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. 2003 Jul;164(3):1099–1118. doi: 10.1093/genetics/164.3.1099

The advantages of segregation and the evolution of sex.

Sarah P Otto 1
PMCID: PMC1462613  PMID: 12871918

Abstract

In diploids, sexual reproduction promotes both the segregation of alleles at the same locus and the recombination of alleles at different loci. This article is the first to investigate the possibility that sex might have evolved and been maintained to promote segregation, using a model that incorporates both a general selection regime and modifier alleles that alter an individual's allocation to sexual vs. asexual reproduction. The fate of different modifier alleles was found to depend strongly on the strength of selection at fitness loci and on the presence of inbreeding among individuals undergoing sexual reproduction. When selection is weak and mating occurs randomly among sexually produced gametes, reductions in the occurrence of sex are favored, but the genome-wide strength of selection is extremely small. In contrast, when selection is weak and some inbreeding occurs among gametes, increased allocation to sexual reproduction is expected as long as deleterious mutations are partially recessive and/or beneficial mutations are partially dominant. Under strong selection, the conditions under which increased allocation to sex evolves are reversed. Because deleterious mutations are typically considered to be partially recessive and weakly selected and because most populations exhibit some degree of inbreeding, this model predicts that higher frequencies of sex would evolve and be maintained as a consequence of the effects of segregation. Even with low levels of inbreeding, selection is stronger on a modifier that promotes segregation than on a modifier that promotes recombination, suggesting that the benefits of segregation are more likely than the benefits of recombination to have driven the evolution of sexual reproduction in diploids.

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Selected References

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  1. Agrawal A. F., Chasnov J. R. Recessive mutations and the maintenance of sex in structured populations. Genetics. 2001 Jun;158(2):913–917. doi: 10.1093/genetics/158.2.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  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., Charlesworth B. Why sex and recombination? Science. 1998 Sep 25;281(5385):1986–1990. [PubMed] [Google Scholar]
  5. Barton N. H., Turelli M. Natural and sexual selection on many loci. Genetics. 1991 Jan;127(1):229–255. doi: 10.1093/genetics/127.1.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chapman T., Liddle L. F., Kalb J. M., Wolfner M. F., Partridge L. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature. 1995 Jan 19;373(6511):241–244. doi: 10.1038/373241a0. [DOI] [PubMed] [Google Scholar]
  7. Charlesworth B., Charlesworth D. The genetic basis of inbreeding depression. Genet Res. 1999 Dec;74(3):329–340. doi: 10.1017/s0016672399004152. [DOI] [PubMed] [Google Scholar]
  8. Chasnov J. R. Mutation-selection balance, dominance and the maintenance of sex. Genetics. 2000 Nov;156(3):1419–1425. doi: 10.1093/genetics/156.3.1419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deng H. W., Lynch M. Inbreeding depression and inferred deleterious-mutation parameters in Daphnia. Genetics. 1997 Sep;147(1):147–155. doi: 10.1093/genetics/147.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dolgin Elie S., Otto Sarah P. Segregation and the evolution of sex under overdominant selection. Genetics. 2003 Jul;164(3):1119–1128. doi: 10.1093/genetics/164.3.1119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. García-Dorado A., López-Fanjul C., Caballero A. Properties of spontaneous mutations affecting quantitative traits. Genet Res. 1999 Dec;74(3):341–350. doi: 10.1017/s0016672399004206. [DOI] [PubMed] [Google Scholar]
  14. Kimura M. Attainment of Quasi Linkage Equilibrium When Gene Frequencies Are Changing by Natural Selection. Genetics. 1965 Nov;52(5):875–890. doi: 10.1093/genetics/52.5.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Kirkpatrick Mark, Johnson Toby, Barton Nick. General models of multilocus evolution. Genetics. 2002 Aug;161(4):1727–1750. doi: 10.1093/genetics/161.4.1727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Lenormand T., Otto S. P. The evolution of recombination in a heterogeneous environment. Genetics. 2000 Sep;156(1):423–438. doi: 10.1093/genetics/156.1.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Moore T., Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 1991 Feb;7(2):45–49. doi: 10.1016/0168-9525(91)90230-N. [DOI] [PubMed] [Google Scholar]
  20. Orr H. A., Otto S. P. Does diploidy increase the rate of adaptation? Genetics. 1994 Apr;136(4):1475–1480. doi: 10.1093/genetics/136.4.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Otto S. P., Goldstein D. B. Recombination and the evolution of diploidy. Genetics. 1992 Jul;131(3):745–751. doi: 10.1093/genetics/131.3.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Perrot V., Richerd S., Valéro M. Transition from haploidy to diploidy. Nature. 1991 May 23;351(6324):315–317. doi: 10.1038/351315a0. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Simmons M. J., Crow J. F. Mutations affecting fitness in Drosophila populations. Annu Rev Genet. 1977;11:49–78. doi: 10.1146/annurev.ge.11.120177.000405. [DOI] [PubMed] [Google Scholar]
  28. Uyenoyama M. K., Bengtsson B. O. On the origin of meiotic reproduction: a genetic modifier model. Genetics. 1989 Dec;123(4):873–885. doi: 10.1093/genetics/123.4.873. [DOI] [PMC free article] [PubMed] [Google Scholar]

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