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Interference among deleterious mutations favours sex and recombination in finite populations

Naturevolume 443, pages89–92 (2006)Cite this article

Abstract

Sex and recombination are widespread, but explaining these phenomena has been one of the most difficult problems in evolutionary biology. Recombination is advantageous when different individuals in a population carry different advantageous alleles1,2. By bringing together advantageous alleles onto the same chromosome, recombination speeds up the process of adaptation1,3,4,5 and opposes the fixation of harmful mutations by means of Muller's ratchet4,5. Nevertheless, adaptive substitutions favour sex and recombination only if the rate of adaptive mutation is high1,6, and Muller's ratchet operates only in small or asexual populations7. Here, by tracking the fate of modifier alleles that alter the frequency of sex and recombination, we show that background selection against deleterious mutant alleles provides a stochastic advantage to sex and recombination that increases with population size. The advantage arises because, with low levels of recombination, selection at other loci severely reduces the effective population size and genetic variance in fitness at a focal locus8 (the Hill–Robertson effect), making a population less able to respond to selection and to rid itself of deleterious mutations. Sex and recombination reveal the hidden genetic variance in fitness by combining chromosomes of intermediate fitness to create chromosomes that are relatively free of (or are loaded with) deleterious mutations. This increase in genetic variance within finite populations improves the response to selection and generates a substantial advantage to sex and recombination that is fairly insensitive to the form of epistatic interactions between deleterious alleles. The mechanism supported by our results offers a robust and broadly applicable explanation for the evolutionary advantage of recombination and can explain the spread of costly sex.

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Figure 1:Effect of model parameters on flux of modifiers of recombination.
Figure 2:Effect of model parameters on flux of modifiers of sex.
Figure 3:Effect of background selection on effective population size.
Figure 4:The long-term evolution of recombination allowing recurrent mutation at modifier loci.

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Acknowledgements

We thank E. Santiago and A. Caballero for advice on predicting effective population size; N. Barton, A. Blachford, C. Haag, W. Hill, D. Roze and M. Whitlock for comments on the manuscript; and M. Blaxter for Linux cluster computing time. S.P.O. was supported by a NSERC grant (Canada).

Author information

Authors and Affiliations

  1. Institute of Evolutionary Biology, University of Edinburgh, West Mains Road, EH9 3JT, Edinburgh, UK

    Peter D. Keightley

  2. Department of Zoology, University of British Columbia, 6270 University Boulevard, British Columbia, V6T 1Z4, Vancouver, Canada

    Sarah P. Otto

Authors
  1. Peter D. Keightley

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  2. Sarah P. Otto

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Corresponding author

Correspondence toPeter D. Keightley.

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Reprints and permissions information is available atwww.nature.com/reprints. The authors declare no competing financial interests.

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This file contains supplementary Figures 1 and 2, and supplementary Tables 1–3. (PDF 946 kb)

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Keightley, P., Otto, S. Interference among deleterious mutations favours sex and recombination in finite populations.Nature443, 89–92 (2006). https://doi.org/10.1038/nature05049

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Editorial Summary

The question of sex

For decades scientists have been seeking to understand the evolutionary forces behind the emergence of sex and recombination. The need to purge deleterious mutations from the genome is one possible driving force. For this idea to be valid, deleterious mutations would probably need to exhibit negative epistasis — that is, they would act synergistically to produce a large cumulative effect. However, experimental evidence suggests that such negative epistasis is uncommon. Now, by invoking a concept called Hill–Robertson interference, Peter Keightley and Sarah Otto have developed a computer simulation that selects for recombination regardless of whether deleterious mutations exhibit epistasis. This provides a robust explanation for the evolution of recombination, and perhaps of sex.

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