn. Acad. Sci. U.S.A. 91, 827–831 (1994).

    ADS  CAS  Article  Google Scholar 

  9. 9

    Crow, J. F. in Mathematical Topics in Population Genetics (ed. Kojima, K.) 128–177 (Springer, Berlin, 1970).

    Google Scholar 

  10. 10

    Haldane, J. B. S. Am. Nat. 71, 337–349 (1937).

    Article  Google Scholar 

  11. 11

    Kimura, M. & Maruyama, T. Genetics 54, 1303–1312 (1966).

    Google Scholar 

  12. 12

    Maynard Smith, J. Am. Nat. 102, 469–473 (1968).

    Article  Google Scholar 

  13. 13

    Mukai, T. Genetics 81, 749–761 (1969).

    Google Scholar 

  14. 14

    Muller, H. J. Mutat. Res. 1, 2–9 (1964).

    Article  Google Scholar 

  15. 15

    Kondrashov, A. S. Genet. Res., Camb. 44, 199–217 (1984).

    CAS  Article  Google Scholar 

  16. 16

    Kondrashov, A. S. & Crow, J. F. Hum. Mutat. 2, 229–234 (1993).

    CAS  Article  Google Scholar 

  17. 17

    Hamilton, W.D., Axelrod, R. & Tanese, R. Proc. natn. Acad. Sci. USA. 87, 3566–3573 (1990).

    ADS  CAS  Article  Google Scholar 

  18. 18

    Howard, R. S. & Lively, C. M. Nature 367, 554–557 (1994).

    ADS  CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Redfield, R. Male mutation rates and the cost of sex for females. Nature 369, 145–147 (1994). https://doi.org/10.1038/369145a0

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.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing