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Unclocklike behaviour of biological clocks

Abstract

The mechanisms which could underlie circadian rhythms fall naturally into groups with qualitatively different responses to disruption. Experiments designed to distinguish between these mechanisms seem to exclude all of them. It may be that multicellular organisms keep time, not by one ‘clock’ but by averaging many independent circadian oscillators.

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References

  1. Thurber, J., The Thirteen Clocks, (Simon and Schuster, New York, 1950).

    Google Scholar 

  2. Cold Spring Harb, Symp. quant. Biol., (edit. by Chovnick, A.), 25, (1960).

  3. Circadian Clocks (edit. by Aschoff, J.), (North-Holland, Amsterdam, 1965).

  4. Biochronometry (edit. by Menaker, M.), (National Academy of Sciences, Washington, DC, 1971).

  5. Sweeney, B., Rhythmic Phenomena in Plants, (Academic Press, New York, 1969).

    Google Scholar 

  6. Bunning, E., The Physiological Clock, 3rd ed. (Springer, New York, 1973).

    Google Scholar 

  7. Feynman, R., Lectures on Physics, 2, 9-3 (Addison-Wesley, Reading, Mass., 1964).

    MATH  Google Scholar 

  8. Hamner, K. C., Finn, J. C., Sirohi, G. S., Hoshizaki, T., and Carpenter, B. H., Nature, 195, 476 (1962).

    Article  ADS  Google Scholar 

  9. Kalmus, H., Biol. Generalis., 9, 93 (1935).

    Google Scholar 

  10. Njus, D., Sulzman, F. M., and Hastings, J. W., Nature, 248, 116 (1974).

    Article  ADS  CAS  Google Scholar 

  11. Spangler, R. A., and Snell, F. M., Nature, 191, 457 (1961).

    Article  ADS  CAS  Google Scholar 

  12. Pye, K., and Chance, B., Proc. natn. Acad. Sci. U.S.A., 55, 888 (1966).

    Article  ADS  CAS  Google Scholar 

  13. Pavlidis, T., and Kauzmann, W., Archs Biochem. Biophys., 132, 338 (1969).

    Article  CAS  Google Scholar 

  14. Ehret, C. F., in Advances in Biological and Medical Physics, 15, 47 (Academic Press, New York, 1974).

    Google Scholar 

  15. Goodwin, B., Temporal Organization in Cells: A Dynamic Theory of Cellular Control Processes, (Academic Press, New York, 1963).

    Google Scholar 

  16. Van Den Driessche, T., Biochem. biophys. Acta, 126, 456 (1966).

    CAS  Google Scholar 

  17. May, R., Stability and Complexity in Model Ecosystems, (Princeton University Press, Princeton, New Jersey, 1973).

    Google Scholar 

  18. Lorenz, E. N., J. atmos. Sci, 20, (1963).

  19. Hoffman, K., in Proc, int. Symp. Circadian Rhythmicity, (edit. by Bierhuizen, J. F.)(Centre for Agricultural Publishing and Documentation, Wageningen, 1972).

    Google Scholar 

  20. Enright, J. T., A. Rev. Ecol. Syst., 1, 221 (1970).

    Article  Google Scholar 

  21. Sage, A. P. Jr, Justice, K. E., and Melsa, J. S., Tech. Doc. Rept. ASD-TDR-63-136, 1 (1963).

  22. Winfree, A. T., in Temporal Aspects of Therapeutics (edit. by Urquardt, J., and Yates, F. E.) (Plenum, New York, 1973).

    Google Scholar 

  23. Johnson, M., J. expt. Zool., 82, 315 (1939).

    Article  Google Scholar 

  24. Brown, F. A., Sci. Am., 190, (4), 34 (1954).

    Article  Google Scholar 

  25. Pittendrigh, C. S., Proc. natn. Acad. Sci. U.S.A., 40, 1018 (1954).

    Article  ADS  CAS  Google Scholar 

  26. Winfree, A. T., Science, 183, 970 (1974).

    Article  ADS  CAS  Google Scholar 

  27. Winfree, A. T., J. theor. Biol., 35, 159 (1972).

    Article  CAS  Google Scholar 

  28. Zimmerman, W. F., and Ives, D., in Biochronometry (edit. by Menaker, M.), 381 (National Academy of Sciences, Washington, DC, 1971).

    Google Scholar 

  29. Engelmann, W., and Honegger, H. W., Naturwiss, 22, 1 (1966).

    Google Scholar 

  30. Hayes, D. K., Sullivan, W. N., Oliver, M. Z., and Schecter, M. S., Science, 169, 382 (1970).

    Article  ADS  CAS  Google Scholar 

  31. Barker, R. J., Cohen, C. F., and Mayer, A., Science, 145, 1195 (1964).

    Article  ADS  CAS  Google Scholar 

  32. Saunders, D. S., Science, 181, 358 (1973).

    Article  ADS  CAS  Google Scholar 

  33. Saunders, D. S., J. Ins. Physiol., 19, 1941 (1973).

    Article  CAS  Google Scholar 

  34. Mitchison, J. M., The Biology of the Cell Cycle (Cambridge University Press, London, 1971).

    Google Scholar 

  35. Perkel, D. H., Schulman, J. H., Bullock, T. H., Moore, G. P., and Segundo, J. P., Science, 145, 61 (1964).

    Article  ADS  CAS  Google Scholar 

  36. Hanson, F. E., Case, J. F., Buck, E., and Buck, J., Science, 174, 161 (1971).

    Article  ADS  CAS  Google Scholar 

  37. Walker, T. J., Science, 166, 891 (1969).

    Article  ADS  CAS  Google Scholar 

  38. Campbell, A., in Synchrony in Cell Division and Growth (edit. by Zeuthen, E.) (Interscience, New York 1964).

    Google Scholar 

  39. Winfree, A. T., in Biochronometry (edit. by Menaker, M.,) (National Academy of Sciences, Washington, DC, 1971).

    Google Scholar 

  40. Halvorson, H. O., Gorman, J. P., Tauro, P., Epstein, R., and Laberge, M., Fed. Proc., 23, 1002 (1964).

    CAS  PubMed  Google Scholar 

  41. Pittendrigh, C. S., Zeit. fur Pflanzenphysiol., 54, 275 (1966).

    Google Scholar 

  42. Aschoff, J., Klotter, K., and Wever, R., in Circadian Clocks (edit. by Aschoff, J.) (North-Holland, 1965).

    Google Scholar 

  43. Pittendrigh, C. S., in Cold Spring Harb. Symp.quant. Biol., (edit. by Chovnick, A.), 25, 159 (1960).

    Article  CAS  Google Scholar 

  44. Winfree, A. T., J. theor. Biol., 16, 15 (1967).

    Article  CAS  Google Scholar 

  45. Swade, R. H., J. theor. Biol., 24, 227 (1969).

    Article  CAS  Google Scholar 

  46. Kalmus, H., and Wigglesworth, Cold Spring Harb. Symp. quant. Biol. (edit. by Chovnick, A.), 25, 211 (1960).

    Article  CAS  Google Scholar 

  47. Mori, S., Mem. Coll. Sci. Univ. Kyoto., B., 19, 1 (1947).

    Google Scholar 

  48. Bonhoeffer, K. F., Z. Elektrochem., 52, 24 (1948).

    CAS  Google Scholar 

  49. Bonhoeffer, K. F., Naturwiss, 40, 301 (1953).

    Article  ADS  CAS  Google Scholar 

  50. Winfree, A. T., J. mathe. Biol., 1, 73 (1974).

    Article  Google Scholar 

  51. Guckenheimer, J., J. mathe. Biol. (in the press).

  52. Pavlidis, T., Biological Oscillators: Their Mathematical Analysis (Academic Press, New York, 1973).

    Google Scholar 

  53. Johnsson, A., and Karlsson, H. G., Proc. First Eur. Biophys. Cong. (edit. by Broada, E., and Locker, A.) (Springer, Berlin, 1971).

    Google Scholar 

  54. van der Pol, B., Acta med. Scand. Suppl., 108, 76 (1940).

    Google Scholar 

  55. Barlow, J. S., Ann. N. Y. Acad. Sci., 98, 788 (1962).

    Article  ADS  CAS  Google Scholar 

  56. Karlsson, H. G., and Johnsson, A., J. theor. Biol., 36, 175 (1972).

    Article  CAS  Google Scholar 

  57. Engelmann, W., Karlsson, H. G., and Johnsson, A., Int. J. Chronobiol., 1, 147 (1973).

    Google Scholar 

  58. Winfree, A. T., in Lectures on Mathematics in the Life Sciences (edit. by Gersten-haber, M.) 2, 109 (Am. Math. Soc., Providence, Rhode Island, 1970).

    Google Scholar 

  59. Winfree, A. T., J. theor. Biol., 28, 327 (1970).

    Article  CAS  Google Scholar 

  60. Winfree, A. T., in Biological and Biochemical Oscillators (edit. by Chance, B., Pye, E. K., and Hess, B.) 461 (Academic Press, New York, 1973).

    Book  Google Scholar 

  61. Kauffman, S. A., and Wille, J., J. theoret. Biol. (in the press).

  62. Ottesen, E., thesis, Princeton Univ. (1965).

  63. Pittendrigh, C. S., in Circadian Clocks (edit. by Aschoff, J.), 277, (NorthHolland, Amsterdam, 1965).

    Google Scholar 

  64. Johnsson, A., Karlsson, H. G., Engelmann, W., Physiol. Plant, 28, 134 (1973).

    Article  Google Scholar 

  65. Eskin, A., in Biochronometry (edit. by Menaker, M.,) 55 (National Academy of Sciences, Washington, DC, 1971).

    Google Scholar 

  66. Winfree, A. T., J. camp. Physiol., 85, 105 (1973).

    Article  Google Scholar 

  67. Pittendrigh, C. S., in Neuroscience (edit. by Adelman, G.), (MIT Press, Cambridge, 1974).

    Google Scholar 

  68. Wever, R., Zeit. Vergl. Physiol., 51, 1 (1965).

    Article  Google Scholar 

  69. Ehret, C. F., in Biochronometry (edit. by Menaker, M.) 108 (National Academy of Sciences, Washington, DC, 1971).

    Google Scholar 

  70. Skopik, S. D., and Pittendrigh, C. S., Proc. natn. Acad. Sci. U.S.A., 58, 1862 (1967).

    Article  ADS  CAS  Google Scholar 

  71. Konopka, R., thesis, Calif. Inst. Tech. (1972).

  72. Nishiitsutsuji-Uwo, J., and Pittendrigh, C. S., Z. Vergl. Physiol., 58, 1 and 14 (1968).

    Article  Google Scholar 

  73. Gwinner, E., Science, 185, 72 (1974).

    Article  ADS  CAS  Google Scholar 

  74. Pittendrigh, C. S., in Life Sciences and Space Research, 122 (North-Holland, Amsterdam, 1967).

    Google Scholar 

  75. Hoffman, K., in Biochronometry (edit. by Menaker, M.) 134 (Nat. Acad. Sci., Washington, DC, 1974).

    Google Scholar 

  76. Pittendrigh, C. S., and Bruce, V., in Rhythmic and Synthetic Processes in Growth (edit. by Rudnick, D.) 75 (Princeton University Press, 1957).

    Google Scholar 

  77. Harker, E. J., Biol. Reviews, 33, 1 (1958).

    Article  ADS  Google Scholar 

  78. Pittendrigh, C. S., Harvey Lectures, 56, 93 (1961).

    CAS  Google Scholar 

  79. Wilkins, M. B., Pl. Physiol., Lancaster, 40, 907 (1965).

    Article  CAS  Google Scholar 

  80. Saunders, D. S., Proc. natn. Acad. Sci. U.S.A., 69, 2738 (1972).

    Article  ADS  CAS  Google Scholar 

  81. Winfree, A. T., in Biochronometry, (edit. by Menaker, M.), 150 (National Academy of Sciences, Washington, DC, 1971).

    Google Scholar 

  82. Chapman, R. N., Animal Ecology, (appendix) (McGraw-Hill, New York, 1931).

    Google Scholar 

  83. Goodwin, B. C., in Towards a Theoretical Biology, 3, (edit. by Waddington, C. H.) (Aldine, Chicago, 1970).

    Google Scholar 

  84. Sweeney, B. M., and Hastings, J. W., J. Protozool., 5, 217 (1958).

    Article  Google Scholar 

  85. Hastings, J. W., and Sweeney, B. M., Biol. Bull., 115, 440 (1958).

    Article  Google Scholar 

  86. Brinkmann, K., Biologische Rhythmen, 10, 138 (1967).

    Google Scholar 

  87. Edmunds, L. N. Jr, in Biochronometry (edit. by Menaker, M.), 594 (National Academy of Sciences, Washington, DC, 1971).

    Google Scholar 

  88. Cymborowski and Brady, Nature new Biol., 230, 221 (1970).

    Google Scholar 

Download references

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Winfree, A. Unclocklike behaviour of biological clocks. Nature 253, 315–319 (1975). https://doi.org/10.1038/253315a0

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