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.

Evolution of sex

The costs and benefits of sex: new insights from old asexual lineages

Abstract

Discussions that are aimed at understanding the maintenance of sexual reproduction are in a bit of a quagmire owing to the many competing theories that have been proposed. Also, one of the central observations — that asexual lineages are typically short lived — still needs to be properly quantified. Exciting new results on ancient asexual organisms show that lineages can persist for many millions of generations without recombination. Understanding how they do so might well provide crucial new insights into the problem of sex.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Inferring the age of asexual lineages.
Figure 2: Candidate ancient asexuals.
Figure 3: Maximum-likelihood gene trees for hsp82 in rotifers.

References

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

    CAS  Article  PubMed  Google Scholar 

  2. Burt, A. Perspective: sex, recombination and the efficacy of selection — was Weismann right? Evolution 54, 337–351 (2000).

    CAS  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  5. Doncaster, C. P., Pound, G. E. & Cox, S. J. The ecological cost of sex. Nature 404, 281–285 (2000).

    CAS  Article  PubMed  Google Scholar 

  6. West, S. A. & Peters, A. D. Paying for sex is not easy. Nature 407, 962 (2000).

    CAS  Article  PubMed  Google Scholar 

  7. West, S. A., Lively, C. M. & Read, A. F. A pluralist approach to sex and recombination. J. Evol. Biol. 12, 1003–1012 (1998).

    Article  Google Scholar 

  8. Brookfield, J. F. Y. Explanation and prediction and the maintenance of sexual reproduction. J. Evol. Biol. 12, 1017–1019 (1999).

    Article  Google Scholar 

  9. Falush, D. Measuring the benefits of sex. J. Evol. Biol. 12, 1026–1028 (1999).

    Article  Google Scholar 

  10. Gouyon, P.-H. Sex: a pluralist approach includes species selection (one step beyond and it's good). J. Evol. Biol. 12, 1029–1030 (1999).

    Article  Google Scholar 

  11. Nunney, L. The maintenance of sex by group selection. Evolution 43, 245–257 (1989).

    Article  PubMed  Google Scholar 

  12. Rispe, C., Pierre, J.-S., Simon, J.-C. & Gouyon, P.-H. Models of sexual and asexual coexistence in aphids based on constraints. J. Evol. Biol. 11, 685–701 (1998).

    Article  Google Scholar 

  13. Bell, G. The Masterpiece of Nature: the Evolution and Genetics of Sexuality (Croom Helm, London, 1982).

    Google Scholar 

  14. Barton, N. H. & Charlesworth, B. Why sex and recombination? Science 281, 1986–1990 (1998).

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  18. Peters, A. D. & Keightley, P. D. A test for epistasis among induced mutations in Caenorhabditis elegans. Genetics 156, 1635–1647 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 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  PubMed  Google Scholar 

  20. Horne, D. J. & Martens, K. Geographical parthenogenesis in European non-marine ostracods: post-glacial invasion or Holocene stability? Hydrobiologia 391, 1–7 (1998).

    Article  Google Scholar 

  21. Peck, J. R., Yearsley, J. M. & Waxman, D. Explaining the geographical distributions of sexual and asexual populations. Nature 391, 889–892 (1998).

    CAS  Article  Google Scholar 

  22. Grimanelli, D., Leblanc, O., Perotti, E. & Grossniklaus, U. Developmental genetics of gametophytic apomixis. Trends Genet. 17, 597–604 (2001).

    CAS  Article  PubMed  Google Scholar 

  23. Avise, J. C., Quattro, J. M. & Vrijenhoek, R. C. Molecular clones within organismal clones: mitochondrial DNA phylogenies and the evolutionary histories of unisexual vertebrates. Evol. Biol. 26, 225–246 (1992).

    CAS  Article  Google Scholar 

  24. Butlin, R. K., Schön, I. & Martens, K. Origin, age and diversity of clones. J. Evol. Biol. 12, 1020–1022 (1999).

    Article  Google Scholar 

  25. Maynard Smith, J. Age and the unisexual lineage. Nature 256, 661–662 (1992).

    Article  Google Scholar 

  26. Martens, K. (ed.) Sex and Parthenogenesis: Evolutionary Ecology of Reproductive Modes in Non-Marine Ostracods (Backhuys Publ., Amsterdam, 1998).

    Google Scholar 

  27. Schön, I. et al. Long-term persistence of asexuality through mixed reproduction in Eucypris virens (Crustacea, Ostracoda). Heredity 84, 161–169 (2000).

    Article  PubMed  Google Scholar 

  28. Butlin, R. K., Schön, I. & Martens, K. Asexual reproduction in non-marine ostracods. Heredity 81, 473–480 (1998).

    Article  Google Scholar 

  29. Judson, O. P. & Normark, B. B. Ancient asexuals. Trends Ecol. Evol. 11, 41–46 (1996).

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  31. Rossetti, G. & Martens, K. Taxonomic revision of the Recent and Holocene representatives of the family Darwinulidae (Crustacea, Ostracoda), with a description of three new genera. Bull. K. Belg. Inst. Natuurw. Biologie 68, 55–110 (1998).

