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. 2004 Jan;166(1):19–24. doi: 10.1534/genetics.166.1.19

Drift increases the advantage of sex in RNA bacteriophage Phi6.

Art Poon 1, Lin Chao 1
PMCID: PMC1470714  PMID: 15020402

Abstract

The pervasiveness of sex and recombination remains one of the most enigmatic problems in evolutionary biology. According to many theoretical models, recombination can increase the rate of adaptation by restoring genetic variation. However, the potential for genetic drift to generate conditions that produce this outcome has yet to be studied experimentally. We have designed and performed an experiment that reveals the effects of drift on existing genetic variation by minimizing the influence of variation on beneficial mutation rate. Our experiment was conducted in populations of RNA bacteriophage Phi6 initiated from a common source population at varying bottleneck sizes. The segmented genome of this virus results in genetic exchange between viruses that co-infect the same host cell. In response to selection for growth in a high-temperature environment, sexual lines outperformed their asexual counterparts on average. The advantage of sex attenuated with increasing effective population size, implying that the rate of adaptation was limited by clonal interference among segments caused by drift. This is the first empirical evidence that the advantage of sex during adaptation increases with the intensity of drift.

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Selected References

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  1. Awadalla Philip. The evolutionary genomics of pathogen recombination. Nat Rev Genet. 2003 Jan;4(1):50–60. doi: 10.1038/nrg964. [DOI] [PubMed] [Google Scholar]
  2. Barton N. H. A general model for the evolution of recombination. Genet Res. 1995 Apr;65(2):123–145. doi: 10.1017/s0016672300033140. [DOI] [PubMed] [Google Scholar]
  3. Bergstrom C. T., McElhany P., Real L. A. Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5095–5100. doi: 10.1073/pnas.96.9.5095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chao L., Tran T. T., Tran T. T. The advantage of sex in the RNA virus phi6. Genetics. 1997 Nov;147(3):953–959. doi: 10.1093/genetics/147.3.953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Colegrave Nick. Sex releases the speed limit on evolution. Nature. 2002 Dec 12;420(6916):664–666. doi: 10.1038/nature01191. [DOI] [PubMed] [Google Scholar]
  6. Drake J. W. Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4171–4175. doi: 10.1073/pnas.90.9.4171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eshel I., Feldman M. W. On the evolutionary effect of recombination. Theor Popul Biol. 1970 May;1(1):88–100. doi: 10.1016/0040-5809(70)90043-2. [DOI] [PubMed] [Google Scholar]
  8. Hill W. G., Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966 Dec;8(3):269–294. [PubMed] [Google Scholar]
  9. Holland J. J., De La Torre J. C., Steinhauer D. A. RNA virus populations as quasispecies. Curr Top Microbiol Immunol. 1992;176:1–20. doi: 10.1007/978-3-642-77011-1_1. [DOI] [PubMed] [Google Scholar]
  10. Kimura M. A stochastic model concerning the maintenance of genetic variability in quantitative characters. Proc Natl Acad Sci U S A. 1965 Sep;54(3):731–736. doi: 10.1073/pnas.54.3.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lai M. M. RNA recombination in animal and plant viruses. Microbiol Rev. 1992 Mar;56(1):61–79. doi: 10.1128/mr.56.1.61-79.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Mindich L. Precise packaging of the three genomic segments of the double-stranded-RNA bacteriophage phi6. Microbiol Mol Biol Rev. 1999 Mar;63(1):149–160. doi: 10.1128/mmbr.63.1.149-160.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mindich L., Sinclair J. F., Levine D., Cohen J. Genetic studies of temperature-sensitive and nonsense mutants of bacteriophage phi6. Virology. 1976 Nov;75(1):218–223. doi: 10.1016/0042-6822(76)90020-9. [DOI] [PubMed] [Google Scholar]
  14. Onodera S., Qiao X., Qiao J., Mindich L. Directed changes in the number of double-stranded RNA genomic segments in bacteriophage phi6. Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3920–3924. doi: 10.1073/pnas.95.7.3920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Otto S. P., Barton N. H. Selection for recombination in small populations. Evolution. 2001 Oct;55(10):1921–1931. doi: 10.1111/j.0014-3820.2001.tb01310.x. [DOI] [PubMed] [Google Scholar]
  16. Otto Sarah P., Lenormand Thomas. Resolving the paradox of sex and recombination. Nat Rev Genet. 2002 Apr;3(4):252–261. doi: 10.1038/nrg761. [DOI] [PubMed] [Google Scholar]
  17. Peck J. R., Waxman D. Mutation and sex in a competitive world. Nature. 2000 Jul 27;406(6794):399–404. doi: 10.1038/35019055. [DOI] [PubMed] [Google Scholar]
  18. Rice William R. Experimental tests of the adaptive significance of sexual recombination. Nat Rev Genet. 2002 Apr;3(4):241–251. doi: 10.1038/nrg760. [DOI] [PubMed] [Google Scholar]
  19. Steinhauer David A., Skehel John J. Genetics of influenza viruses. Annu Rev Genet. 2002 Jun 11;36:305–332. doi: 10.1146/annurev.genet.36.052402.152757. [DOI] [PubMed] [Google Scholar]
  20. Szathmáry E. Do deleterious mutations act synergistically? Metabolic control theory provides a partial answer. Genetics. 1993 Jan;133(1):127–132. doi: 10.1093/genetics/133.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Worobey M., Holmes E. C. Evolutionary aspects of recombination in RNA viruses. J Gen Virol. 1999 Oct;80(Pt 10):2535–2543. doi: 10.1099/0022-1317-80-10-2535. [DOI] [PubMed] [Google Scholar]

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