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. 2003 Dec;165(4):2167–2179. doi: 10.1093/genetics/165.4.2167

On the evolutionary advantage of fitness-associated recombination.

Lilach Hadany 1, Tuvik Beker 1
PMCID: PMC1462912  PMID: 14704195

Abstract

The adaptive value of recombination remains something of a puzzle. One of the basic problems is that recombination not only creates new and advantageous genetic combinations, but also breaks down existing good ones. A negative correlation between the fitness of an individual and its recombination rate would result in prolonged integrity of fitter genetic combinations while enabling less fit ones to produce new combinations. Such a correlation could be mediated by various factors, including stress responses, age, or direct DNA damage. For haploid population models, we show that an allele for such fitness-associated recombination (FAR) can spread both in asexual populations and in populations reproducing sexually at any uniform recombination rate. FAR also carries an advantage for the population as a whole, resulting in a higher average fitness at mutation-selection balance. These results are demonstrated in populations adapting to new environments as well as in well-adapted populations coping with deleterious mutations. Current experimental results providing evidence for the existence of FAR in nature are discussed.

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Selected References

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  1. Abdullah M. F., Borts R. H. Meiotic recombination frequencies are affected by nutritional states in Saccharomycescerevisiae. Proc Natl Acad Sci U S A. 2001 Nov 27;98(25):14524–14529. doi: 10.1073/pnas.201529598. [DOI] [PMC free article] [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. Bernstein C. Damage in DNA of an infecting phage T4 shifts reproduction from asexual to sexual allowing rescue of its genes. Genet Res. 1987 Jun;49(3):183–189. doi: 10.1017/s0016672300027063. [DOI] [PubMed] [Google Scholar]
  4. Bernstein C., Johns V. Sexual reproduction as a response to H2O2 damage in Schizosaccharomyces pombe. J Bacteriol. 1989 Apr;171(4):1893–1897. doi: 10.1128/jb.171.4.1893-1897.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chandley A. C. The effect of x-rays on female germ cells of Drosophila melanogaster. 3. A comparison with heat-treatment on crossing-over in the X-chromosome. Mutat Res. 1968 Jan-Feb;5(1):93–107. doi: 10.1016/0027-5107(68)90083-3. [DOI] [PubMed] [Google Scholar]
  6. Charlesworth B. Recombination modification in a flucturating environment. Genetics. 1976 May;83(1):181–195. doi: 10.1093/genetics/83.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clark A. G., Feldman M. W. Disequilibrium between linked inversions: an alternative hypothesis. Heredity (Edinb) 1981 Jun;46(3):379–390. doi: 10.1038/hdy.1981.46. [DOI] [PubMed] [Google Scholar]
  8. Crow J. F. How much do we know about spontaneous human mutation rates? Environ Mol Mutagen. 1993;21(2):122–129. doi: 10.1002/em.2850210205. [DOI] [PubMed] [Google Scholar]
  9. Davis L., Smith G. R. Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe. Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8395–8402. doi: 10.1073/pnas.121005598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Drake J. W., Charlesworth B., Charlesworth D., Crow J. F. Rates of spontaneous mutation. Genetics. 1998 Apr;148(4):1667–1686. doi: 10.1093/genetics/148.4.1667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dubnau D. Genetic competence in Bacillus subtilis. Microbiol Rev. 1991 Sep;55(3):395–424. doi: 10.1128/mr.55.3.395-424.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Fabre F., Roman H. Genetic evidence for inducibility of recombination competence in yeast. Proc Natl Acad Sci U S A. 1977 Apr;74(4):1667–1671. doi: 10.1073/pnas.74.4.1667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Feldman M. W., Otto S. P., Christiansen F. B. Population genetic perspectives on the evolution of recombination. Annu Rev Genet. 1996;30:261–295. doi: 10.1146/annurev.genet.30.1.261. [DOI] [PubMed] [Google Scholar]
  15. Gessler D. D., Xu S. Meiosis and the evolution of recombination at low mutation rates. Genetics. 2000 Sep;156(1):449–456. doi: 10.1093/genetics/156.1.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Golub E. I., Low K. B. Indirect stimulation of genetic recombination. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1401–1405. doi: 10.1073/pnas.80.5.1401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Grell R. F. A Comparison of Heat and Interchromosomal Effects on Recombination and Interference in DROSOPHILA MELANOGASTER. Genetics. 1978 May;89(1):65–77. doi: 10.1093/genetics/89.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hadany L., Beker T. Fitness-associated recombination on rugged adaptive landscapes. J Evol Biol. 2003 Sep;16(5):862–870. doi: 10.1046/j.1420-9101.2003.00586.x. [DOI] [PubMed] [Google Scholar]