    Google Scholar 

  32. Judson, O. P. & Normark, B. B. Sinless originals. Science 288, 1185–1186 (2000).

    CAS  Article  PubMed  Google Scholar 

  33. Butlin, R. K. Virgin rotifers. Trends Ecol. Evol. 15, 389–390 (2000).

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  35. Hickey, D. A. Selfish DNA — a sexually-transmitted nuclear parasite. Genetics 101, 519–531 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Arkhipova, I. & Meselson, M. Transposable elements in sexual and ancient asexual taxa. Proc. Natl Acad. Sci. USA 98, 14473–14477 (2000).

    Article  Google Scholar 

  37. Schon, I. & Martens, K. Transposable elements and asexual reproduction. Trends Ecol. Evol. 15, 287–288 (2000).

    CAS  Article  PubMed  Google Scholar 

  38. Mark Welch, D. & Meselson, M. Rates of nucleotide substitution in sexual and anciently asexual rotifers. Proc. Natl Acad. Sci. USA 98, 6720–6724 (2001).

    CAS  Article  PubMed  Google Scholar 

  39. Schön, I., Butlin, R. K., Griffiths, H. I. & Martens, K. Slow molecular evolution in an ancient asexual ostracod. Proc. R. Soc. Lond. B 265, 235–242 (1998).

    Article  Google Scholar 

  40. Schön, I. & Martens, K. Opinion: DNA repair in ancient asexuals — a new solution for an old problem? J. Nat. Hist. 32, 943–948 (1998).

    Article  Google Scholar 

  41. Birky, C. W. Jr. Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144, 427–437 (1996).

    PubMed  Google Scholar 

  42. Okubo, I. Freshwater ostracod Darwinula stevensoni from Lake Biwa. Bull. Biogeogr. Soc. Jpn 56, 39-43 (2001).

    Google Scholar 

Download references

Acknowledgements

I am very grateful to D. Mark Welch, K. Martens, I. Schön, S. West and an anonymous referee for their insightful comments on earlier drafts of this article.

Author information

Authors and Affiliations

Authors

Related links

Related links

FURTHER INFORMATION

Sex: advantage

 Resource for phylogenetic software packages

The Meselson home page

Glossary

ALLOTETRAPLOID

A polyploid of hybrid origin in which there are four copies of each homologous chromosome per cell, two derived from each parent species.

ANISOGAMOUS

A form of reproduction in which the male gametes are a different size to the female gametes.

APOMIXIS

Reproduction that is exclusively through mitotic cell division, with no form of meiosis.

BOOTSTRAP ANALYSIS

A type of statistical analysis to test the reliability of certain branches in the evolutionary tree. The bootstrap proceeds by re-sampling the original data, with replacement, to create a series of bootstrap samples of the same size as the original data. The bootstrap value of a node is the percentage of times that a node is present in the set of trees that is constructed from the new data sets.

CLADE SELECTION

A clade is a lineage of organisms/alleles comprising an ancestor and its descendants. Clade selection is a form of group selection arising when a trait alters the probability of extinction of lineages that carry it, or the rate of production of new lineages, relative to those lineages that do not have the trait.

FOURFOLD DEGENERATE SITE

The position in a coding region of DNA sequence at which the presence of any of the four bases is translated into the same amino acid.

GENE CONVERSION

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

MOLECULAR CLOCK

The principle that any gene or protein has a near-constant rate of evolution in all branches of a clade, which means that the amount of sequence divergence between two sequences will be proportional to the amount of time elapsed since their shared ancestor existed.

MONOGONONT

A member of the rotifer class Monogononta, the sister clade to the Bdelloidea. They are cyclical parthenogens.

MULLER'S RATCHET

The irreversible accumulation of deleterious mutations in asexual populations of finite size. The average load of mutations increases over generations because the class of individuals that carry the smallest number of mutant alleles is occasionally lost by genetic drift. In the absence of recombination, this class can never be re-created.

NEGATIVE EPISTASIS

The increase in the harmful effect of a mutation when other deleterious mutations are simultaneously present in a genome.

PARSIMONY

The principle that, as trait changes during evolution are rare, the hypothesis that minimizes the number of events that are required to explain the current distribution of a trait should be preferred.

PARTHENOGENESIS

The production of offspring by a female with no genetic contribution from a male.

RELATIVE-RATE TEST

A method for testing for constancy of base substitution rate in part of an evolutionary tree. If species A and B are sister taxa and C is an outgroup, then the number of substitutions that separate the pairs AC and BC are expected to be equal.

VARIANCE

A measure of the variation around the central class of a distribution (the average squared deviation of the observations from their mean value).

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Butlin, R. The costs and benefits of sex: new insights from old asexual lineages. Nat Rev Genet 3, 311–317 (2002). https://doi.org/10.1038/nrg749

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrg749

Further reading

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