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Evolution of Simple Sequence Repeats as Mutable Sites

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Tandem Repeat Polymorphisms

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB))

Abstract

Because natural selection is commonly presumed to minimize mutation rates, the discovery of mutationally unstable simple sequence repeats (SSRs) in many functional genomic locations came as a surprise to many biologists. Whether such SSRs persist in spite of or because of their intrinsic mutability — whether they constitute a genetic burden or an evolutionary boon — remains uncertain. Two contrasting evolutionary explanations can be offered for SSR abundance. First, suppressing the inherent mutability of repetitive sequences might simply lie beyond the reach of natural selection. Alternatively, natural selection might indirectly favor SSRs at sites where particular repeat-number variants have provided positive contributions to fitness. Indirect selection could thereby shape SSRs into “tuning knobs” that facilitate evolutionary adaptation by implementing an implicit protocol of incremental adjustability. The latter possibility is consistent with deep evolutionary conservation of some SSRs, including several in genes with neurological and neurodevelopmental function.

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References

  1. Morell V. The puzzle of the triplet repeats. Science 1993; 260:1422–1423.

    Article  CAS  Google Scholar 

  2. Hamada H, Scidman M, Howard BH et al. Enhanced gene expression by the poly(dT-dG) poly(dC-dA) sequence. Mol Cellular Biol 1984; 4:2622–2630.

    Article  CAS  Google Scholar 

  3. Gerber HP, Scipel K, Georgiev O et al. Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science 1994; 263:808–811.

    Article  CAS  Google Scholar 

  4. Kashi Y, King DG, Soller M. Simple sequence repeats as a source of quantitative genetic variation. Trends Genet 1997; 13:74–78.

    Article  CAS  Google Scholar 

  5. Li YC, Korol AB, Fahima T et al. Microsatellites within genes: Structure, function and evolution. Mol BiolEvol 2004; 21:991–1007.

    Article  CAS  Google Scholar 

  6. Buschiazzo E, Gemmel NJ. Conservation of Human Microsatellites across 450 Million Years of Evolution. Genome Biol Evol 2010; 2:153–165.

    Article  Google Scholar 

  7. Sung W, Tucker A, Bergeron DR et al. Simple sequence repeat variation in the Daphnia pulex genome. BMC Genomics 2010; 11:691. doi:10.1186/1471-2164-11-691.

    Article  CAS  Google Scholar 

  8. Darwin CR. On the Origin of Species by Means of Natural Selection. London: John Murray, 1859:131 (Facsimile edition by Harvard University Press, Cambridge, Massachusetts, 1964).

    Google Scholar 

  9. de Vries H. The origin of species by mutation. Science 1902; 15:721–729.

    Article  Google Scholar 

  10. Bridges CB. Specific modifiers of eosin eye color in Drosophilamelanogaster. J Exp Zool 1919; 28:337–384.

    Article  Google Scholar 

  11. Sturtevant AH. Essays on evolution. I. On the effects of selection on mutation rate. Q Rev Biol 1937; 12:464–467.

    Article  Google Scholar 

  12. Williams GC. Adaptation and Natural Selection. Princeton: Princeton University Press, 1966:139–141.

    Google Scholar 

  13. Sniegowski PD, Gerrish PJ, Johnson T et al. The evolution of mutation rates: separating causes from consequences. BioEssays 2000; 22:1057–1066.

    Article  CAS  Google Scholar 

  14. Baer CF, Miyamoto MM, Denver DR. Mutation rate variation in multicellular eukaryotes: causes and consequences. Nature Rev Genet 2007; 8:619–631.

    Article  CAS  Google Scholar 

  15. Sniegowski PD, Murphy HA. Evolvability. Current Biology 2006; 16:R831–R834.

    Article  CAS  Google Scholar 

  16. Ayala FJ. One hundred fifty years without Darwin are enough! Genome Res 2009; 19:693–699.

    Article  CAS  Google Scholar 

  17. Darlington CD. A diagram of evolution. Nature 1978; 276:447–452.

    Article  CAS  Google Scholar 

  18. Lennox JG. Teleology. In: Keller EF, Lloyd EA, eds. Keywords in Evolutionary Biology. Cambridge, Massachusetts: Harvard University Press, 1992:324–333.

    Google Scholar 

  19. Gould SJ. Darwinism and the expansion of evolutionary theory. Science 1982; 216:380–387.

    Article  CAS  Google Scholar 

  20. Maynard Smith J. Evolutionary Genetics. Oxford: Oxford University Press, 1989:55.

    Google Scholar 

  21. Shaw RG, Shaw FH, Geyer C. What fraction of mutations reduces fitness? Evolution 2003; 57:686–689.

    Google Scholar 

  22. Hadany L, Comeron JM. Why are sex and recombination so common? Ann NY Acad Sci 2008; 1133: 26–43.

    Article  Google Scholar 

  23. Futuyma DJ. Evolutionary Biology, 3rd ed. Sunderland, Massachusetts: Sinauer Associates, 1998: 769.

    Google Scholar 

  24. Barry JD. Implicit information in eukaryotic pathogens as the basis of antigenic variation. In: Caporale LH, ed. The Implicit Genome. Oxford: Oxford University Press, 2006:91–106.

    Google Scholar 

  25. Bayliss CD, Moxon ER. Repeats and variation in pathogen selection. In: Caporale LH, ed. The Implicit Genome. Oxford: Oxford University Press, 2006:54–76.

    Google Scholar 

  26. Arber W. Gene products with evolutionary functions. Proteomics 2005; 5:2280–2284.

    Article  CAS  Google Scholar 

  27. King DG, Kashi Y. Mutation rate variation in eukaryotes: evolutionary implications of site-specific mechanisms. Nature Rev Genet 2007; 8. doi:10.1038/nrg2158-c1.

    Article  Google Scholar 

  28. Ellegren H. Microsatellites: Simple sequences with complex evolution. Nat Rev Genet 2004; 5:435–445.

    Article  CAS  Google Scholar 

  29. Parker SCJ, Hansen L, Abaan HO et al. Local DNA topography correlates with functional noncoding regions of the human genome. Science 2009; 324:389–392.

    Article  CAS  Google Scholar 

  30. Trifonov EN. The multiple codes of nucleotide sequences. Bull Math Biol 1989; 51:417–432.

    Article  CAS  Google Scholar 

  31. King DG, Soller M, Kashi Y. Evolutionary tuning knobs. Endeavour 1997; 21:36–40.

    Article  Google Scholar 

  32. Doyle J, Csete M, Caporale L. An engineering perspective: The implicit protocols. In: Caporale LH, ed. The Implicit Genome. Oxford: Oxford University Press, 2006:294–298.

    Google Scholar 

  33. Fisher RA. The Genetical Theory of Natural Selection. Oxford: Oxford University Press, 1930.

    Book  Google Scholar 

  34. Levins R. Theory of fitness in a heterogeneous environment. VI. The adaptive significance of mutation. Genetics 1967; 56:163–178.

    CAS  PubMed  Google Scholar 

  35. Levins R. Evolution in Changing Environments: Some Theoretical Explorations. Princeton: Princeton University Press, 1968.

    Google Scholar 

  36. Orr HA. The population genetics of adaptation: The distribution of factors fixed during adaptive evolution. Evolution 1998; 52:935–949.

    Article  Google Scholar 

  37. Kashi Y, King DG. Simple sequence repeats as advantageous mutators in evolution. Trends Genet 2006; 22:253–259.

    Article  CAS  Google Scholar 

  38. Sawyer LA, Sandrelli F, Pasetto C et al. The period gene Thr-Gly polymorphism in Australian and African Drosophila melanogaster populations: Implications for selection. Genetics 2006; 174:465–480.

    Article  CAS  Google Scholar 

  39. Lindqvist C, Laakkonen L, Albert VA. Polyglutamine variation in a flowering time protein correlates with island age in a Hawaiian plant radiation. BMC Evol Biol 2007; 7:105. doi: 10.1186/1471-2148-7-105.

    Article  Google Scholar 

  40. Johnsen A, Fidler AE, Kuhn S et al. Avian Clock gene polymorphism: evidence for a latitudinal cline in allele frequencies. Mol Ecol 2007; 16:4867–4880.

    Article  CAS  Google Scholar 

  41. Vinces MD, Legendre M, Caldara M et al. Unstable tandem repeats in promoters confer transcriptional evolvability. Science 2009; 324:1213–1216.

    Article  CAS  Google Scholar 

  42. King DG, Soller M. Variation and fidelity: The evolution of simple sequence repeats as functional elements in adjustable genes. In: Wasser SP, ed. Evolutionary Theory and Processes: Modern Perspectives. Dordrecht: Kluwer Academic Publishers, 1999: 65–82.

    Chapter  Google Scholar 

  43. King DG, Trifonov EN, Kashi Y. Tuning knobs in the genome: Evolution of simple sequence repeats by indirect selection. In: Caporale LH, ed. The Implicit Genome. Oxford: Oxford University Press, 2006:77–90.

    Google Scholar 

  44. Kashi Y, King DG. Has simple sequence repeat mutability been selected to facilitate evolution? Isr J Ecol Evol 2006; 52:331–342.

    Article  Google Scholar 

  45. King DG, Kashi Y. Indirect selection for mutability. Heredity 2007; 99:123–124.

    Article  CAS  Google Scholar 

  46. Buschiazzo E, Gemmel NJ. The rise, fall and renaissance of microsatellites in eukaryotic genomes. BioEssays 2006; 28:1040–1050.

    Article  CAS  Google Scholar 

  47. Zhu Y, Strassmann JE, Queller DC. Insertions, substitutions, and the origin of microsatellites. Genet Res Camb 2000; 76:227–236.

    Article  CAS  Google Scholar 

  48. Jurka J, Kapitonov VV, Kohany O et al. Repetitive sequences in complex genomes: Structure and evolution. Annu Rev Genomics Hum Genet 2007; 8:241–259.

    Article  CAS  Google Scholar 

  49. Oliver KR, Green WK. Transposable elements: powerful facilitators of evolution. BioEssays 2009; 31:703–714.

    Article  CAS  Google Scholar 

  50. Kelkar YD, Strubczewski N, Hile SE et al. What is a microsatellite: A computational and experimental definition based upon repeat mutational behavior at A/T and GT/AC repeats. Genome Biol Evol 2010; 2:620–635.

    Article  Google Scholar 

  51. Barbará T, Palma-Silva C, Paggi GM et al. Cross-species transfer of nuclear microsatellite markers: potential and limitations. Molec Ecol 2007; 16:3759–3767.

    Article  Google Scholar 

  52. Riley DE, Krieger JN. Embryonic nervous system genes predominate in searches for dinucleotide simple sequence repeats flanked by conserved sequences. Gene 2009; 429:74–79.

    Article  CAS  Google Scholar 

  53. Riley DE, Krieger JN. UTR dinucleotide simple sequence repeat evolution exhibits recurring patterns including regulatory sequence motif replacements. Gene 2009; 429:80–86.

    Article  CAS  Google Scholar 

  54. Fondon JW, Hammock EAD, Hannan A et al. Simple sequence repeats: Genetic modulators of brain function and behavior. Trends Neurosci 2008; 31:328–334.

    Article  CAS  Google Scholar 

  55. Karlin S, Burge C. Trinucleotide repeats and long homopeptides in genes and proteins associated with nervous system disease and development. Proc Natl Acad Sci USA 1996; 93:1560–1565.

    Article  CAS  Google Scholar 

  56. Huntley MA, Mahmood S, Golding BG. Simple sequence in brain and nervous system specific proteins. Genome 2005; 48:291–301.

    Article  CAS  Google Scholar 

  57. Labaj PP, Leparc GG, Bardet AF et al. Single amino acid repeats in signal peptides. FEBS Journal 2010; 277:3147–3157.

    Article  CAS  Google Scholar 

  58. Huntley MA, Clark AG. Evolutionary analysis of amino acid repeats across the genomes of 12 Drosophila species. Mol Biol Evol 2007; 24:2598–2609.

    Article  CAS  Google Scholar 

  59. Birge LM, Pitts ML, Baker RH et al. Length polymorphism and head shape association among genes with polyglutamine repeats in the stalk-eyed fly, Teleopsis dalmanni. BMC Evol Biol 2010; 10:227. doi:10.1186/1471-2148-10-227.

    Article  Google Scholar 

  60. Tompa P. Intrinsically unstructured proteins evolve by repeat expansion. BioEssays 2003; 25:847–855.

    Article  CAS  Google Scholar 

  61. Tyedmers J, Madariaga ML, Lindquist S. Prion switching in response to environmental stress. PLoS Biol 2008; 6(11): e294. doi:10.1371/journal.pbio.0060294.

    Article  Google Scholar 

  62. Williams GC. Adaptation and Natural Selection. Princeton: Princeton University Press, 1966:270.

    Google Scholar 

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King, D.G. (2012). Evolution of Simple Sequence Repeats as Mutable Sites. In: Hannan, A.J. (eds) Tandem Repeat Polymorphisms. Advances in Experimental Medicine and Biology. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5434-2_2

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