Journal of Molecular Evolution

, Volume 56, Issue 6, pp 770–777 | Cite as

A Case for the Extreme Antiquity of Recombination

  • Niles LehmanEmail author


Recombination is usually assumed to be a mode of reproduction that evolved long after asexual reproduction in response to specific genetic and environmental circumstances. Here the argument is made that recombination was an evolutionary development as ancient as the origins of life. To support this proposition four lines of evidence are given, in particular, the need for primordial genomes to acquire substantial length and to escape from Muller’s Ratchet.


Recombination Origins of life Origins of sex Muller’s Ratchet 



I thank A. Krummel, M. Zwick, and two anonymous reviewers for insightful comments on the manuscript, and NASA for funding (NAG5-11441).


  1. 1.
    Aravind, L, Leipe, DD, Koonin, EV 1998Toprim—A conserved catalytic domain in type IA and type II topoisomerases, DnaG-type primases, OLD family nucleases and RecR proteins.Nucleic Acids Res2642054213PubMedGoogle Scholar
  2. 2.
    Asai, T, Bates, DB, Kogoma, T 1994DNA replication triggered by double-stranded breaks in E. coli: Dependence on homologous recombination functions.Cell7810511061PubMedGoogle Scholar
  3. 3.
    Bernstein, H, Byerly, HC, Hopf, FA, Michod, RE 1985Genetic damage, mutation, and the evolution of sex.Science22912771281PubMedGoogle Scholar
  4. 4.
    Biebricher, CK, Luce, R 1992 In vitro recombination and terminal elongation of RNA by Qβ replicase.EMBO J1151295135PubMedGoogle Scholar
  5. 5.
    Börner, GV, Yokobori, S-I, Mörl, M, Dörner, D, Pääbo, S 1997RNA editing in metazoan mitochondria: Staying fit without sex.FEBS Lett409320324PubMedGoogle Scholar
  6. 6.
    Breaker, RR, Joyce, GF 1994Inventing and improving ribozyme function: Rational design versus iterative selection methods.Trends Biotechnol12268275PubMedGoogle Scholar
  7. 7.
    Cavalier-Smith, T 2001Obcells as proto-organisms membrane heredity, lithophosphorylation, and the origins of the genetic code, the first cells, and photosynthesis.J Mol Evol53555595PubMedGoogle Scholar
  8. 8.
    Cavalier-Smith, T 2002Origins of the machinery of recombination and sex.Heredity88125141PubMedGoogle Scholar
  9. 9.
    Cech, TR 1985Self-splicing RNA: Implications for evolution.Int Rev Cytol93322PubMedGoogle Scholar
  10. 10.
    Cech, TR 1990Self-splicing of group I introns.Annu Rev Biochem59543568PubMedGoogle Scholar
  11. 11.
    Cox, MM 2001Historical overview: Searching for replication help in all the rec places.Proc Natl Acad Sci USA9881738180CrossRefPubMedGoogle Scholar
  12. 12.
    Eigen, M 1971Self-organization of matter and the evolution of biological macromolecules.Naturwissenschaften58465523PubMedGoogle Scholar
  13. 13.
    Ekland, EH, Bartel, DP 1996RNA-catalysed RNA polymerization using nucleoside triphosphates.Nature382373376PubMedGoogle Scholar
  14. 14.
    Ferris, JP, Hill Jr, AR, Liu, R, Orgel, LE 1996Synthesis of long prebiotic oligomers on mineral surfaces.Nature3815961PubMedGoogle Scholar
  15. 15.
    Fisher, RA 1930The genetical theory of natural selection.Oxford University PressOxfordGoogle Scholar
  16. 16.
    Gilbert, W 1986The RNA world.Nature319618Google Scholar
  17. 17.
    Jacobson, H 1955Information, reproduction, and the origin of life.Am Sci43119127Google Scholar
  18. 18.
    Johnston, WK, Unrau, PJ, Lawrence, MS, Glasner, ME, Bartel, DP 2001RNA-catalyzed RNA polymerization: Accurate and general RNA-templated primer extension.Science29213191325PubMedGoogle Scholar
  19. 19.
    Joyce, GF, Orgel, LE 1999Origin of the RNA world.Gesteland, RFCech, TRAtkins, JF eds. The RNA world, 2nd ed.Cold Spring Harbor PressCold Spring Harbor, NY4977Google Scholar
  20. 20.
    Kauffman, SA 2000Investigations.Oxford University PressOxfordGoogle Scholar
  21. 21.
    Kowalczykowski, SC 2000Initiation of genetic recombination and recombination-dependent replication.Trends Biochem Sci25156165CrossRefPubMedGoogle Scholar
  22. 22.
    Kowalczykowski, SC, Krupp, RA 1995DNA-strand exchange promoted by RecA protein in the absence of ATP: Implications for the mechanism of energy transduction in protein-promoted nucleic acid transactions.Proc Natl Acad Sci USA9234783482PubMedGoogle Scholar
  23. 23.
    Kowalczykowski, SC, Dixon, DA, Eggleston, AK, Lauder, SD, Rehrauer, WM 1994Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev58401465PubMedGoogle Scholar
  24. 24.
    Lai, MM 1992RNA recombination in animal and plant viruses.Microbiol Rev566179PubMedGoogle Scholar
  25. 25.
    Levin, BR 1988The evolution of sex in bacteria.Michod, RELevin, BR eds. The evolution of sex: An examination of current ideas.SinauerSunderland MA194211Google Scholar
  26. 26.
    Luo, Y, Wasserfallen, A 2001Gene transfer systems and their applications in Archaea.Syst Appl Microbiol241525PubMedGoogle Scholar
  27. 27.
    Lynch, M, Gabriel, W 1990Mutation load and the survival of small populations.Evolution4417251737Google Scholar
  28. 28.
    Lynch, M, Burger, R, Butcher, D, Gabriel, W 1993The mutational meltdown in asexual populations.J Hered84339344Google Scholar
  29. 29.
    Marintcheva, B, Weller, SK 2001A tale of two HSV-1 helicases: Roles of phage and animal virus helicases in DNA replication and recombination.Prog Nucleic Acid Res Mol Biol7077118PubMedGoogle Scholar
  30. 30.
    Maynard Smith, J 1978The evolution of sex.Cambridge University PressCambridgeGoogle Scholar
  31. 31.
    Maynard Smith, J, Szathmáry, E 1995The major transitions in evolution.WH FreemanNew YorkGoogle Scholar
  32. 32.
    Michel, F, Westhof, E 1990Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis.J Mol Biol216585610PubMedGoogle Scholar
  33. 33.
    Michod, RE, Wojciechowski, M, Hoelzer, M 1988DNA repair and the evolution of transformation in the bacterium Bacillus subtilis. Genetics1183139PubMedGoogle Scholar
  34. 34.
    Muller, HJ 1964The relation of recombination to mutational advance.Mutat Res129CrossRefGoogle Scholar
  35. 35.
    Negroni, M, Buc, H 2001Mechanisms of retroviral recombination.Annu Rev Genet35275302PubMedGoogle Scholar
  36. 36.
    Nowak, M, Schuster, P 1989Error thresholds of replication in finite populations mutation frequencies and the onset of Muller’s Ratchet.J Theor Biol137375395PubMedGoogle Scholar
  37. 37.
    Ogawa, T, Yu, X, Shinohara, A, Egelman, EH 1993Similarity of the yeast RAD51 filament to the bacterial RecA filament.Science25918961899PubMedGoogle Scholar
  38. 38.
    Orgel, LE 1992Molecular replication.Nature358203209PubMedGoogle Scholar
  39. 39.
    Orgel, LE 1998The origin of life—A review of facts and speculations.Trends Biochem Sci23491495CrossRefPubMedGoogle Scholar
  40. 40.
    Redfield, RJ 1993aEvolution of natural transformation: Testing the DNA repair hypothesis in Bacillus subtilis and Haemophilus influenzae. Genetics133755761Google Scholar
  41. 41.
    Redfield, RJ 1993bGenes for breakfast: The have-your-cake-and-eat-it-too of transformation.J Hered84400404Google Scholar
  42. 42.
    Rice, WR, Chippendale, AK 2001Sexual recombination and the power of natural selection.Science294555559PubMedGoogle Scholar
  43. 43.
    Scott, A 1986The creation of life: Past, future, alien.Basil BlackwellOxfordGoogle Scholar
  44. 44.
    Simon, HA 1996The sciences of the artificial, 3rd ed.MIT PressCambridge, MAGoogle Scholar
  45. 45.
    Woese, C 1998The universal ancestor.Proc Natl Acad Sci USA9568546859PubMedGoogle Scholar
  46. 46.
    Wu, T, Orgel, LE 1992Nonenzymatic template-directed synthesis on oligodeoxycytidylate sequences in hairpin oligonucleotides.J Am Chem Soc114317322PubMedGoogle Scholar
  47. 47.
    Zaug, AJ, Cech, TR 1986The intervening sequence RNA of Tetrahymena is an enzyme.Science231470475PubMedGoogle Scholar
  48. 48.
    Zintzaras, E, Santos, M, Szathmáry, E 2002“Living” under the challenge of informational decay: The stochastic corrector model vs. hypercycles.J Theor Biol217167181PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 2003

Authors and Affiliations

  1. 1.Department of ChemistryPortland State University, P.O. Box 751, Portland, OR 97207USA

Personalised recommendations