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.

  • Review Article
  • Published:

Evolution of sex

Experimental tests of the adaptive significance of sexual recombination

Key Points

  • Theory predicts that sex can be advantageous because it reduces the mutational load of a population, increases the efficiency by which different beneficial mutations are combined in the same genome, and reduces the degree to which selection on genetic backgrounds interferes with both the recruitment of new beneficial mutations and the purging of new, harmful mutations.

  • Experiments provide support for the idea that the genome-wide mutation rate is sufficient in many, but not all, species to make the load-reducing effect of recombination highly favourable, but the mechanism by which this occurs is still unresolved.

  • No experiments have directly tested the idea that recombination speeds the rate at which new beneficial mutations are combined into the same genome, but related experiments concerning interference between beneficial mutations that are located in different clonal genomes do indicate an advantage to recombination.

  • Only one experiment has directly tested whether recombination slows the rate of accumulation of harmful mutations (retrogressive evolution), but this experiment showed a strong advantage to recombination.

  • Many experiments have tested the idea that recombination speeds the rate of accumulation of beneficial mutations (progressive evolution), and, on balance, these studies provide strong support for a substantial advantage to recombination.

Abstract

Numerous theories have been proposed to explain the advantages of sexual recombination — the exchange of hereditary material between different genomes or homologous chromosomes. Many of these candidate benefits have been evaluated in controlled laboratory experiments, which, collectively, strongly indicate that sexual recombination provides important long-term advantages.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Typical phylogenetic distribution of asexual species.
Figure 2: Fate of a mutation depends on direct selection (s), background selection and recombination.

Similar content being viewed by others

References

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

    Google Scholar 

  2. Williams, G. C. Sex and Evolution (Princeton Univ. Press, New Jersey, 1975).

    Google Scholar 

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

    Google Scholar 

  4. Stebbins, G. L. Variation and Evolution in Plants (Columbia Univ. Press, New York, 1950).

    Google Scholar 

  5. White, M. J. D. Modes of Speciation (W. H. Freeman, San Francisco, 1978).

    Google Scholar 

  6. Bell, G. The Masterpiece of Nature: The Evolution and Genetics of Sexuality (Croom Helm and Univ. California Press, London and Berkeley, 1982).References 4–6 provide exhaustive reviews of the prevalence of clonal reproduction among different taxonomic groups.

    Google Scholar 

  7. Welsh, D. M. & Meselson, M. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288, 1211–1215 (2000).

    Google Scholar 

  8. Judson, O. P. & Nomark, B. B. Ancient asexual scandals. Trends Ecol. Evol. 11, A41–A46 (1996).

    Google Scholar 

  9. Butlin, R., Schon, I. & Martens, K. Asexual reproduction in nonmarine ostracods. Heredity 81, 473–480 (1998).

    Google Scholar 

  10. Steinemann, M. & Steinemann, S. Enigma of Y chromosome degeneration: neo-Y and neo-X chromosomes of Drosophila miranda, a model for sex chromosome evolution. Genetica 103, 409–420 (1998).

    Google Scholar 

  11. Lahn, B. T. & Page, D. C. Four evolutionary strata on the human X chromosome. Science 286, 964–967 (1999).

    CAS  PubMed  Google Scholar 

  12. Lynch, M. & Blanchard, J. L. Deleterious mutation accumulation in organelle genomes. Genetica 103, 29–39 (1998).

    Google Scholar 

  13. Tilford, C. A. et al. A physical map of the human Y chromosome. Nature 409, 943–945 (2001).

    CAS  PubMed  Google Scholar 

  14. Rice, W. R. Parent–offspring pathogen transmission: a selective agent promoting sexual recombination. Am. Nat. 121, 187–203 (1983).

    Google Scholar 

  15. Kimura, M. & Maruyama, T. Mutational load with epistatic gene interactions in fitness. Genetics 54, 1303–1312 (1966).A classic reference to the theoretical concept of mutational load and how it is influenced by recombination.

    Google Scholar 

  16. Kondroshov, A. S. Deleterious mutations as an evolutionary factor. 1. The advantage of recombination. Genet. Res. 44, 199–217 (1984).

    Google Scholar 

  17. Crow, J. F. Mathematical Topics in Population Genetics (ed. Kojima, K. I.) (Springer, Heidelberg, 1970).Reviews the experimental work concerning changes in recombination rate that is associated with strong directional selection in small populations.

    Google Scholar 

  18. Rice, W. R. Requisite mutational load, pathway epistasis, and deterministic mutation accumulation in sexual versus asexual populations. Genetica 103, 71–81 (1998).

    Google Scholar 

  19. Otto, S. P. & Barton, N. H. Selection for recombination in small populations. Evolution 55, 1921–1931 (2001).

    CAS  PubMed  Google Scholar 

  20. Zeyl, C., Bell. G. & Green, D. M. Sex and the spread of retroposon Ty3 in experimental populations of Saccharomyces cerevisiae. Genetics 143, 1567–1577 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Wright, S. & Finnegan, D. Genomic evolution: sex and the transposable element. Curr. Biol. 11, R296–R299 (2001).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  23. Agrawal, A. F. Sexual selection and the maintenance of sexual reproduction. Nature 411, 692–695 (2001).

    CAS  PubMed  Google Scholar 

  24. Muller, H. J. Some genetic aspects of sex. Am. Nat. 66, 118–138 (1932).

    Google Scholar 

  25. Crow, J. F. & Kimura, M. Evolution in sexual and asexual populations. Am. Nat. 99, 439–450 (1965).

    Google Scholar 

  26. Hill, W. H. & Robertson, A. The effect of linkage on limits to artificial selection. Genet. Res. 8, 269–294 (1966).

    CAS  PubMed  Google Scholar 

  27. de Visser, J. A. G. M., Zeyl, C. W., Gerrish, P. J., Blanchard, J. L. & Lenski. R. E. Diminishing returns from mutation supply rate in asexual populations. Science 283, 404–406 (1999).

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  29. Davies, E. K. & Keightley, P. D. High frequency of cryptic deleterious mutations in Caenorhabditis elegans. Science 285, 1748–1751 (1999).Provides an empirical appraisal of the effectiveness of using the mutation accumulation technique to estimate the genome-wide mutation rate.

    CAS  PubMed  Google Scholar 

  30. Thatcher, J. W., Shaw, J. M. & Dickinson, W. J. S. Marginal fitness contributions of nonessential genes in yeast. Proc. Natl Acad. Sci. USA 95, 253–257 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Wright, S. Evolution in Mendelian populations. Genetics 16, 97–159 (1931).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Kimura, M. On the probability of fixation of mutant genes in a population. Genetics 47, 713–719 (1962).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Peck, J. R. A ruby in the rubbish: beneficial mutations, deleterious mutations and the evolution of sex. Genetics 137, 597–606 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Charlesworth, D., Charlesworth, B. & Morgan, M. T. The pattern of neutral molecular variation under the background selection model. Genetics 141, 1619–1632 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Charlesworth, B. The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet. Res. 63, 213–227 (1994).

    CAS  PubMed  Google Scholar 

  36. Barton, N. H. Linkage and the limits to natural selection. Genetics 140, 821–841 (1995).References 33–36 are key theoretical references concerning the adaptive significance of sexual recombination.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Manning, J. T. & Thompson, D. J. Muller's ratchet and the accumulation of favorable mutations. Acta Biotheor. 33, 219–225 (1984).

    Google Scholar 

  38. Rice, W. R. Evolution of the Y sex chromosome in animals. Bioscience 46, 331–343 (1996).

    Google Scholar 

  39. Li, W.-H. Maintenance of genetic variability under joint effect of mutation, selection and random drift. Genetics 90, 349–382 (1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Butcher, D. Mullers ratchet, epistasis and mutation effects. Genetics 141, 431–437 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Gessler, D. D. G. The constraints of finite size in asexual populations and the rate of the ratchet. Genet. Res. 66, 241–253 (1995).

    CAS  PubMed  Google Scholar 

  42. Rice. W. R. Genetic polarization: unifying theories for the adaptive significance of recombination. J. Evol. Biol. 12, 1047–1049 (1999).

    Google Scholar 

  43. Gordo, I. & Charlesworth, B. On the speed of Muller's ratchet. Genetics 156, 2137–2140 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Chippindale, A. K., Gibson, J. R. & Rice, W. R. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl Acad. Sci. USA 98, 1671–1675 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Drake, J. W., Charlesworth, B., Charlesworth, D. & Crow, J. F. Rates of spontaneous mutation. Genetics 148, 1667–1686 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Lynch, M. et al. Perspective: spontaneous deleterious mutation. Evolution 53, 645–663 (1999).References 45 and 46 are extensive reviews of empirical work on the genome-wide mutation rate and the fitness effects of spontaneous mutations.

    PubMed  Google Scholar 

  47. Bataillon, T. Estimation of spontaneous genome-wide mutation rate parameters: whither beneficial mutations? Heredity 84, 497–501 (2000).

    PubMed  Google Scholar 

  48. Kondrashov, A. S. Sex and U. Trends Genet. 17, 75–77 (2001).

    CAS  PubMed  Google Scholar 

  49. Keightley, P. D. & Eyre-Walker, A. Sex and U: response. Trends Genet. 17, 77–78 (2001).

    CAS  PubMed  Google Scholar 

  50. Kondrashov, A. S. & Crow, J. F. A molecular approach to estimating the human deleterious mutation rate. Hum. Mutat. 2, 229–234 (1993).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  52. Barkai, N. & Leibler, S. Robustness in simple biochemical networks. Nature 387, 913–917 (1997).

    CAS  PubMed  Google Scholar 

  53. Wiley, R. H. & Poston, J. Perspective: indirect mate choice, competition for mates, and coevolution of the sexes. Evolution 50, 1371–1381 (1996).

    PubMed  Google Scholar 

  54. Rowe, L. & Arnqvist, G. Analysis of the causal components of assortative mating in water striders. Behav. Ecol. Sociobiol. 38, 279–286 (1996).

    Google Scholar 

  55. 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  PubMed  PubMed Central  Google Scholar 

  56. Parker, G. A. in Sexual Selection and Reproductive Competition in Insects (eds Blum, M. S. & Blum, N. A.) 123–166 (Academic, New York, 1979).

    Google Scholar 

  57. Chapman, T. et al. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373, 241–244 (1995).

    CAS  PubMed  Google Scholar 

  58. Rice, W. R. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 361, 232–234 (1996).

    Google Scholar 

  59. Rice, W. R. & Holland, B. The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav. Ecol. Sociobiol. 41, 1–10 (1997).

    Google Scholar 

  60. Arnqvist, G. & Rowe, L. Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proc. R. Soc. Lond. B 261, 123–127 (1995).

    Google Scholar 

  61. Nachman, M. W. & Crowell, S. L. Estimate of the mutation rate per nucleotide in humans. Genetics 156, 297–304 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Redfield, R. J. Male mutation rates and the cost of sex for females. Nature 69, 145–147 (1994).

    Google Scholar 

  63. Petrie, M. Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371, 598–599 (1994).

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  65. Reinke, V. et al. A global profile of germline gene expression in C. elegans. Mol. Cell 6, 605–616 (2000).

    CAS  PubMed  Google Scholar 

  66. Rice, W. R. & Chippindale, A. K. Intersexual ontogenetic conflict. J. Evol. Biol. 14, 685–693 (2001).

    Google Scholar 

  67. de Visser, J. A. G. M. et al. Diminishing returns from mutation supply rate in asexual populations. Science 283, 404–406 (1999).

    CAS  Google Scholar 

  68. Miralles, R., Gerrish, P. J., Moya, A. & Elena, S. F. Clonal interference and the evolution of RNA viruses. Science 285, 1745–1747 (1999).

    CAS  PubMed  Google Scholar 

  69. Miralles, R., Moya, A. & Elena, S. F. Diminishing returns of population size in the rate of RNA virus adaptation. J. Virol. 74, 3566–3571 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. de la Pena, M., Elena. S. F. & Moya, A. Effect of deleterious mutation accumulation on the fitness of RNA bacteriophage MS2. Evolution 54, 686–691 (2000).

    CAS  PubMed  Google Scholar 

  71. Chao, L., Tran, T. R. & Matthews, C. Muller ratchet and the advantage of sex in the RNA virus-phi-6. Evolution 46, 289–299 (1992).

    PubMed  Google Scholar 

  72. Chao, L., Tran, T. T. & Tran, T. T. The advantage of sex in the RNA virus phi 6. Genetics 147, 953–959 (1997).Illustrates the capacity of non-recombining populations to rapidly recover from fitness loss, attributed to the accumulation of deleterious mutations, through the accumulation of compensatory mutations.

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Rice, W. R. Degeneration of a nonrecombining chromosome. Science 263, 230–232 (1994).

    CAS  PubMed  Google Scholar 

  74. Carson, H. L. Response to selection under different conditions of recombination in Drosophila. Cold Spring Harb. Symp. Quant. Biol. 23, 291–306 (1958).

    CAS  PubMed  Google Scholar 

  75. McPhee, C. P. & Robertson, A. Effect of suppressing crossing-over on response to selection in Drosophila melanogaster. Genet. Res. 16, 1–16 (1970).

    CAS  PubMed  Google Scholar 

  76. Markow, T. A. Genetic analysis of phototactic behavior in Drosophila melanogaster. 1. Selection in presence of inversions. Genetics 79, 527–534 (1975).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Thompson, V. Recombination and response to selection in Drosophila melanogaster. Genetics 85, 125–140 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Rice, W. R. & Chippindale, A. K. Sexual recombination and the power of natural selection. Science 294, 555–559 (2001).

    CAS  PubMed  Google Scholar 

  79. Kolkman, J. A. & Stemmer, W. P. C. Directed evolution of proteins by exon shuffling. Nature Biotechnol. 19, 423–428 (2001).

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  81. Mukai, T. Genetic structure of natural populations of Drosophila melanogaster. 1. Spontaneous mutation rate of polygenes controlling viability. Genetics 50, 1–19 (1964).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Kitagawa, O. Interactions in fitness between lethal genes in heterozygous condition in Drosophila melanogaster. Genetics 57, 809–820 (1967).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Elena, S. F. Little evidence for synergism among deleterious mutations in a nonsegmented RNA virus. J. Mol. Evol. 49, 703–707 (1999).

    CAS  PubMed  Google Scholar 

  84. de la Pena, M., Elena, S. F. & Moya, A. Effect of deleterious mutation accumulation on the fitness of RNA bacteriophage MS2. Evolution 54, 686–691 (2000).

    CAS  PubMed  Google Scholar 

  85. Peters, A. D. & Keightley, P. D. A test for epistasis among induced mutations in Caenorhabditis elegans. Genetics 156, 1635–1647 (2000).This and reference 27 describe two of the best experiments, so far, to test for epistasis among newly arisen mutations.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. deVisser, J. A. G. M., Hoekstra, R. F. & VandenEnde, H. The effect of sex and deleterious mutations on fitness in Chlamydomonas. Proc. R. Soc. Lond. B 263, 193–200 (1996).

    Google Scholar 

  87. 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 

  88. Wloch, D. M., Borts, R. H. & Korona, R. Epistatic interactions of spontaneous mutations in haploid strains of the yeast Saccharomyces cerevisiae. J. Evol. Biol. 14, 310–316 (2001).

    CAS  Google Scholar 

  89. Malmberg, R. L. Evolution of epistasis and advantage of recombination in populations of bacteriophage-T4. Genetics 86, 607–621 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Souza, V., Turner, P. E. & Lenski, R. E. Long-term experimental evolution in Escherichia coli. 5. Effects of recombination with immigrant genotypes on the rate of bacterial evolution. J. Evol. Biol. 10, 743–769 (1997).

    Google Scholar 

  91. Birdsell, J. & Wills, C. Significant competitive advantage conferred by meiosis and syngamy in the yeast Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 93, 908–912 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Greig, D., Borts. R. H. & Louis, E. J. The effect of sex on adaptation to high temperature in heterozygous and homozygous yeast. Proc. R. Soc. Lond. B 265, 1017–1023 (1998).

    CAS  Google Scholar 

  93. Zeyl, C. & Bell, G. The advantage of sex in evolving yeast populations. Nature 388, 465–468 (1997).

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Related links

Related links

FURTHER INFORMATION

William Rice's lab

Glossary

BDELLOID ROTIFERS

Microscopic organisms that seem to have experienced a period of evolution without sex, and probably without other forms of recombination, for more than 80 million years.

MUTATIONAL LOAD

The fitness reduction of a population owing to accumulated deleterious mutations in the gene pool.

ANTAGONISTIC COEVOLUTION

A cycle of adaptation and counter-adaptation between males and females of the same species or between a species and its enemies.

SEXUALLY ANTAGONISTIC FITNESS VARIATION

Variation in polymorphic genes that increase the fitness of one sex but decrease the fitness of the other sex.

REQUISITE MUTATIONAL LOAD

The excess in the net reproductive rate of the fittest class, above exact replacement, that is required to prevent open-ended mutation accumulation.

SEXUAL SELECTION

Competition among members of one sex (generally males) for fertilization opportunities with the other sex.

FIXATION

The accumulation of a mutation to a frequency of 100% in a gene pool.

CLONAL INTERFERENCE

The reduced competitive advantage of a clone that carries a beneficial mutation owing to the simultaneous presence of one or more other clones that carry different beneficial mutations.

DIRECT SELECTION

Darwinian selection on a specific mutation.

MULLER'S RATCHET

Recurrent stochastic loss of the fittest genomes in an asexual population.

CENSUS SIZE

The total number of individuals in a population.

SELECTIVE SWEEP

The gradual accumulation to fixation of a genome or chromosomal region that has a net selective advantage.

EFFECTIVE POPULATION SIZE

The equivalent number of breeding adults in a population after adjusting for complicating factors such as nonrandom variation in family size or stochastic fluctuation in population size.

HERITABILITY

The fraction of the phenotypic variance that is attributable to additive genetic variance

GENE CONVERSION

The non-reciprocal transfer of genetic information between homologous genes (as a consequence of mismatch repair after heteroduplex formation).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rice, W. Experimental tests of the adaptive significance of sexual recombination. Nat Rev Genet 3, 241–251 (2002). https://doi.org/10.1038/nrg760

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrg760

This article is cited by

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