Advertisement

Genetica

, Volume 86, Issue 1–3, pp 269–274 | Cite as

Evolutionary dynamics of transposable elements in prokaryotes and eukaryotes

  • D. A. Hickey
Article

Abstract

This paper summarizes some recent theories about the evolution of transposable genetic elements in outbreeding, sexual eukaryotic organisms. The evolutionary possibilities available to self-replicating transposable elements are shown to vary depending on the reproductive biology of the host genome. This effect can be used to explain, in part, the differences in abundance of transposable elements between prokaryotes and eukaryotes. It is argued that the pattern of sexual outbreeding seen in mammals and plants is especially favorable to the spread of transposons. Moreover, because transposon spread is facilitated by zygote formation, the evolutionary origin of sexual conjugation may have been due to selection on transposon-encoded genes. Finally, evidence is also presented that introns could have originated as transposable genetic elements.

Key words

Evolution Introns Selfish DNA Sex transposons 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Belfort, M., 1991. Self-splicing introns in prokaryotes: migrant fossils? Cell 64: 9–11.Google Scholar
  2. Bell-Pedersen, D., S. Quirk, J. Clyman & M. Belfort, 1990. Intron mobility in phage T4 is dependent upon a distinctive class of endonucleases and independent of DNA sequences encoding the intron core: mechanistic and evolutionary implications. Nucleic Acids Res. 18: 3763–3770.Google Scholar
  3. Biel, S. W. & D. L. Hartl, 1983. Evolution of transposons: natural selection for Tn5 in Escherichia coli K12. Genetics 103: 581–592.Google Scholar
  4. Cavalier-Smith, T., 1978. Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA c-value paradox. J. Cell Sci. 34: 247–278.Google Scholar
  5. Cavalier-Smith, T., 1980. How selfish is DNA? Nature 285: 617–618.Google Scholar
  6. Cavalier-Smith, T., 1985. Nature 315: 283–284.Google Scholar
  7. Cavalier-Smith, T., 1991. Intron phylogeny: a new hypothesis. Trends in Genet. 7: 145–148.Google Scholar
  8. Cech, T., 1986. The generality of self-splicing RNA: Relationship to nuclear mRNA splicing. Cell 44: 207–210.Google Scholar
  9. Chao, L. & S. McBroom, 1985. Evolution of transposable elements: an IS10 insertion increases fitness in Escherichia coli. Mol. Biol. Evol. 2: 359–369.Google Scholar
  10. Charlesworth, B., 1987. The population biology of transposable elements. Trends Ecol. Evol. 2: 21–23.Google Scholar
  11. Charlesworth, B. & D. Charlesworth, 1983. The population dynamics of transposable elements. Genet. Res. 42: 1–27.Google Scholar
  12. Charlesworth, B. & C. H. Langley, 1986. The evolution of self-regulated transposition of transposable elements. Genetics 112: 359–383.Google Scholar
  13. Condit, R., F. M. Stewart & B. R. Levin, 1988. The population biology of bacterial transposons: a priori conditions for maintenance as parasitic DNA. Amer. Nat. 132: 129–147.Google Scholar
  14. Doolittle, W. F., 1978. Genes in pieces: were they ever together? Nature 272: 581–582.Google Scholar
  15. Doolittle, W. F. & C. Sapienza, 1980. Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601–603.Google Scholar
  16. Dover, G., 1980. Ingnorant DNA? Nature 285: 618–620.Google Scholar
  17. Engels, W. R., 1989. P elements in Drosophila, pp. 437–484 in Mobile DNA, edited by D. E. Berg and M. Howe. A.S.M. Publications, Washington D.C.Google Scholar
  18. Gawron-Burke, C. & D. B. Clewell, 1982. A transposon in Streptomyces faecalis with fertility properties. Nature 300: 1–3.Google Scholar
  19. Gilbert, W., 1979. Introns and exons: playgrounds of evolution. ICN-UCLA Symp. Mol. Cell. Biol. 14: 1–12.Google Scholar
