Skip to main content

Thank you for visiting 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.

Mutation load and rapid adaptation favour outcrossing over self-fertilization


The tendency of organisms to reproduce by cross-fertilization despite numerous disadvantages relative to self-fertilization is one of the oldest puzzles in evolutionary biology. For many species, the primary obstacle to the evolution of outcrossing is the cost of production of males1, individuals that do not directly contribute offspring and thus diminish the long-term reproductive output of a lineage. Self-fertilizing (‘selfing’) organisms do not incur the cost of males and therefore should possess at least a twofold numerical advantage over most outcrossing organisms2. Two competing explanations for the widespread prevalence of outcrossing in nature despite this inherent disadvantage are the avoidance of inbreeding depression generated by selfing3,4,5 and the ability of outcrossing populations to adapt more rapidly to environmental change1,6,7. Here we show that outcrossing is favoured in populations of Caenorhabditis elegans subject to experimental evolution both under conditions of increased mutation rate and during adaptation to a novel environment. In general, fitness increased with increasing rates of outcrossing. Thus, each of the standard explanations for the maintenance of outcrossing are correct, and it is likely that outcrossing is the predominant mode of reproduction in most species because it is favoured under ecological conditions that are ubiquitous in natural environments.

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.


All prices are NET prices.

Figure 1: Experimental test of the major theories of the evolution of outcrossing.


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

    Google Scholar 

  2. Lively, C. M. & Lloyd, D. G. The cost of biparental sex under individual selection. Am. Nat. 135, 489–500 (1990)

    Article  Google Scholar 

  3. Charlesworth, D. & Charlesworth, B. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18, 237–268 (1987)

    Article  Google Scholar 

  4. Lande, R. & Schemske, D. W. The evolution of self-fertilization and inbreeding depression in plants. 1. Genetic models. Evolution 39, 24–40 (1985)

    Article  PubMed  Google Scholar 

  5. Heller, J. & Maynard Smith, J. Does Muller's Ratchet work with selfing? Genet. Res. 8, 269–294 (1979)

    Google Scholar 

  6. Stebbins, G. L. Self-fertilization and population variation in higher plants. Am. Nat. 91, 337–354 (1957)

    Article  Google Scholar 

  7. Crow, J. F. An advantage of sexual reproduction in a rapidly changing environment. J. Hered. 83, 169–173 (1992)

    CAS  Article  PubMed  Google Scholar 

  8. Fisher, R. A. Average excess and average effect of a gene substitution. Ann. Eugen. 11, 53–63 (1941)

    Article  Google Scholar 

  9. Williams, G. C. Sex and Evolution (Princeton Univ. Press, 1975)

    Google Scholar 

  10. Kondrashov, A. S. Deleterious mutations as an evolutionary factor. I. The advantage of recombination. Genet. Res. 44, 199–217 (1984)

    CAS  Article  PubMed  Google Scholar 

  11. Schultz, S. T. & Lynch, M. Mutation and extinction: the role of variable mutational effects, synergistic epistasis, beneficial mutations, and degree of outcrossing. Evolution 51, 1363–1371 (1997)

    Article  PubMed  Google Scholar 

  12. Felsenstein, J. The evolutionary advantage of recombination. Genetics 78, 737–756 (1974)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Barton, N. H. Linkage and the limits to natural selection. Genetics 140, 821–841 (1995)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Chasnov, J. R. & Chow, K. L. Why are there males in the hermaphroditic species Caenorhabditis elegans? Genetics 160, 983–994 (2002)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Stewart, A. D. & Phillips, P. C. Selection and maintenance of androdioecy in Caenorhabditis elegans . Genetics 160, 975–982 (2002)

    PubMed  PubMed Central  Google Scholar 

  16. Sivasundar, A. & Hey, J. Population genetics of Caenorhabditis elegans: the paradox of low polymorphism in a widespread species. Genetics 163, 147–157 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Barriere, A. & Felix, M. A. High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr. Biol. 15, 1176–1184 (2005)

    CAS  Article  PubMed  Google Scholar 

  18. Haber, M. et al. Evolutionary history of Caenorhabditis elegans inferred from microsatellites: evidence for spatial and temporal genetic differentiation and the occurrence of outbreeding. Mol. Biol. Evol. 22, 160–173 (2005)

    CAS  Article  PubMed  Google Scholar 

  19. Teotónio, H., Manoel, D. & Phillips, P. C. Genetic variation for outcrossing among Caenorhabditis elegans isolates. Evolution 60, 1300–1305 (2006)

    Article  PubMed  Google Scholar 

  20. Miller, L. M., Plenefisch, J. D., Casson, L. P. & Meyer, B. J. xol-1 — a gene that controls the male modes of both sex determination and X-chromosome dosage compensation in C. elegans . Cell 55, 167–183 (1988)

    CAS  Article  PubMed  Google Scholar 

  21. Schedl, T. & Kimble, J. fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans . Genetics 119, 43–61 (1988)

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Estes, S., Phillips, P. C., Denver, D. R., Thomas, W. K. & Lynch, M. Mutation accumulation in populations of varying size: the distribution of mutational effects for fitness correlates in Caenorhabditis elegans . Genetics 166, 1269–1279 (2004)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Loewe, L. & Cutter, A. D. On the potential for extinction by Muller's ratchet in Caenorhabditis elegans . BMC Evol. Biol. 8, 125 (2008)

    Article  PubMed  PubMed Central  Google Scholar 

  24. Cutter, A. D. Mutation and the experimental evolution of outcrossing in Caenorhabditis elegans . J. Evol. Biol. 18, 27–34 (2005)

    CAS  Article  PubMed  Google Scholar 

  25. Manoel, D., Carvalho, S., Phillips, P. C. & Teotónio, H. Selection against males in Caenorhabditis elegans under two mutational treatments. Proc. R. Soc. Lond. B 274, 417–424 (2007)

    Article  Google Scholar 

  26. Pradel, E. et al. Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans . Proc. Natl Acad. Sci. USA 104, 2295–2300 (2007)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Mallo, G. V. et al. Inducible antibacterial defense system in C. elegans . Curr. Biol. 12, 1209–1214 (2002)

    CAS  Article  PubMed  Google Scholar 

  28. Colegrave, N. Sex releases the speed limit on evolution. Nature 420, 664–666 (2002)

    ADS  CAS  Article  PubMed  Google Scholar 

  29. Goddard, M. R., Charles, H., Godfray, J. & Burt, A. Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434, 636–640 (2005)

    ADS  CAS  Article  PubMed  Google Scholar 

  30. Whitlock, M. C. & Agrawal, A. F. Purging the genome with sexual selection: reducing mutation load through selection on males. Evolution 63, 569–582 (2009)

    CAS  Article  PubMed  Google Scholar 

Download references


We thank S. Scholz, A. Ohdera and J. Chiem for logistical help, S. Katz for providing the S. marcescens 2170 strain, and J. Thornton for use of laboratory space and equipment. We also thank B. Cresko, C. Lively, J. Thornton and the members of the Phillips and Cresko laboratories for comments and discussion pertaining to this work. Funding was provided by NSF grants DEB-0236180, DEB-0710386 and DEB-0641066, and an NIH Genetics Fellowship awarded to L.T.M. Some nematode strains used in this work were provided by the Caenorhabditis Genetics Center, which is funded by the NIH National Center for Research Resources (NCRR).

Author Contributions L.T.M. and P.C.P. designed the experiments. L.T.M. and M.D.P. performed the experiments. L.T.M. and P.C.P. analysed the data. L.T.M. and P.C.P. wrote the paper.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Patrick C. Phillips.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Table S1, Supplementary References and Supplementary Figures S1-S2 with Legends. (PDF 1362 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Morran, L., Parmenter, M. & Phillips, P. Mutation load and rapid adaptation favour outcrossing over self-fertilization. Nature 462, 350–352 (2009).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

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.


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