Sexual selection and the maintenance of sex


Sex is expensive. A population of females that reproduce asexually should prima facie have twice the growth rate of an otherwise equivalent anisogamous sexual population lacking paternal care, or a population with modes of paternal care that can be co-opted by parthenogenetic females1,2,3,4,5,6. The two leading theories for the maintenance of sex require either synergistic interactions between deleterious mutations, or antagonistic epistasis between beneficial mutations5. Current evidence is equivocal as to whether the required levels of epistasis exist6,7,8,9,10. Here I show that a third factor, differential male mating success (or, more generally, higher variance in male than in female fitness), can drastically reduce mutational load in sexual populations with or without any form of epistasis. Differential mating success has the further advantage of being ubiquitous, and is likely to have preceded or evolved concurrently with anisogamy11.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Contour graph of the relative viability advantage of a sexual population with best of n mate choice over an equivalent asexual population [(1 - Lsex)/(1 - Lasex)].


  1. 1

    Maynard Smith, J. in Group Selection (ed. Williams, G. C.) 163–175 (Aldine–Atherton, Chicago, 1971).

  2. 2

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

    CAS  Article  Google Scholar 

  3. 3

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

    CAS  Article  Google Scholar 

  4. 4

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

    CAS  Article  Google Scholar 

  5. 5

    Barton, N. H. & Charlesworth, B. Why sex and recombination? Science 281, 1986–1989 (1998).

    CAS  Article  Google Scholar 

  6. 6

    West, S. A., Lively, C. M. & Read, A. F. A pluralist approach to sex and recombination. J. Evol. Biol. 12, 1003–1012 (1999).

    Article  Google Scholar 

  7. 7

    Lenski, R. E., Ofria, C., Collier, T. C. & Adami, C. Genome complexity, robustness and genetic interactions in digital organisms. Nature 400, 661–664 (1999).

    CAS  Article  Google Scholar 

  8. 8

    Elena, S. F. & Lenski, R. E. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390, 395–398 (1997).

    CAS  Article  Google Scholar 

  9. 9

    De Visser, J. A. G. M. & Hoekstra, R. F. Synergistic epistasis between loci affecting fitness: evidence in plants and fungi. Genet. Res. Camb. 71, 39–49 (1998).

    Article  Google Scholar 

  10. 10

    West, S. A., Peters, A. D. & Barton, N. H. Testing for epistasis between deleterious mutations. Genetics 149, 435–444 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11

    Bell, G. The Masterpiece of Nature: The Evolution and Genetics of Sexuality (Univ. California Press, Berkeley, 1982).

    Google Scholar 

  12. 12

    Trivers, R. L. Sexual selection and resource-accruing abilities in Anolis garmani. Evolution 30, 253–269 (1976).

    Article  Google Scholar 

  13. 13

    Atmar, W. On the role of males. Anim. Behav. 41, 195–205 (1991).

    Article  Google Scholar 

  14. 14

    Koeslag, P. D. & Koeslag, J. H. Koinophilia stabilizes bi-gender sexual reproduction against asexual in an unchanging environment. J. Theor. Biol. 166, 251–260 (1994).

    CAS  Article  Google Scholar 

  15. 15

    Kodric-Brown, A. & Brown, J. H. Anisogamy, sexual selection, and the evolution and maintenance of sex. Evol. Ecol. 1, 95–105 (1987).

    Article  Google Scholar 

  16. 16

    Manning, J. T. Males and the advantage of sex. J. Theor. Biol. 108, 215–220 (1984).

    CAS  Article  Google Scholar 

  17. 17

    Kondrashov, A. S. & Crow, J. F. King's formula for the mutation load with epistasis. Genetics 120, 853–856 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 18

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

    Google Scholar 

  19. 19

    Rohlf, F. J. & Sokal, R. R. Statistical Tables (W. H. Freeman, New York, 1994).

    Google Scholar 

  20. 20

    Simmons, M. J. & Crow, J. F. Mutations affecting fitness in Drosophila populations. Ann. Rev. Genet. 11, 49–78 (1977).

    CAS  Article  Google Scholar 

  21. 21

    Petrie, M., Halliday, T. & Sanders, C. Peahens prefer peacocks with elaborate trains. Anim. Behav. 41, 323–332 (1991).

    Article  Google Scholar 

  22. 22

    Dale, S., Rinde, H. & Slagsvold, T. Competition for a mate restricts mate search of female pied flycatchers. Behav. Ecol. Sociobiol. 30, 165–176 (1992).

    Article  Google Scholar 

  23. 23

    Holland, B. & Rice, W. R. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc. Natl Acad. Sci. USA 96, 5083–5088 (1999).

    CAS  Article  Google Scholar 

  24. 24

    Lynch, M. et al. Perspective: spontaneous deleterious mutation. Evolution 63, 645–663 (1999).

    Article  Google Scholar 

  25. 25

    Keightley, P. D. & Eyre-Walker, A. Terumi Mukai and the riddle of deleterious mutation rates. Genetics 153, 515–523 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

    Keightley, P. D. & Eyre-Walker, A. Deleterious mutations and the evolution of sex. Science 290, 331–333 (2000).

    CAS  Article  Google Scholar 

  27. 27

    Kondrashov, A. S. Sex and U. Trends Genet. 17, 75–77 (2000).

    Article  Google Scholar 

  28. 28

    Arnold, S. J. et al. Sexual selection in plants and animals. Am. Nat. 144, S1–S149 (1994).

    Article  Google Scholar 

Download references


I would like to thank R. Dawkins, L. Eshel, A. Grafen, L. Hurst, A. Kacelnik, A. Kondrashov, J. Metcalf, R. Nair, S. Schultz, F. Weissing, and in particular, M. Ridley for their comments on drafts of this manuscript.

Author information



Corresponding author

Correspondence to Steven Siller.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Siller, S. Sexual selection and the maintenance of sex. Nature 411, 689–692 (2001).

Download citation

Further reading


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.


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