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. 1997 Oct;147(2):879–906. doi: 10.1093/genetics/147.2.879

The Evolution of Recombination: Removing the Limits to Natural Selection

S P Otto 1, N H Barton 1
PMCID: PMC1208206  PMID: 9335621

Abstract

One of the oldest hypotheses for the advantage of recombination is that recombination allows beneficial mutations that arise in different individuals to be placed together on the same chromosome. Unless recombination occurs, one of the beneficial alleles is doomed to extinction, slowing the rate at which adaptive mutations are incorporated within a population. We model the effects of a modifier of recombination on the fixation probability of beneficial mutations when beneficial alleles are segregating at other loci. We find that modifier alleles that increase recombination do increase the fixation probability of beneficial mutants and subsequently hitchhike along as the mutants rise in frequency. The strength of selection favoring a modifier that increases recombination is proportional to λ(2)Sδr/r when linkage is tight and λ(2)S(3)δ r/N when linkage is loose, where λ is the beneficial mutation rate per genome per generation throughout a population of size N, S is the average mutant effect, r is the average recombination rate, and δr is the amount that recombination is modified. We conclude that selection for recombination will be substantial only if there is tight linkage within the genome or if many loci are subject to directional selection as during periods of rapid evolutionary change.

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Selected References

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  1. Altenberg L., Feldman M. W. Selection, generalized transmission and the evolution of modifier genes. I. The reduction principle. Genetics. 1987 Nov;117(3):559–572. doi: 10.1093/genetics/117.3.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker B. S., Carpenter A. T., Esposito M. S., Esposito R. E., Sandler L. The genetic control of meiosis. Annu Rev Genet. 1976;10:53–134. doi: 10.1146/annurev.ge.10.120176.000413. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Barton N. H. Linkage and the limits to natural selection. Genetics. 1995 Jun;140(2):821–841. doi: 10.1093/genetics/140.2.821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Basile G., Aker M., Mortimer R. K. Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene RAD51. Mol Cell Biol. 1992 Jul;12(7):3235–3246. doi: 10.1128/mcb.12.7.3235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Burt A., Bell G. Mammalian chiasma frequencies as a test of two theories of recombination. Nature. 1987 Apr 23;326(6115):803–805. doi: 10.1038/326803a0. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Charlesworth D., Charlesworth B., Strobeck C. Effects of selfing on selection for recombination. Genetics. 1977 May;86(1):213–226. doi: 10.1093/genetics/86.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cox M. M. Relating biochemistry to biology: how the recombinational repair function of RecA protein is manifested in its molecular properties. Bioessays. 1993 Sep;15(9):617–623. doi: 10.1002/bies.950150908. [DOI] [PubMed] [Google Scholar]
  10. Engebrecht J., Hirsch J., Roeder G. S. Meiotic gene conversion and crossing over: their relationship to each other and to chromosome synapsis and segregation. Cell. 1990 Sep 7;62(5):927–937. doi: 10.1016/0092-8674(90)90267-i. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Feldman M. W. Selection for linkage modification. I. Random mating populations. Theor Popul Biol. 1972 Sep;3(3):324–346. doi: 10.1016/0040-5809(72)90007-x. [DOI] [PubMed] [Google Scholar]
  13. Felsenstein J. The evolutionary advantage of recombination. Genetics. 1974 Oct;78(2):737–756. doi: 10.1093/genetics/78.2.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Felsenstein J., Yokoyama S. The evolutionary advantage of recombination. II. Individual selection for recombination. Genetics. 1976 Aug;83(4):845–859. doi: 10.1093/genetics/83.4.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hawley R. S., Theurkauf W. E. Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet. 1993 Sep;9(9):310–317. doi: 10.1016/0168-9525(93)90249-h. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Kirkpatrick M., Jenkins C. D. Genetic segregation and the maintenance of sexual reproduction. Nature. 1989 May 25;339(6222):300–301. doi: 10.1038/339300a0. [DOI] [PubMed] [Google Scholar]
  18. Koehler K. E., Hawley R. S., Sherman S., Hassold T. Recombination and nondisjunction in humans and flies. Hum Mol Genet. 1996;5(Spec No):1495–1504. doi: 10.1093/hmg/5.supplement_1.1495. [DOI] [PubMed] [Google Scholar]
  19. Kondrashov A. S. Classification of hypotheses on the advantage of amphimixis. J Hered. 1993 Sep-Oct;84(5):372–387. doi: 10.1093/oxfordjournals.jhered.a111358. [DOI] [PubMed] [Google Scholar]
  20. Kondrashov A. S. Selection against harmful mutations in large sexual and asexual populations. Genet Res. 1982 Dec;40(3):325–332. doi: 10.1017/s0016672300019194. [DOI] [PubMed] [Google Scholar]
  21. Korol A. B., Iliadi K. G. Increased recombination frequencies resulting from directional selection for geotaxis in Drosophila. Heredity (Edinb) 1994 Jan;72(Pt 1):64–68. doi: 10.1038/hdy.1994.7. [DOI] [PubMed] [Google Scholar]
  22. Mukai T., Chigusa S. I., Mettler L. E., Crow J. F. Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics. 1972 Oct;72(2):335–355. doi: 10.1093/genetics/72.2.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mukai T. The Genetic Structure of Natural Populations of DROSOPHILA MELANOGASTER. VII Synergistic Interaction of Spontaneous Mutant Polygenes Controlling Viability. Genetics. 1969 Mar;61(3):749–761. doi: 10.1093/genetics/61.3.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Otto S. P., Feldman M. W. Deleterious mutations, variable epistatic interactions, and the evolution of recombination. Theor Popul Biol. 1997 Apr;51(2):134–147. doi: 10.1006/tpbi.1997.1301. [DOI] [PubMed] [Google Scholar]
  26. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  27. True J. R., Mercer J. M., Laurie C. C. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics. 1996 Feb;142(2):507–523. doi: 10.1093/genetics/142.2.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Villeneuve A. M. A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics. 1994 Mar;136(3):887–902. doi: 10.1093/genetics/136.3.887. [DOI] [PMC free article] [PubMed] [Google Scholar]

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