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Phylogenetic origins and adaptive evolution of avian and mammalian haemoglobin genes

Abstract

Recent years have seen rapid growth in amino acid sequence data on globins and nucleotide sequence data on haemoglobin genes and pseudogenes, and cladistic analysis1 of these data continues to reveal new facets of globin evolution. Our present findings demonstrate: (1) avian and mammalian embryonic α genes (π and ξ, respectively) had a monophyletic origin involving an α locus duplication about 400 Myr ago soon after the duplication which separated α and β genes; (2) much later in phylogeny, independent β-gene duplications produced the embryonic ρ locus of birds and embryonic ɛ and fetal γ loci of mammals. This parallels the earlier finding2 that myoglobins evolved more than once from generalized globin ancestors. Here we support the view2 that such globin evolution resulted from natural selection acting on mutations in duplicated genes. Thus, our evidence contradicts the neutralist view3,4 in which almost all amino acid substitutions in descent to extant globins evaded positive selection.

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References

  1. Goodman, M. Prog. Biophys. molec. Biol. 38, 105–164 (1981).

    Article  CAS  Google Scholar 

  2. Goodman, M. J. molec. Evol. 17, 114–120 (1981).

    Article  ADS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  4. Kimura, M. J. molec. Evol. 17, 110–113 (1981).

    Article  ADS  Google Scholar 

  5. Goodman, M. in Calcium-Binding Proteins: Structure and Function (eds Siegel, F. L., Carafoli, E., Kretsinger, R. H., MacLennan, D. H. & Wasserman, R. H.) 347–354 (Elsevier, New York, 1980).

    Google Scholar 

  6. Baba, M. L., Darga, L. L., Goodman, M. & Czelusniak, J. J. molec. Evol. 17, 197–213 (1981).

    Article  ADS  CAS  Google Scholar 

  7. De Jong, W. W., Zweers, A. & Goodman, M. Nature 292, 538–540 (1981).

    Article  ADS  CAS  Google Scholar 

  8. Tashian, R. E., Hewett-Emmett, D. & Goodman, M. in Protides of the Biological Fluids Colloq. 28 (ed. Peeters, H.) 153–156 (Pergamon, Oxford, 1980).

    Google Scholar 

  9. Beintema, J. et al. J. molec. Evol. 10, 49–71 (1977).

    Article  ADS  CAS  Google Scholar 

  10. Ladner, R. C., Heidner, E. J. & Perutz, M. F. J. mlec. Biol. 114, 385–414 (1977).

    Article  CAS  Google Scholar 

  11. Fermi, G. & Perutz, M. F. J. molec. Biol. 114, 421–431 (1977).

    Article  CAS  Google Scholar 

  12. Li, W-H., Gojóbori, T. & Nei, M. Nature 292, 237–239 (1981).

    Article  ADS  CAS  Google Scholar 

  13. Cleary, M. L., Schon, E. A. & Lingrel, J. B. Cell 26, 181–190 (1981).

    Article  CAS  Google Scholar 

  14. Efstratiadis, A. et al. Cell 21, 653–668 (1980).

    Article  CAS  Google Scholar 

  15. Hewett-Emmett, D. et al. Fedn Proc. 40, 1591 (1981).

    Google Scholar 

  16. Goodman, M., Romero-Herrera, A. E., Czelusniak, J., Dene, H. & Tashian, R. E. in Macromolecular Sequences in Systematic and Evolutionary Biology (ed. Goodman, M) (Plenum, New York, in the press).

  17. Dodgson, J. B., McCune, K. C., Rusling, D. J., Krust, A. & Engel, J. D. Proc. natn. Acad. Sci. U.S.A. 78, 5998–6002 (1981).

    Article  ADS  CAS  Google Scholar 

  18. Aschauer, J., Sanguansermsri, T. & Braunitzer, G. Hoppe-Seyler's Z. physiol. Chem. 362, 1159–1162 (1981).

    CAS  PubMed  Google Scholar 

  19. Roninson, I. B. & Ingram, V. M. Proc. natn. Acad. Sci. U.S.A. 78, 4782 (1981).

    Article  ADS  CAS  Google Scholar 

  20. Hardison, R. C. J. biol. Chem. 2566, 11780–11786 (1981).

    Google Scholar 

  21. Hansen, J. N., Konkel, D. A. & Leder, P. J. biol. Chem. 257, 1048–1052 (1982).

    CAS  PubMed  Google Scholar 

  22. Holmquist, R. J. molec. Biol. 135, 929–938 (1979).

    Article  Google Scholar 

  23. Wilson, J. T. et al. J. biol. Chem. 255, 2807–2815 (1980).

    CAS  PubMed  Google Scholar 

  24. Heindell, H. C. et al. Cell 15, 43–54 (1978).

    Article  CAS  Google Scholar 

  25. Proudfoot, N. J. & Maniatis, T. Cell 21, 537–544 (1980).

    Article  CAS  Google Scholar 

  26. Nishioka, Y. & Leder, P. Cell 18, 875–882 (1979).

    Article  CAS  Google Scholar 

  27. Vanin, E. F., Goldberg, G. I., Tucker, P. W. & Smithies, O. Nature 286, 222–226 (1980).

    Article  ADS  CAS  Google Scholar 

  28. Nishioka, Y., Leder, A. & Leder, P. Proc. natn. Acad. Sci. U.S.A. 77, 2806–2809 (1980).

    Article  ADS  CAS  Google Scholar 

  29. Paddock, G. V. & Gaubatz, J. Eur. J. Biochem. 117, 269–273 (1981).

    Article  CAS  Google Scholar 

  30. Richardson, L., Cappello, J., Cochran, M. D., Armentrout, R. W. & Brown, R. D. Devl Biol. 78, 161–172 (1980).

    Article  CAS  Google Scholar 

  31. Williams, J. G., Kay, R. M. & Patient, R. K. Nucleic Acids Res. 8, 4247–4258 (1980).

    Article  CAS  Google Scholar 

  32. Richards, R. I. et al. Nucleic Acids Res. 7, 1137–1146 (1980).

    Article  Google Scholar 

  33. Niessing, J. Biochem. Int. 2, 113–120 (1981).

    CAS  Google Scholar 

  34. Haupe, A., Therwath, A., Soriano, P. & Galibert, F. Gene 14, 11–21 (1980).

    Google Scholar 

  35. Barelle, F. E., Shoulders, C. C. & Proudfoot, N. J. Cell 21, 621–626 (1980).

    Article  Google Scholar 

  36. Slightom, J. L., Blechl, A. E. & Smithies, O. Cell 21, 627–638 (1980).

    Article  CAS  Google Scholar 

  37. Konkel, D. A., Maizel, J. V. Jr & Leder, P. Cell 18, 865–873 (1981).

    Article  Google Scholar 

  38. Cleary, M. L., Haynes, J. R., Schon, E. A. & Lingrel, J. B. Nucleic Acids Res. 8, 4791–4802 (1980).

    Article  CAS  Google Scholar 

  39. Lacy, E. & Maniatis, T. Cell 21, 545–553 (1980).

    Article  CAS  Google Scholar 

  40. Van Ooyen, A., van den Berg, J., Mantai, N. & Weissman, C. Science 206, 337–344 (1979).

    Article  ADS  CAS  Google Scholar 

  41. Hardison, R. C. et al. Cell 18, 1285–1297 (1979).

    Article  CAS  Google Scholar 

  42. Spritz, R. A., De Riel, J. K., Forget, G. B. & Weissman, S. Cell 21, 639–646 (1980).

    Article  CAS  Google Scholar 

  43. Lawn, R. M., Efstratiadis, A., O'Connell, C. & Maniatis, T. Cell 21, 647–651 (1980).

    Article  CAS  Google Scholar 

  44. Partington, G. A. & Baralle, F. E. J. molec. Biol. 145, 463–470 (1981).

    Article  CAS  Google Scholar 

  45. Haynes, J. R. et al. J. biol. Chem. 255, 6355–6367 (1980).

    CAS  PubMed  Google Scholar 

  46. Haynes, J. R., Rosteck, P. Jr & Lingrel, J. B. Proc. natn. Acad. Sci. U.S.A. 77, 7127–1731 (1980).

    Article  ADS  CAS  Google Scholar 

  47. Kretschmer, P. J. et al. J. biol. Chem. 256, 1975–1982 (1981).

    CAS  PubMed  Google Scholar 

  48. Barrie, P. A., Jeffreys, A. J. & Scott, A. F. J. molec. Biol. 149, 319–336 (1981).

    Article  CAS  Google Scholar 

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Czelusniak, J., Goodman, M., Hewett-Emmett, D. et al. Phylogenetic origins and adaptive evolution of avian and mammalian haemoglobin genes. Nature 298, 297–300 (1982). https://doi.org/10.1038/298297a0

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