  20. Good, A. G., G. Meister, H. Brock, T. A. Grigliatti & D. Hickey, 1989. Rapid spread of transposable P elements in experimental populations of Drosophila melanogaster. Genetics 122: 387–396.Google Scholar
  21. Hartl, D. L., D. E. Dykhuizen, R. D. Miller, L. Green & J.de Framond, 1983. Transposable element IS50 improves growth rate of E. coli cells without transposition. Cell 35: 503–510.Google Scholar
  22. Hickey, D. A., 1982. Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101: 519–531.Google Scholar
  23. Hickey, D. A. & B. F. Benkel, 1985. Splicing and the evolution of introns. Nature 316: 582.Google Scholar
  24. Hickey, D. A. & B. F. Benkel, 1986. Introns as relict retrotransposons: implications for the evolutionary origin of eukaryotic mRNA splicing mechanisms. J. Theoret. Biol. 121: 283–291.Google Scholar
  25. Hickey, D.A., A. Loverre & G. C. Carmody, 1986. Is the segregation distortion phenomenon in Drosophila due to active recurrent genetic transposition? Genetics 114: 665–668.Google Scholar
  26. Hickey, D. A., B. F. Benkel & S. M. Abukashawa, 1989. A general model for the evolution of nuclear pre-mRNA introns. J. Theoret. Biol. 137: 41–53.Google Scholar
  27. Hickey, D. A. & M. R. Rose, 1988. The role of gene transfer in the evolution of eukaryotic sex, pp. 161–175 in The Evolution of Sex, edited by R. E. Michod and B. R. Levin. Sinauer, Sunderland, Mass.Google Scholar
  28. Hurst, L. D., 1991. Sex, slime and selfish genes. Nature 354: 23–24.Google Scholar
  29. Kidwell, M., 1983. Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proc. Natl. Acad. Sci. (USA) 80: 1655–1659.Google Scholar
  30. Kiyasu, P. K. & M. G. Kidwell, 1984. Hybrid dysgenesis in Drosophila melanogaster: the evolution of mixed P and M populations maintained at high temperature. Genet. Res. 44: 251–259.Google Scholar
  31. Kleckner, N., 1981. Transposable elements in prokaryotes. Ann. Rev. Genet. 15: 341–404.Google Scholar
  32. Lambowitz, A. M., 1989. Infectious introns. Cell 56: 323–326.Google Scholar
  33. Langley, C. H., J. F. Y. Brookfield & N. Kaplan, 1983. Transposable elements in Mendelian populations. I. A. theory Genetics 104: 457–471.Google Scholar
  34. McClintock, B., 1951. Chromosome organization and genic expression. Cold Spr. Harb. Symp. Quant. Biol. 16: 13–47.Google Scholar
  35. McClure, M. A., 1991. Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol. Biol. Evol. 8: 835–856.Google Scholar
  36. Montgomery, E. A. & C. H. Langley, 1983. Transposable elements in Mendelian populations. II. Distribution of three copia-like elements in a natural population of Drosophila melanogaster. Genetics 104: 473–483.Google Scholar
  37. Nanjndiah, V., 1985. Transposable element copy number and stable polymorphisms. J. Genet. 64: 127–134.Google Scholar
  38. Orgel, L. E. & F. H. C. Crick, 1986. Selfish DNA: the ultimate parasite. Nature 284: 604–607.Google Scholar
  39. Rose, M. R., 1983. The contagion mechanism for the origin of sex. J. Theoret. Biol. 101: 137–146.Google Scholar
  40. Temin, H. M., 1985. Reverse transcription in the eukaryotic genome: retroviruses, pararetroviruses, retrotransposons, and retrotranscripts. Mol. Biol. Evol. 2: 455–468.Google Scholar
  41. Willets, N. & R. Skurray, 1980. The conjugation system of F-like plasmids. Ann. Rev. Genet. 14: 41–76.Google Scholar
  42. Woodson, S. A. & T. R. Cech, 1989. Reverse self-splicing of the Tetrahymena group I intron: implication for the directionality of splicing and for intron transposition. Cell 57: 335–345.Google Scholar
  43. Xiong, Y. & T. H. Eickbush, 1988. Similarity of reverse-transcriptase-like sequences of viruses, transposable elements and mitochondrial introns. Mol. Biol. Evol. 5: 675–690.Google Scholar

Copyright information

© Kluwer Academic Publishers 1992

Authors and Affiliations

  • D. A. Hickey
    • 1
  1. 1.Department of BiologyUniversity of OttawaOttawaCanada

Personalised recommendations