  19. Jarmer Hanne, Berka Randy, Knudsen Steen, Saxild Hans H. Transcriptome analysis documents induced competence of Bacillus subtilis during nitrogen limiting conditions. FEMS Microbiol Lett. 2002 Jan 10;206(2):197–200. doi: 10.1111/j.1574-6968.2002.tb11009.x. [DOI] [PubMed] [Google Scholar]
  20. Kassir Y., Granot D., Simchen G. IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell. 1988 Mar 25;52(6):853–862. doi: 10.1016/0092-8674(88)90427-8. [DOI] [PubMed] [Google Scholar]
  21. Kon N., Krawchuk M. D., Warren B. G., Smith G. R., Wahls W. P. Transcription factor Mts1/Mts2 (Atf1/Pcr1, Gad7/Pcr1) activates the M26 meiotic recombination hotspot in Schizosaccharomyces pombe. Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13765–13770. doi: 10.1073/pnas.94.25.13765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kondrashov A. S. Deleterious mutations and the evolution of sexual reproduction. Nature. 1988 Dec 1;336(6198):435–440. doi: 10.1038/336435a0. [DOI] [PubMed] [Google Scholar]
  23. Kupiec M. Damage-induced recombination in the yeast Saccharomyces cerevisiae. Mutat Res. 2000 Jun 30;451(1-2):91–105. doi: 10.1016/s0027-5107(00)00042-7. [DOI] [PubMed] [Google Scholar]
  24. Lewontin R. C. The effect of genetic linkage on the mean fitness of a population. Proc Natl Acad Sci U S A. 1971 May;68(5):984–986. doi: 10.1073/pnas.68.5.984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Liberman U., Feldman M. W. Modifiers of mutation rate: a general reduction principle. Theor Popul Biol. 1986 Aug;30(1):125–142. doi: 10.1016/0040-5809(86)90028-6. [DOI] [PubMed] [Google Scholar]
  26. Mai B., Breeden L. CLN1 and its repression by Xbp1 are important for efficient sporulation in budding yeast. Mol Cell Biol. 2000 Jan;20(2):478–487. doi: 10.1128/mcb.20.2.478-487.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Michod R. E. Origin of sex for error repair. III. Selfish sex. Theor Popul Biol. 1998 Feb;53(1):60–74. doi: 10.1006/tpbi.1997.1341. [DOI] [PubMed] [Google Scholar]
  28. Nei M. Modification of linkage intensity by natural selection. Genetics. 1967 Nov;57(3):625–641. doi: 10.1093/genetics/57.3.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nevo E. Evolution in action across phylogeny caused by microclimatic stresses at "Evolution Canyon". Theor Popul Biol. 1997 Dec;52(3):231–243. doi: 10.1006/tpbi.1997.1330. [DOI] [PubMed] [Google Scholar]
  30. REID D. H., PARSONS P. A. Sex of parent and variation of recombination with age in the mouse. Heredity (Edinb) 1963 Feb;18:107–108. doi: 10.1038/hdy.1963.9. [DOI] [PubMed] [Google Scholar]
  31. Redfield R. J. Evolution of bacterial transformation: is sex with dead cells ever better than no sex at all? Genetics. 1988 May;119(1):213–221. doi: 10.1093/genetics/119.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Redfield R. J. Genes for breakfast: the have-your-cake-and-eat-it-too of bacterial transformation. J Hered. 1993 Sep-Oct;84(5):400–404. doi: 10.1093/oxfordjournals.jhered.a111361. [DOI] [PubMed] [Google Scholar]
  33. Smith G. R. Homologous recombination near and far from DNA breaks: alternative roles and contrasting views. Annu Rev Genet. 2001;35:243–274. doi: 10.1146/annurev.genet.35.102401.090509. [DOI] [PubMed] [Google Scholar]
  34. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  35. Takeda T., Toda T., Kominami K., Kohnosu A., Yanagida M., Jones N. Schizosaccharomyces pombe atf1+ encodes a transcription factor required for sexual development and entry into stationary phase. EMBO J. 1995 Dec 15;14(24):6193–6208. doi: 10.1002/j.1460-2075.1995.tb00310.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Watanabe Y., Yamamoto M. Schizosaccharomyces pombe pcr1+ encodes a CREB/ATF protein involved in regulation of gene expression for sexual development. Mol Cell Biol. 1996 Feb;16(2):704–711. doi: 10.1128/mcb.16.2.704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. White M. A., Dominska M., Petes T. D. Transcription factors are required for the meiotic recombination hotspot at the HIS4 locus in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6621–6625. doi: 10.1073/pnas.90.14.6621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wojciechowski M. F., Hoelzer M. A., Michod R. E. DNA repair and the evolution of transformation in Bacillus subtilis. II. Role of inducible repair. Genetics. 1989 Mar;121(3):411–422. doi: 10.1093/genetics/121.3.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Young Jennifer A., Schreckhise Randall W., Steiner Walter W., Smith Gerald R. Meiotic recombination remote from prominent DNA break sites in S. pombe. Mol Cell. 2002 Feb;9(2):253–263. doi: 10.1016/s1097-2765(02)00452-5. [DOI] [PubMed] [Google Scholar]

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