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.
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Maynard-Smith, J. The Evolution of Sex (Cambridge Univ. Press, Cambridge, 1978).
Bell, G. The Masterpiece of Nature: The Evolution and Genetics of Sexuality (Univ. of California Press, Berkeley, 1982).
Andersson, M. Sexual Selection (Princeton Univ. Press, Princeton, 1994).
Trivers, R. L. in Sexual Selection and the Descent of Man (ed. Campbell, B. G.) 141 (Aldine, Chicago, 1972).
Arnold, S. J. & Wade, M. J. On the measurement of natural and sexual selection: applications. Evolution 38, 720–734 (1984).
Manning, J. T. Males and the advantage of sex. J. Theor. Biol. 108, 215–220 (1984).
Kodric-Brown, A. & Brown, J. H. Anisogamy, sexual selection, and the evolution and maintenance of sex. Evol. Ecol. 1, 95–105 (1987).
Koselag, J. H. & Koeslag, P. D. Evolutionary stable meiotic sex. J. Hered. 84, 396–399 (1993).
Kimura, M. & Maruyama, T. The mutational load with epistatic interactions in fitness. Genetics 54, 1337–1351 (1966).
Kondrashov, A. S. Selection against harmful mutations in large sexual and asexual populations. Genet. Res. 40, 325–332 (1982).
Kondrashov, A. S. Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440 (1988).
Charlesworth, B. Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet. Res. 55, 199–221 (1990).
Chasnov, J. R. Mutation-selection balance, dominance and the maintenance of sex. Genetics 156, 1419–1425 (2000).
Crow, J. F. in Mathematical Topics in Population Genetics (ed. Kojima, K.-I.) 128–177 (Springer, Berlin, 1970).
Elena, S. E. & Lenski, R. E. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390, 395–398 (1997).
Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer Associates, Sunderland, 1998).
García-Dorado, A. & Caballero, A. On the average coefficient of dominance of deleterious spontaneous mutations. Genetics 155, 1991–2001 (2000).
Peck, J. R. & Waxman, D. Mutation and sex in a competitive world. Nature 406, 399–404 (2000).
Keightley, P. D. & Eyre-Walker, A. Terumi Mukai and the riddle of deleterious mutation rates. Genetics 153, 515–523 (1999).
Lynch, M. et al. Spontaneous deleterious mutation. Evolution 53, 645–663 (1999).
Keightley, P. D. & Eyre-Walker, A. Deleterious mutations and the evolution of sex. Science 290, 331–333 (2000).
Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001).
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).
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).
Evans, J. P. & Magurran, A. E. Multiple benefits of multiple mating in guppies. Proc. Natl Acad. Sci. USA 97, 10074–10076 (2000).
Mulcahy, D. L. The rise of angiosperms: a genecological factor. Science 206, 20–23 (1979).
Whitlock, M. C. & Bourget, D. Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components. Evolution 54, 1654–1660 (2000).
Hurst, L. D. & Peck, J. R. Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol. Evol. 11, 46–52 (1996).
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).
Howard, R. S. & Lively, C. M. Parasitism, mutation accumulation and the maintenance of sex. Nature 367, 554–557 (1994).
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.
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