Sexual selection and the maintenance of sexual reproduction


The maintenance of sexual reproduction is a problem in evolutionary theory because, all else being equal, asexual populations have a twofold fitness advantage over their sexual counterparts1,2 and should rapidly outnumber a sexual population because every individual has the potential to reproduce. The twofold cost of sex exists because of anisogamy or gamete dimorphism2—egg-producing females make a larger contribution to the zygote compared with the small contribution made by the sperm of males, but both males and females contribute 50% of the genes. Anisogamy also generates the conditions for sexual selection3, a powerful evolutionary force that does not exist in asexual populations. The continued prevalence of sexual reproduction indicates that the ‘all else being equal’ assumption is incorrect. Here I show that sexual selection can mitigate or even eliminate the cost of sex. If sexual selection causes deleterious mutations to be more deleterious in males than females, then deleterious mutations are maintained at lower equilibrium frequency in sexual populations relative to asexual populations. The fitness of sexual females is higher than asexuals because there is no difference in the fecundity of sexual females and asexuals of the same genotype, but the equilibrium frequency of deleterious mutations is lower in sexual populations. The results are not altered by synergistic epistasis in males.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Effects of mutation rate and sexual selection on the cost of sex.
Figure 2: Multiplicative versus synergistically epistatic effects in males.


  1. 1

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

    Google Scholar 

  2. 2

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

    Google Scholar 

  3. 3

    Andersson, M. Sexual Selection (Princeton Univ. Press, Princeton, 1994).

    Google Scholar 

  4. 4

    Trivers, R. L. in Sexual Selection and the Descent of Man (ed. Campbell, B. G.) 141 (Aldine, Chicago, 1972).

    Google Scholar 

  5. 5

    Arnold, S. J. & Wade, M. J. On the measurement of natural and sexual selection: applications. Evolution 38, 720–734 (1984).

    Article  Google Scholar 

  6. 6

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

    CAS  Article  Google Scholar 

  7. 7

    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 

  8. 8

    Koselag, J. H. & Koeslag, P. D. Evolutionary stable meiotic sex. J. Hered. 84, 396–399 (1993).

    Article  Google Scholar 

  9. 9

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

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Kondrashov, A. S. Selection against harmful mutations in large sexual and asexual populations. Genet. Res. 40, 325–332 (1982).

    CAS  Article  Google Scholar 

  11. 11

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

    CAS  Article  Google Scholar 

  12. 12

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

    CAS  Article  Google Scholar 

  13. 13

    Chasnov, J. R. Mutation-selection balance, dominance and the maintenance of sex. Genetics 156, 1419–1425 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

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

    Google Scholar 

  15. 15

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

    CAS  Article  Google Scholar 

  16. 16

    Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer Associates, Sunderland, 1998).

    Google Scholar 

  17. 17

    García-Dorado, A. & Caballero, A. On the average coefficient of dominance of deleterious spontaneous mutations. Genetics 155, 1991–2001 (2000).

    PubMed  PubMed Central  Google Scholar 

  18. 18

    Peck, J. R. & Waxman, D. Mutation and sex in a competitive world. Nature 406, 399–404 (2000).

    CAS  Article  Google Scholar 

  19. 19

    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 

  20. 20

    Lynch, M. et al. Spontaneous deleterious mutation. Evolution 53, 645–663 (1999).

    Article  Google Scholar 

  21. 21

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

    CAS  Article  Google Scholar 

  22. 22

    Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001).

    CAS  Article  Google Scholar 

  23. 23

    Drickamer, L. C., Gowaty, P. A. & Holmes, C. M. Free female choice in house mice affects reproductive success and offspring viability and performance. Anim. Behav. 59, 371–378 (2000).

    CAS  Article  Google Scholar 

  24. 24

    Welch, A. M., Semlitsch, R. D. & Gerhardt, H. C. Call duration as an indicator of genetic quality in male gray tree frogs. Science 280, 1928–1930 (1998).

    CAS  Article  Google Scholar 

  25. 25

    Evans, J. P. & Magurran, A. E. Multiple benefits of multiple mating in guppies. Proc. Natl Acad. Sci. USA 97, 10074–10076 (2000).

    CAS  Article  Google Scholar 

  26. 26

    Mulcahy, D. L. The rise of angiosperms: a genecological factor. Science 206, 20–23 (1979).

    CAS  Article  Google Scholar 

  27. 27

    Whitlock, M. C. & Bourget, D. Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components. Evolution 54, 1654–1660 (2000).

    CAS  Article  Google Scholar 

  28. 28

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

    CAS  Article  Google Scholar 

  29. 29

    Whitlock, M. C. Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution 54, 1855–1861 (2000).

    CAS  Article  Google Scholar 

  30. 30

    Howard, R. S. & Lively, C. M. Parasitism, mutation accumulation and the maintenance of sex. Nature 367, 554–557 (1994).

    CAS  Article  Google Scholar 

Download references


I thank C. Lively, K. Quinlan and M. Wade for comments. A. Kondrashov suggested using the multilocus approach to this problem. S. Otto pointed out that the analytical solution is exact by use of equation (6). This work was supported by NSERC Canada.

Author information



Corresponding author

Correspondence to Aneil F. Agrawal.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Agrawal, A. Sexual selection and the maintenance of sexual reproduction. Nature 411, 692–695 (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