GeezerVison

Abstract

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 counterparts^1,2 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.

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year only $3.90 per issue

Learn more

Buy this article

Purchase on SpringerLink
Instant access to the full article PDF.

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

**Figure 1: Effects of mutation rate and sexual selection on the cost of sex.**

**Figure 2: Multiplicative versus synergistically epistatic effects in males.**

Why put all your eggs in one basket? Evolutionary perspectives on the origins of monogenic reproduction

Article Open access 16 June 2023

Transitions in sex determination mechanisms through parental and sexual antagonism

Article 21 August 2024

Parallel loss of sexual reproduction in field populations of a brown alga sheds light on the mechanisms underlying the emergence of asexuality

Article Open access 16 August 2024

Explore related subjects

Discover the latest articles and news in related subjects.

Reproductive Strategies in Evolutionary Biology

References

Maynard-Smith, J. The Evolution of Sex (Cambridge Univ. Press, Cambridge, 1978).
Google Scholar
Bell, G. The Masterpiece of Nature: The Evolution and Genetics of Sexuality (Univ. of California Press, Berkeley, 1982).
Google Scholar
Andersson, M. Sexual Selection (Princeton Univ. Press, Princeton, 1994).
Book Google Scholar
Trivers, R. L. in Sexual Selection and the Descent of Man (ed. Campbell, B. G.) 141 (Aldine, Chicago, 1972).
Google Scholar
Arnold, S. J. & Wade, M. J. On the measurement of natural and sexual selection: applications. Evolution 38, 720–734 (1984).
Article Google Scholar
Manning, J. T. Males and the advantage of sex. J. Theor. Biol. 108, 215–220 (1984).
Article ADS CAS Google Scholar
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
Koselag, J. H. & Koeslag, P. D. Evolutionary stable meiotic sex. J. Hered. 84, 396–399 (1993).
Article Google Scholar
Kimura, M. & Maruyama, T. The mutational load with epistatic interactions in fitness. Genetics 54, 1337–1351 (1966).
Article CAS Google Scholar
Kondrashov, A. S. Selection against harmful mutations in large sexual and asexual populations. Genet. Res. 40, 325–332 (1982).
Article CAS Google Scholar
Kondrashov, A. S. Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440 (1988).
Article ADS CAS Google Scholar
Charlesworth, B. Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet. Res. 55, 199–221 (1990).
Article CAS Google Scholar
Chasnov, J. R. Mutation-selection balance, dominance and the maintenance of sex. Genetics 156, 1419–1425 (2000).
Article CAS Google Scholar
Crow, J. F. in Mathematical Topics in Population Genetics (ed. Kojima, K.-I.) 128–177 (Springer, Berlin, 1970).
Book Google Scholar
Elena, S. E. & Lenski, R. E. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390, 395–398 (1997).
Article ADS CAS Google Scholar
Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer Associates, Sunderland, 1998).
Google Scholar
García-Dorado, A. & Caballero, A. On the average coefficient of dominance of deleterious spontaneous mutations. Genetics 155, 1991–2001 (2000).
Article Google Scholar
Peck, J. R. & Waxman, D. Mutation and sex in a competitive world. Nature 406, 399–404 (2000).
Article ADS CAS Google Scholar
Keightley, P. D. & Eyre-Walker, A. Terumi Mukai and the riddle of deleterious mutation rates. Genetics 153, 515–523 (1999).
Article CAS Google Scholar
Lynch, M. et al. Spontaneous deleterious mutation. Evolution 53, 645–663 (1999).
Article Google Scholar
Keightley, P. D. & Eyre-Walker, A. Deleterious mutations and the evolution of sex. Science 290, 331–333 (2000).
Article ADS CAS Google Scholar
Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001).
Article CAS Google Scholar
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).
Article CAS Google Scholar
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).
Article ADS CAS Google Scholar
Evans, J. P. & Magurran, A. E. Multiple benefits of multiple mating in guppies. Proc. Natl Acad. Sci. USA 97, 10074–10076 (2000).
Article ADS CAS Google Scholar
Mulcahy, D. L. The rise of angiosperms: a genecological factor. Science 206, 20–23 (1979).
Article ADS CAS Google Scholar
Whitlock, M. C. & Bourget, D. Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components. Evolution 54, 1654–1660 (2000).
Article CAS Google Scholar
Hurst, L. D. & Peck, J. R. Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol. Evol. 11, 46–52 (1996).
Article CAS Google Scholar
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).
Article CAS Google Scholar
Howard, R. S. & Lively, C. M. Parasitism, mutation accumulation and the maintenance of sex. Nature 367, 554–557 (1994).
Article ADS CAS Google Scholar

Download references

Acknowledgements

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

Authors and Affiliations

Department of Biology, Indiana University, Bloomington, 47405-3700, Indiana, USA
Aneil F. Agrawal

Authors

Aneil F. Agrawal
View author publications
Search author on:PubMed Google Scholar

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). https://doi.org/10.1038/35079590

Download citation

Received: 09 October 2000
Accepted: 19 March 2001
Published: 01 June 2001
Issue date: 07 June 2001
DOI: https://doi.org/10.1038/35079590

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative