Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Darwinian evolution in the genealogy of haemoglobin

Nature volume 253, pages 603–608 (1975)Cite this article

Abstract

Frequencies of mutations between reconstructed ancestor and descendant sequences of codons for metazoan globin chains show that natural selection guided protein evolution. Mutations which improved haemoglobin function were accepted at an accelerated rate in the first vertebrates. Rates decelerated after functional opportunities had been exploited.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Ellfolk, N., and Sievers, G., Acta Chem. Scand., 25, 3532–3534 (1971).

    Article  PubMed  CAS  Google Scholar 

  2. Buse, G., Braig, S., and Braunitzer, G., Z. Physiol. Chem., 349, 1686–1690 (1969).

    Google Scholar 

  3. Imamura, T., Baldwin, T. O., and Riggs, A., J. biol. Chem., 247, 2785–2797 (1972).

    Article  PubMed  CAS  Google Scholar 

  4. Tentori, L., Vivaldi, G., Carta, S., Marinucci, M., Massa, A., Antonini, E., and Brumori, M., Int. J. Peptide Protein Res., 5, 187–200 (1973).

    Article  CAS  Google Scholar 

  5. Li, S. L., and Riggs, A., J. biol. Chem., 245, 6149–6169 (1970).

    Article  PubMed  CAS  Google Scholar 

  6. Braunitzer, G., and Fujuki, H., Naturwissenschaften, 56, 322–323 (1969).

    Article  ADS  PubMed  CAS  Google Scholar 

  7. Air, G. M., Thompson, E. O. P., Richardson, B. J., and Sharman, G. B., Nature, 229, 391–394 (1971).

    Article  ADS  PubMed  CAS  Google Scholar 

  8. Romero-Herrera, A. E., and Lehmann, H., Nature new Biol., 232, 149–152 (1971).

    Article  CAS  Google Scholar 

  9. Dautrevaux, M., Boulanger, Y., Han, K., and Biserte, G., Eur. J. Biochem., 11, 267–277 (1969).

    Article  PubMed  CAS  Google Scholar 

  10. Han, K., Tetaert, D., Moschetto, Y., and Dautrevaux, M., Eur. J. Biochem., 27, 585–592 (1972).

    Article  PubMed  CAS  Google Scholar 

  11. Han, K., Dautrevaux, M., Chaila, X., and Biserte, G., Eur. J. Biochem., 16, 465–471 (1970).

    Article  PubMed  CAS  Google Scholar 

  12. Bradshaw, R. A., and Gurd, R. R. N., J. biol. Chem., 244, 2167–2181 (1969).

    Article  PubMed  CAS  Google Scholar 

  13. Karadjova, M., Nedkov, P., Bakardjieva, A., and Genov, N., Biochim. biophys. Acta, 221, 136–139 (1970).

    Article  PubMed  CAS  Google Scholar 

  14. Kluh, I., and Bakardjieva, A., FBBS Lett., 17, 31–34 (1971).

    Article  CAS  Google Scholar 

  15. Edmundson, A. B., Nature, 205, 883–887 (1965).

    Article  ADS  CAS  Google Scholar 

  16. Whittaker, R. G., Fisher, W. K., and Thompson, E. O. P., Aust. J. biol. Sci., 25, 989–1004 (1972).

    Article  PubMed  CAS  Google Scholar 

  17. Thompson, E. O. P., and Air, G. M., Aust. J. biol. Sci., 24, 1199–1217 (1971).

    Article  PubMed  CAS  Google Scholar 

  18. Air, G. M., and Thompson, E. O. P., Aust. J. biol. Sci., 22, 1437–1454 (1969).

    Article  CAS  Google Scholar 

  19. Schroeder, W. A., Shelton, J. R., Shelton, J. B., Cormick, J., and Jones, R. T., Biochemistry, 2, 992–1008 (1963).

    Article  PubMed  CAS  Google Scholar 

  20. Jones, R. T., Brimhall, B., and Duerst, M., Fedn. Proc., 30, Part 2 Abst. 1207 (1971).

    Google Scholar 

  21. Popp, R. A., Biochim. biophys. Acta, 303, 52–60 (1973).

    Article  PubMed  CAS  Google Scholar 

  22. Matsuda, G., Maita, T., Ota, H., Araya, A., Nakashima, Y., Ishii, U., and Nakashima, M., Int. J. Peptide Protein Res., 5, 405–418 (1973).

    Article  CAS  Google Scholar 

  23. Matsuda, G., Maita, T., Takei, H., Ota, H., Yamaguchi, M., Miyauchi, T., and Migita, M., J. Biochem., Tokyo, 64, 279–282 (1968).

    Article  CAS  Google Scholar 

  24. Matsuda, G., Maita, T., Watanabe, B., Araya, A., Morokuma, K., Goodman, M., and Prychodko, W., Z. physiol. Chem., 354, 1153–1155 (1973).

    CAS  Google Scholar 

  25. Matsuda, G., Maita, T., Nakashima, Y., Barnabas, J., Ranjekar, P. K., and Gandhi, N. S., Int. J. Peptide Protein Res., 5, 423–425 (1973).

    Article  CAS  Google Scholar 

  26. Braunitzer, G., Gehring-Muller, R., Hilschmann, N., Hilse, K., Hobom, G., Rudloff, V., and Wittmann-Liebold, B., Z. physiol. Chem., 325, 283–286 (1961).

    Article  CAS  Google Scholar 

  27. Matsuda, G., Maita, T., Watanabe, B., Araya, A., Morokuma, K., Ota, Y., Goodman, M., Barnabas, J., and Prychodko, W., Z. physiol. Chem., 354, 1513–1516 (1973).

    CAS  Google Scholar 

  28. Matsuda, G., Matia, T., Watanabe, B., Ota, H., Araya, A., Goodman, M., and Prychodko, W., Int. J. Peptide Protein Res., 5, 419–421 (1973).

    Article  CAS  Google Scholar 

  29. Best, J. S., Flamm, V., and Braunitzer, G., Z. physiol. Chem., 350, 563–580 (1969).

    Article  CAS  Google Scholar 

  30. Smith, D. B., and Chung, W. P., Can. J. Biochem., 48, 1160–1164 (1970).

    Article  PubMed  CAS  Google Scholar 

  31. Dayhoff, M. O., Atlas of protein sequence and structure, 5 (National Biochemical Research Foundation, Silver Spring, Maryland, 1972).

    Google Scholar 

  32. Babin, D. R., Schroeder, W. A., Shelton, J. R., Shelton, J. B., and Robberson, B., Biochemistry, 5, 1297–1310 (1966).

    Article  PubMed  CAS  Google Scholar 

  33. Schroeder, W. A., Shelton, J. R., Shelton, J. B., Robberson, B., and Babin, D. R., Archs Biochem. Biophys., 120, 124–135 (1967).

    Article  CAS  Google Scholar 

  34. Boyer, S. H., Hathaway, P., Pascasio, F., Bordley, J., Orton, C., and Naughton, M. A., J. biol. Chem., 242, 2211–2232 (1967).

    Article  PubMed  CAS  Google Scholar 

  35. Matsuda, G., Maita, T., Mizumo, K., and Ota, H., Nature new Biol., 244, 244 (1973).

    Article  ADS  PubMed  CAS  Google Scholar 

  36. Chauvert, J., Acher, R., Biochemistry, 11, 916–926 (1972).

    Article  Google Scholar 

  37. Hilse, K., and Braunitzer, G., Z. physiol. Chem., 349, 433–450 (1968).

    Article  CAS  Google Scholar 

  38. Powers, D. A., and Edmundson, A. B., J. biol. Chem., 247, 6694–6702 (1972).

    Article  PubMed  CAS  Google Scholar 

  39. Matsuda, G., Takei, H., Wu, K. L., and Shiozawa, T., Int. J. Peptide Protein Res., 3, 149–150 (1971).

    Google Scholar 

  40. Whittaker, R. G., Fisher, W. K., and Thompson, E. O. P., Aust. J. biol. Sci., 26, 877–888 (1973).

    Article  PubMed  CAS  Google Scholar 

  41. Beard, J. M., Thompson, E. O. P., Aust. J. biol. Sci., 24, 765–786 (1971).

    Article  PubMed  CAS  Google Scholar 

  42. Von Ehrenstein, G., Cold Spring Harb. Symp. quant. Biol., 31, 705–714 (1966).

    Article  PubMed  CAS  Google Scholar 

  43. Matsuda, G., Gehring-Muller, R., and Braunitzer, G., Biochem. Z., 338, 669–673 (1963).

    PubMed  CAS  Google Scholar 

  44. Yamaguchi, Y., Horie, H., Matsuo, A., Sasakawa, S., and Satake, K., J. Biochem., Tokyo, 58, 186–187 (1965).

    Article  CAS  Google Scholar 

  45. Schroeder, W. A., Shelton, J. R., Shelton, J. B., Robberson, B., and Babin, D. R., Archs Biochem. Biophys., 120, 1–14 (1967).

    Article  CAS  Google Scholar 

  46. Popp, R. A., J. molec. Biol., 27, 9–16 (1967).

    Article  PubMed  CAS  Google Scholar 

  47. Matsuda, G., et al., Z. physiol. Chem., 354, 1517–1520 (1973).

    CAS  Google Scholar 

  48. Perutz, M. F., Kendrew, J. C., and Watson, H. C., J. molec. Biol., 13, 669–678 (1965).

    Article  CAS  Google Scholar 

  49. Perutz, M. F., Proc. R. Soc., B 173, 113–140 (1969).

    ADS  CAS  Google Scholar 

  50. Perutz, M. F., Nature, 228, 726–734 (1970).

    Article  ADS  PubMed  CAS  Google Scholar 

  51. Perutz, M. F., Nature, 228, 734–739 (1970).

    Article  ADS  CAS  Google Scholar 

  52. Perutz, M. F., and Ten Eyck, L. F., Cold Spring Harb. Symp. quant. Biol., 36, 295–310 (1972).

    Article  PubMed  CAS  Google Scholar 

  53. Arnone, A., Nature, 237, 146–149 (1972).

    Article  ADS  PubMed  CAS  Google Scholar 

  54. Kimura, M., Nature, 217, 624–626 (1968).

    Article  ADS  PubMed  CAS  Google Scholar 

  55. King, J. L., and Jukes, T. H., Science, 164, 788–798 (1969).

    Article  ADS  PubMed  CAS  Google Scholar 

  56. Moore, G. W., Barnabas, J., and Goodman, M., J. theor. Biol., 38, 459–485 (1973).

    Article  PubMed  CAS  ADS  Google Scholar 

  57. Goodman, M., Moore, G. W., Barnabas, J., and Matsuda, G., J. molec. Evol., 3, 1–48 (1974).

    Article  ADS  PubMed  CAS  Google Scholar 

  58. Estabrook, G. F., J. theor. Biol., 21, 421–438 (1968).

    Article  PubMed  CAS  ADS  Google Scholar 

  59. Farris, J. S., Syst. Zool., 19, 83–92 (1970).

    Article  Google Scholar 

  60. Fitch, W. M., Syst. Zool., 20, 406–416 (1971).

    Article  Google Scholar 

  61. Hartigan, J. A., Biometrics, 29, 53–65 (1973).

    Article  Google Scholar 

  62. Sankoff, D., Publication Centre de Recherches Mathematiques Tech. Rep. No. 262 (Universite de Montreal, 1973).

  63. Sokal, R. R., and Michener, C. D., Kansas Univ. sci. Bull., 38, 1409–1438 (1958).

    Google Scholar 

  64. Holmquist, R., Cantor, L. R., and Jukes, T. H., J. molec. Biol., 64, 145–161 (1972).

    Article  PubMed  CAS  Google Scholar 

  65. Jukes, T. H., and Holmquist, R., J. molec. Biol., 64, 163–179 (1972).

    Article  PubMed  CAS  Google Scholar 

  66. Goodman, M., Moore, G. W., and Matsuda, G., in Proc. third Int. Conf. Isozymes (edit. by Markert, C. L.) (Academic Press, New York in the press).

  67. Young, J. Z., The life of vertebrates (Oxford University Press, 1962).

    Book  Google Scholar 

  68. Romer, A. S., Vertebrate paleontology (University of Chicago Press, 1966).

    Google Scholar 

  69. McKenna, M. C., Ann. N. Y. Acad. Sci., 167, 217–240 (1969).

    Article  ADS  Google Scholar 

  70. Simons, E. L., Primate evolution (Macmillan, New York, 1972).

    Google Scholar 

  71. Romero-Herrera, A. E., Lehmann, H., Joysey, K. A., and Friday, A. E., Nature, 246, 389–395 (1973).

    Article  ADS  PubMed  CAS  Google Scholar 

  72. Schopf, J. W., Ford, T. D., and Breed, W. J., Science, 179, 1319–1321 (1973).

    Article  ADS  PubMed  CAS  Google Scholar 

  73. Glaessner, M. F., and Wade, M., Paleontology, 9, 599–628 (1966).

    Google Scholar 

  74. Cloud, P., Am. Scientist, 62, 54–66 (1974).

    ADS  CAS  Google Scholar 

  75. Goodman, M., Human Biol., 33, 131–162 (1961).

    PubMed  CAS  Google Scholar 

  76. Goodman, M., in Classification and Human Evolution (edit. by Washburn, S. L.) (Aldine Press, Chicago, 1963).

    Google Scholar 

  77. Goodman, M., in Protides of the Biological Fluids, 12 (edit. by Peters, H.) (Elsevier, Amsterdam, 1965).

    Google Scholar 

  78. Zuckerkandl, E., and Pauling, L., in Evolving Genes and Proteins (edit. by Bryson, V., and Vogel, H. J.) (Academic Press, New York, 1965).

    Google Scholar 

  79. Goodman, M., Barnabas, J., Matsuda, G., and Moore, G. W., Nature, 223, 604–613 (1971).

    Article  ADS  Google Scholar 

  80. Dickerson, R. E., J. molec. Evol., 1, 26–45 (1971).

    Article  ADS  PubMed  CAS  Google Scholar 

  81. Kimura, M., Proc. natn. Acad. Sci. U.S.A., 63, 1181–1188 (1969).

    Article  ADS  CAS  Google Scholar 

  82. Kimura, M., and Ohta, T., Proc. natn. Acad. Sci. U.S.A., 71, 2848–2852 (1974).

    Article  ADS  CAS  Google Scholar 

  83. Langley, C. H., and Fitch, W. M., J. molec. Evol. 3, 161–177 (1974).

    Article  ADS  PubMed  CAS  Google Scholar 

  84. Benesch, R., Benesch, R. E., and Yung, S., Biochem. biophys. Res. Commun., 55, 261–265 (1973).

    Article  PubMed  CAS  Google Scholar 

  85. Benesch, R., and Benesch, R. E., Science, 185, 905–908 (1974).

    Article  ADS  PubMed  CAS  Google Scholar 

  86. Andersen, M. E., and Gibson, Q. H., J. biol. Chem. 246, 4790–4799 (1971).

    Article  PubMed  CAS  Google Scholar 

  87. Behlke, J., and Schelee, W., FEBS Lett., 7, 177–179 (1970).

    Article  PubMed  CAS  Google Scholar 

  88. Simpson, G. G., in Protides of the Biological Fluids, 12 (edit. by Peters, M.) (Elsevier, Amsterdam, 1965).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Wayne State University, Detroit, Michigan, 48201

    Morris Goodman & G. William Moore

  2. Department of Biochemistry, Nagasaki University, School of Medicine, Nagasaki, Japan

    Genji Matsuda

Authors
  1. Morris Goodman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. William Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Genji Matsuda
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goodman, M., Moore, G. & Matsuda, G. Darwinian evolution in the genealogy of haemoglobin. Nature 253, 603–608 (1975). https://doi.org/10.1038/253603a0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/253603a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing