Skip to main content
Genetics logoLink to Genetics
. 1995 Nov;141(3):1173–1187. doi: 10.1093/genetics/141.3.1173

Evolutionary Consequences of Mutation and Selection within an Individual

S P Otto 1, M E Orive 1
PMCID: PMC1206839  PMID: 8582622

Abstract

Whether in sexual or asexual organisms, selection among cell lineages during development is an effective way of eliminating deleterious mutations. Using a mathematical analysis, we find that relatively small differences in cell replication rates during development can translate into large differences in the proportion of mutant cells within the adult, especially when development involves a large number of cell divisions. Consequently, intraorganismal selection can substantially reduce the deleterious mutation rate observed among offspring as well as the mutation load within a population, because cells rather than individuals provide the selective ``deaths'' necessary to stem the tide of deleterious mutations. The reduction in mutation rate among offspring is more pronounced in organisms with plastic development than in those with structured development. It is also more pronounced in asexual organisms that produce multicellular rather than unicellular offspring. By effecting the mutation rate, intraorganismal selection may have broad evolutionary implications; as an example, we consider its influence on the evolution of ploidy levels, finding that cell-lineage selection is more effective in haploids and tends to favor their evolution.

Full Text

The Full Text of this article is available as a PDF (1.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amos C. I., Elston R. C. Robust methods for the detection of genetic linkage for quantitative data from pedigrees. Genet Epidemiol. 1989;6(2):349–360. doi: 10.1002/gepi.1370060205. [DOI] [PubMed] [Google Scholar]
  2. Amos C. I., Elston R. C., Wilson A. F., Bailey-Wilson J. E. A more powerful robust sib-pair test of linkage for quantitative traits. Genet Epidemiol. 1989;6(3):435–449. doi: 10.1002/gepi.1370060306. [DOI] [PubMed] [Google Scholar]
  3. Andersson L., Haley C. S., Ellegren H., Knott S. A., Johansson M., Andersson K., Andersson-Eklund L., Edfors-Lilja I., Fredholm M., Hansson I. Genetic mapping of quantitative trait loci for growth and fatness in pigs. Science. 1994 Mar 25;263(5154):1771–1774. doi: 10.1126/science.8134840. [DOI] [PubMed] [Google Scholar]
  4. Birky C. W., Jr Relaxed cellular controls and organelle heredity. Science. 1983 Nov 4;222(4623):468–475. doi: 10.1126/science.6353578. [DOI] [PubMed] [Google Scholar]
  5. Buss L. W. Evolution, development, and the units of selection. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1387–1391. doi: 10.1073/pnas.80.5.1387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buss L. W. Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc Natl Acad Sci U S A. 1982 Sep;79(17):5337–5341. doi: 10.1073/pnas.79.17.5337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Churchill G. A., Doerge R. W. Empirical threshold values for quantitative trait mapping. Genetics. 1994 Nov;138(3):963–971. doi: 10.1093/genetics/138.3.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Churchill G. A., Giovannoni J. J., Tanksley S. D. Pooled-sampling makes high-resolution mapping practical with DNA markers. Proc Natl Acad Sci U S A. 1993 Jan 1;90(1):16–20. doi: 10.1073/pnas.90.1.16. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Darvasi A., Soller M. Selective DNA pooling for determination of linkage between a molecular marker and a quantitative trait locus. Genetics. 1994 Dec;138(4):1365–1373. doi: 10.1093/genetics/138.4.1365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dearolf C. R., Hersperger E., Shearn A. Developmental consequences of awdb3, a cell-autonomous lethal mutation of Drosophila induced by hybrid dysgenesis. Dev Biol. 1988 Sep;129(1):159–168. doi: 10.1016/0012-1606(88)90170-4. [DOI] [PubMed] [Google Scholar]
  11. Fulker D. W., Cardon L. R. A sib-pair approach to interval mapping of quantitative trait loci. Am J Hum Genet. 1994 Jun;54(6):1092–1103. [PMC free article] [PubMed] [Google Scholar]
  12. Goldgar D. E. Multipoint analysis of human quantitative genetic variation. Am J Hum Genet. 1990 Dec;47(6):957–967. [PMC free article] [PubMed] [Google Scholar]
  13. Goldgar D. E., Oniki R. S. Comparison of a multipoint identity-by-descent method with parametric multipoint linkage analysis for mapping quantitative traits. Am J Hum Genet. 1992 Mar;50(3):598–606. [PMC free article] [PubMed] [Google Scholar]
  14. Haldane J B, Waddington C H. Inbreeding and Linkage. Genetics. 1931 Jul;16(4):357–374. doi: 10.1093/genetics/16.4.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Haley C. S., Knott S. A. A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity (Edinb) 1992 Oct;69(4):315–324. doi: 10.1038/hdy.1992.131. [DOI] [PubMed] [Google Scholar]
  16. Haley C. S., Knott S. A. A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity (Edinb) 1992 Oct;69(4):315–324. doi: 10.1038/hdy.1992.131. [DOI] [PubMed] [Google Scholar]
  17. Haley C. S., Knott S. A., Elsen J. M. Mapping quantitative trait loci in crosses between outbred lines using least squares. Genetics. 1994 Mar;136(3):1195–1207. doi: 10.1093/genetics/136.3.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Haseman J. K., Elston R. C. The investigation of linkage between a quantitative trait and a marker locus. Behav Genet. 1972 Mar;2(1):3–19. doi: 10.1007/BF01066731. [DOI] [PubMed] [Google Scholar]
  19. Jansen R. C. Controlling the type I and type II errors in mapping quantitative trait loci. Genetics. 1994 Nov;138(3):871–881. doi: 10.1093/genetics/138.3.871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jansen R. C. Interval mapping of multiple quantitative trait loci. Genetics. 1993 Sep;135(1):205–211. doi: 10.1093/genetics/135.1.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jansen R. C. Interval mapping of multiple quantitative trait loci. Genetics. 1993 Sep;135(1):205–211. doi: 10.1093/genetics/135.1.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jansen R. C., Stam P. High resolution of quantitative traits into multiple loci via interval mapping. Genetics. 1994 Apr;136(4):1447–1455. doi: 10.1093/genetics/136.4.1447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Khatib H., Darvasi A., Plotski Y., Soller M. Determining relative microsatellite allele frequencies in pooled DNA samples. PCR Methods Appl. 1994 Aug;4(1):13–18. doi: 10.1101/gr.4.1.13. [DOI] [PubMed] [Google Scholar]
  24. Kimura M., Maruyama T. The mutational load with epistatic gene interactions in fitness. Genetics. 1966 Dec;54(6):1337–1351. doi: 10.1093/genetics/54.6.1337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Knott S. A., Haley C. S. Maximum likelihood mapping of quantitative trait loci using full-sib families. Genetics. 1992 Dec;132(4):1211–1222. doi: 10.1093/genetics/132.4.1211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Lander E. S., Botstein D. Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics. 1989 Jan;121(1):185–199. doi: 10.1093/genetics/121.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lander E. S., Botstein D. Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics. 1989 Jan;121(1):185–199. doi: 10.1093/genetics/121.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lenski R. E., Slatkin M., Ayala F. J. Mutation and selection in bacterial populations: alternatives to the hypothesis of directed mutation. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2775–2778. doi: 10.1073/pnas.86.8.2775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. McMillan I., Robertson A. The power of methods for the detection of major genes affecting quantitative characters. Heredity (Edinb) 1974 Jun;32(3):349–356. doi: 10.1038/hdy.1974.43. [DOI] [PubMed] [Google Scholar]
  31. Moyret C., Madsen M. W., Cooke J., Briand P., Theillet C. Gradual selection of a cellular clone presenting a mutation at codon 179 of the p53 gene during establishment of the immortalized human breast epithelial cell line HMT-3522. Exp Cell Res. 1994 Dec;215(2):380–385. doi: 10.1006/excr.1994.1355. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Olson J. M., Wijsman E. M. Linkage between quantitative trait and marker loci: methods using all relative pairs. Genet Epidemiol. 1993;10(2):87–102. doi: 10.1002/gepi.1370100202. [DOI] [PubMed] [Google Scholar]
  35. Orr H. A. Somatic mutation favors the evolution of diploidy. Genetics. 1995 Mar;139(3):1441–1447. doi: 10.1093/genetics/139.3.1441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Pacek P., Sajantila A., Syvänen A. C. Determination of allele frequencies at loci with length polymorphism by quantitative analysis of DNA amplified from pooled samples. PCR Methods Appl. 1993 May;2(4):313–317. doi: 10.1101/gr.2.4.313. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Rand D. M., Harrison R. G. Mitochondrial DNA transmission genetics in crickets. Genetics. 1986 Nov;114(3):955–970. doi: 10.1093/genetics/114.3.955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sax K. The Association of Size Differences with Seed-Coat Pattern and Pigmentation in PHASEOLUS VULGARIS. Genetics. 1923 Nov;8(6):552–560. doi: 10.1093/genetics/8.6.552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Schork N. J. Extended multipoint identity-by-descent analysis of human quantitative traits: efficiency, power, and modeling considerations. Am J Hum Genet. 1993 Dec;53(6):1306–1319. [PMC free article] [PubMed] [Google Scholar]
  42. Thompson J. N., Jr Quantitative variation and gene number. Nature. 1975 Dec 25;258(5537):665–668. doi: 10.1038/258665a0. [DOI] [PubMed] [Google Scholar]
  43. Thrailkill K. M., Birky C. W., Jr Intracellular population genetics: evidence for random drift of mitochondrial allele frequencies in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Genetics. 1980 Sep;96(1):237–262. doi: 10.1093/genetics/96.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Van Arendonk J. A., Tier B., Kinghorn B. P. Use of multiple genetic markers in prediction of breeding values. Genetics. 1994 May;137(1):319–329. doi: 10.1093/genetics/137.1.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Weller J. I. Maximum likelihood techniques for the mapping and analysis of quantitative trait loci with the aid of genetic markers. Biometrics. 1986 Sep;42(3):627–640. [PubMed] [Google Scholar]
  46. Wolf C. R., Smith C. A., Forman D. Metabolic polymorphisms in carcinogen metabolising enzymes and cancer susceptibility. Br Med Bull. 1994 Jul;50(3):718–731. doi: 10.1093/oxfordjournals.bmb.a072920. [DOI] [PubMed] [Google Scholar]
  47. Zeng Z. B. Precision mapping of quantitative trait loci. Genetics. 1994 Apr;136(4):1457–1468. doi: 10.1093/genetics/136.4.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Zeng Z. B. Precision mapping of quantitative trait loci. Genetics. 1994 Apr;136(4):1457–1468. doi: 10.1093/genetics/136.4.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Zeng Z. B. Theoretical basis for separation of multiple linked gene effects in mapping quantitative trait loci. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):10972–10976. doi: 10.1073/pnas.90.23.10972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zeng Z. B. Theoretical basis for separation of multiple linked gene effects in mapping quantitative trait loci. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):10972–10976. doi: 10.1073/pnas.90.23.10972. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES