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The phylogeny of human globin genes investigated by the maximum parsimony method

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Abstract

Gene phylogenetic trees were constructed by the maximum parsimony method for various sets of ninety six globin chain amino acid sequences spanning plant and animal kingdoms. The method, executed by several computer programs, constructed ancestor and descendant globin messengers on tree topologies which required the least number of nucleotide replacements to account for the evolution of the globins. The human myoglobin-hemoglobin divergence was traced to a gene duplication which occurred either in the first vertebrates or earlier yet in the common ancestor of chordates and annelids, the alpha-beta divergence to a gene duplication in the common ancestor of teleosts and tetrapods, the gamma divergence from typical beta chains to a gene duplication in basal therian mammals, and the delta separation from beta to a duplication in the basal catarrhine primates. Evidence was provided by the globin phylogenies for the hominoid affinities of the gibbon and the close phyletic relationship of the African apes to man. Over the period of teleos-tetrapod divergence the globin messengers evolved at an average rate of 18.5 nucleotide replacements per 100 codons per 108 years, a faster rate than most previous estimates. Very fast and very slow rates were encountered in different globin lineages and at different stages of descent, reducing the effectiveness of globins as molecular clocks. Rates increased with gene duplication and decreased after selection discovered useful specializations in the products of genes which had previously been freer to accept mutations. The early eutherian radiation was characterized by rapid rates of globin evolution, but the later hominoid radiation by extremely slow rates. This pattern was related to more complicated grades of internal organization evolving in human ancestors. The types of nucleotide replacements in the globin messengers over the long course of globin evolution did not seem indicative of any special mutational mechanisms.

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References

  • Air, G. M., Thompson, E. O. P.: Aust. J. Biol. Sci.22, 1437 (1969)

    Google Scholar 

  • Air, G. M., Thompson, E. O. P., Richardson, B. J., Sharman, G. B.: Nature229, 391 (1971)

    PubMed  Google Scholar 

  • Babin, D. R., Schroeder, W. A., Shelton, J. R., Shelton, J. B., Robberson, B.: Biochem.5, 1297 (1966)

    Google Scholar 

  • Barnabas, J., Goodman, M., Moore, G. W.: J. Mol. Biol.69, 249 (1972)

    PubMed  Google Scholar 

  • Barnicot, N. A., Hewett-Emmett, D.: In: Prosimian biology, R. D. Martin, G. A. Doyle, A. C. Walker, Eds. London: Duckworth (in press)

  • Beale, D.: Biochem. J.103, 129 (1967)

    PubMed  Google Scholar 

  • Beard, J. M., Thompson, E. O. P.: Aust. J. Biol. Sci.24, 765 (1971)

    PubMed  Google Scholar 

  • Best, J. S., Flamm, V., Braunitzer, G.: Z. Physiol. Chem.350, 563 (1969)

    Google Scholar 

  • Boyer, S. H., Crosby, E. F., Noyes, A. N., Fuller, G. F., Leslie, S. E., Donaldson, L. J., Vrablik, G. R., Schefer, E. W., Jr., Thurmon, T. F.: Biochem. Genet.5, 405 (1971a)

    PubMed  Google Scholar 

  • Boyer, S. H., Hathaway, P., Pascasio, F., Bordley, J., Orton, C., Naughton, M. A.: J. Biol. Chem.242, 2211 (1967)

    PubMed  Google Scholar 

  • Boyer, S. H., Noyes, A. N., Boyer, M. L., Marr, K.: J. Biol. Chem.248, 992 (1973)

    PubMed  Google Scholar 

  • Boyer, S. H., Noyes, A. N., Vrablik, G. R., Donaldson, L. J., Schaefer, E. W., Jr., Gray, C. W., Thurmon, T. F.: Science171, 182 (1971b)

    PubMed  Google Scholar 

  • Bradshaw, R. A., Gurd, R. R. N.: J. Biol. Chem.244, 267 (1969)

    Google Scholar 

  • Braunitzer, G., Fujiki, H.: Naturwissenschaften56, 322 (1969)

    PubMed  Google Scholar 

  • Braunitzer, G., Gehring-Muller, R., Hilschmann, N., Hilse, K., Hobom, G., Rudloff, V., Wittmann-Liebold, B.: Z. Physiol. Chem.325, 283 (1961)

    Google Scholar 

  • Braunitzer, G., Hilse, K., Rudloff, V., Hilschmann, N.: Adv. Protein Chem.19, 34 (1964)

    Google Scholar 

  • Braunitzer, G., Kohler, H.: Z. Physiol. Chem.343, 290 (1966)

    Google Scholar 

  • Buse, G., Braig, S., Braunitzer, G.: Hoppe-Seylers Z. Physiol. Chem.349, 1686 (1969)

    Google Scholar 

  • Chauvet, J., Acher, R.: Biochem.11, 916 (1972)

    Google Scholar 

  • Chiarelli, B.: Am. J. Phys. Anthrop.24, 155 (1966)

    PubMed  Google Scholar 

  • Dautrevaux, M., Boulanger, Y., Han, K., Biserte, G.: Eur. J. Biochem.11, 267 (1969)

    PubMed  Google Scholar 

  • Dayhoff, M. O.: Atlas of protein sequence and structure, Vol. 5. Maryland: National Biomedical Research Foundation 1972

    Google Scholar 

  • DeJong, W. W. W.: Biochim. Biophys. Acta251, 217 (1971)

    PubMed  Google Scholar 

  • Dickerson, R. E.: J. Molec. Evolution1, 26 (1971)

    Google Scholar 

  • Edmundson, A. B.: Nature205, 383 (1965)

    Google Scholar 

  • Ellfolk, N., Sievers, G.: Acta Chem. Scand.25, 3532 (1971)

    PubMed  Google Scholar 

  • Fitch, W. M.: Syst. Zool.20, 406 (1971)

    Google Scholar 

  • Fitch, W. M.: Humangenetik16, 67 (1972)

    PubMed  Google Scholar 

  • Fitch, W. M., Margoliash, E.: Science155, 279 (1967)

    PubMed  Google Scholar 

  • Gentry, A. U.: Fossil vertebrates of Africa, L. S. B. Leakey, R. J. G. Savage, Eds., Vol. 2. London: Academic Press 1970

    Google Scholar 

  • Goodman, M.: Human Biol.33, 131 (1961)

    PubMed  Google Scholar 

  • Goodman, M.: In: Classification and human evolution, S. L. Washburn, Ed., p. 204. Chicago: Aldine Press 1963

    Google Scholar 

  • Goodman, M.: In: Protides of the biological fluids, H. Peters, Ed., Vol. 12, p. 70. Amsterdam: Elsevier 1965

    Google Scholar 

  • Goodman, M., Barnabas, J., Matsuda, G., Moore, G. W.: Nature233, 604 (1971)

    PubMed  Google Scholar 

  • Goodman, M., Barnabas, J., Moore, G. W.: J. Human Evol.1, 663 (1972)

    Google Scholar 

  • Goodman, M., Moore, G. W.: Systematic Zoology (in press)

  • Han, K., Dautrevaux, M., Chaila, X., Biserte, G.: Eur. J. Biochem.16, 465 (1970)

    PubMed  Google Scholar 

  • Han, K., Tetaert, D., Moschetto, Y., Dautrevaux, M.: Eur. J. Biochem.27, 585 (1972)

    PubMed  Google Scholar 

  • Hill, R. L.: Unpublished results in handbook of biochemistry, H. A. Sober, Ed., p. C-174. Chicago: The Chemical Rubber Company 1968

    Google Scholar 

  • Hilse, K., Braunitzer, G.: Z. Physiol. Chem.349, 433 (1968)

    Google Scholar 

  • Holmquist, R., Cantor, C. R., Jukes, T. H.: J. Mol. Biol.64, 145 (1972)

    Google Scholar 

  • Huber, R., Epp, O., Steigemann, W., Formanek, H.: Eur. J. Biochem.19, 42 (1971)

    PubMed  Google Scholar 

  • Huisman, T. H. J., Adams, H. R., Dimmock, M. O., Edwards, W. E., Wilson, J. B.: J. Biol. Chem.242, 2534 (1967)

    PubMed  Google Scholar 

  • Huisman, T. H. J., Brandt, G., Wilson, J. B.: J. Biol. Chem.243, 3675 (1968a)

    PubMed  Google Scholar 

  • Huisman, T. H. J., Dasher, G. A., Moretz, W. H., Jr., Dozy, A. M., Wilson, J. B., Vliet, G. V.: Biochem. J.107, 745 (1968b)

    Google Scholar 

  • Huisman, T. H. J., Schroeder, W. A.: New aspects of the structure, function, and synthesis of hemoglobins. Cleveland: CRC Press 1971

    Google Scholar 

  • Imamura, T., Baldwin, T. O., Riggs, A.: J. Biol. Chem.247, 2785 (1972)

    PubMed  Google Scholar 

  • Ingram, V. M., Stretton, A. O. W.: Biochim. Biophys. Acta63, 20 (1962)

    PubMed  Google Scholar 

  • Jones, R. T.: Cold Spring Harbor Symp. Quant. Biol.29, 297 (1964)

    PubMed  Google Scholar 

  • Jones, R. T., Brimhall, B., Duerst, M.: Fed. Proc.30, pt. 2 of two volumes, Abst. 1207 (1971)

  • Jukes, T. H., Holmquist, R.: J. Mol. Biol.64, 163 (1972)

    Google Scholar 

  • Karadjova, M., Nedkov, P., Bakardjieva, A., Genov, N.: Biochim. Biophys. Acta221, 136 (1970)

    PubMed  Google Scholar 

  • Kendrew, J. C., Watson, H. C., Strandberg, B. E., Dickerson, R. E., Phillips, D. C., Shore, V. C.: Nature190, 666 (1961)

    PubMed  Google Scholar 

  • Kilmartin, J. V., Clegg, J. B.: Nature213, 269 (1967)

    PubMed  Google Scholar 

  • Kimura, M.: Proc. Nat. Acad. Sci., Wash.63, 1181 (1969)

    Google Scholar 

  • Kluh, I., Bakardjieva, A.: FEBS Letters17, 31 (1971)

    PubMed  Google Scholar 

  • Kohne, D. E., Chiscon, J. A., Hoyer, B. H.: J. Human Evol.1, 627 (1972)

    Google Scholar 

  • LeGros Clark, W. E.: The antecedents of man: An introduction to the evolution of primates. Chicago: Quadrangle Books 1960

    Google Scholar 

  • Lehmann, H., Carrell, R. W.: Brit. Med. J.4, 748 (1968)

    PubMed  Google Scholar 

  • Lewis, O. J.: J. Human Evol.2, 1 (1973)

    Google Scholar 

  • Li, S. L., Riggs, A.: J. Biol. Chem.245, 6149 (1970)

    PubMed  Google Scholar 

  • Love, W. E., Klock, P. A., Lattman, E. E., Padlan, E. A., Ward, K. B., Jr., Hendrickson, W. A.: Cold Spring Harbor Symp. Quant. Biol.36, 349 (1972)

    PubMed  Google Scholar 

  • Matsuda, G., Gehring-Muller, R., Braunitzer, G.: Biochem. Zeit.338, 669 (1963)

    Google Scholar 

  • Matsuda, G., Maita, T., Mezuno, K., Ota, H.: Nature299, 244 (1973)

    Google Scholar 

  • Matsuda, G., Maita, T., Ota, H., Tachikawa, I., Tanaka, Y., Araya, A., Nakashima, Y.: Int. J. Protein Res.3, 53 (1971a)

    PubMed  Google Scholar 

  • Matsuda, G., Maita, T., Ota, H., Takei, H.: Int. J. Protein Res.2, 99 (1970)

    PubMed  Google Scholar 

  • Matsuda, G., Maita, T., Ota, H., Araya, A., Tachikawa, I., Terao, Y., Tanaka, Y.: Int. J. Protein Res.4, 327 (1972).

    Google Scholar 

  • Matsuda, G., Takei, H., Wu, K. C., Shiozawa, T.: Int. J. Protein Res.3, 149 (1971b)

    PubMed  Google Scholar 

  • McKenna, M. C.: Ann. N.Y. Acad. Sci.167, 217 (1969)

    Google Scholar 

  • Moore, G. W., Barnabas, J., Goodman, M.: J. Theor. Biol.38, 459 (1973)

    PubMed  Google Scholar 

  • Moore, G. W., Goodman, M., Barnabas, J.: J. Theor. Biol.38, 423 (1973)

    PubMed  Google Scholar 

  • Padlan, E. A., Love, W. E.: Nature220, 376 (1968)

    PubMed  Google Scholar 

  • Perutz, M. F.: Proc. Roy. Soc.173B, 113 (1969)

    Google Scholar 

  • Perutz, M. F., Muirhead, H., Cox, J. M., Goaman, L. C. G.: Nature219, 131 (1968)

    PubMed  Google Scholar 

  • Perutz, M. F., TenEyck, L. F.: Cold Spring Harbor Symp. Quant. Biol.36, 295 (1972)

    PubMed  Google Scholar 

  • Pilbeam, P.: Nature219, 1335 (1968)

    PubMed  Google Scholar 

  • Popp, R. A.: J. Mol. Biol.27, 9 (1967)

    PubMed  Google Scholar 

  • Powers, D. A., Edmundson, A. B.: J. Biol. Chem.247, 6686 (1972a)

    PubMed  Google Scholar 

  • Powers, D. A., Edmundson, A. B.: J. Biol. Chem.247, 6694 (1972b)

    PubMed  Google Scholar 

  • Rifkin, D. B., Konigsberg, W.: Biochim. Biophys. Acta104, 457 (1965)

    PubMed  Google Scholar 

  • Romer, A. S.: Vertebrate paleontology. Chicago: The University of Chicago Press 1966

    Google Scholar 

  • Romero-Herrera, A. E., Lehmann, H.: Nature, NewBiology232, 149 (1971a)

    Google Scholar 

  • Romero Herrera, A. E., Lehmann, H.: Biochim. Biophys. Acta251, 482 (1971b)

    PubMed  Google Scholar 

  • Romero Herrera, A. E., Lehmann, H.: Biochim. Biophys. Acta278, 62 (1972a)

    PubMed  Google Scholar 

  • Romero Herrera, H. E., Lehmann, H.: Biochim. Biophys. Acta278, 465 (1972b)

    PubMed  Google Scholar 

  • Schopf, J. W., Ford, T. D., Breed, W. J.: Science179, 1319 (1973)

    Google Scholar 

  • Schroeder, W. A., Shelton, J. R., Shelton, J. B., Cormick, J., Jones, R. T.: Biochemistry2, 992 (1963)

    Google Scholar 

  • Schroeder, W. A., Shelton, J. R., Shelton, J. B., Robberson, B., Babin, D. R.: Arch. Biochem. Biophys.120, 124 (1967a)

    PubMed  Google Scholar 

  • Schroeder, W. A., Shelton, J. R., Shelton, J. B., Robberson, B., Babin, D. R.: Arch. Biochem. Biophys.120, 1 (1967b)

    PubMed  Google Scholar 

  • Simons, E. L.: Primate evolution: An introduction to man's place in nature. New York: MacMillan 1972

    Google Scholar 

  • Simpson, G. G.: The principles of classification and a classification of mammals. Bull. Amer. Mus. Nat. Hist., Vol. 85, New York (1945)

  • Smith, D. B., Chung, W. P.: Canad. J. Biochem.48, 1160 (1970)

    Google Scholar 

  • Sokal, R. R., Michener, C. D.: Kansas Univ. Sci. Bull.38, 1049 (1958)

    Google Scholar 

  • Thompson, E. O. P., Air, G. M.: Aust. J. Biol. Sci.24, 1199 (1971)

    PubMed  Google Scholar 

  • Vogel, F.: Humangenetik16, 71 (1972)

    PubMed  Google Scholar 

  • Von Ehrenstein, G.: Cold Spring Harbor Symp. Quant. Biol.31, 705 (1966)

    PubMed  Google Scholar 

  • Webb. D.: Osteology of Camelops. Bull Los Angeles County Mus. Sci. No. 1, p. 1 (1965)

    Google Scholar 

  • Whittaker, R. G., Fisher, W. K., Thompson, E. O. P.: Aust. J. Biol. Sci.25, 989 (1972)

    PubMed  Google Scholar 

  • Wilson, J. B., Edwards, W. C., McDaniel, M., Dobbs, M. M., Huisman, T. H. J.: Arch. Biochem. Biophys.115, 385 (1966)

    Google Scholar 

  • Wollmer, A., Buse, G., Sick, H., Gersonde, K.: Eur. J. Biochem.24, 547 (1972)

    PubMed  Google Scholar 

  • Yamaguchi, Y., Horie, H., Matsuo, A., Sasakawa, S., Satake, K.: J. Biochem.58, 186 (1965)

    PubMed  Google Scholar 

  • Young, J. Z.: The life of the vertebrates, 2nd ed. Oxford: Univ. Press 1962

    Google Scholar 

  • Zuckerkandl, E., Derancourt, J., Vogel, H.: J. Mol. Biol.59, 473 (1971)

    PubMed  Google Scholar 

  • Zuckerkandl, E., Pauling, L.: In: Evolving genes and proteins, V. Bryson, H. J. Vogel, Eds., p. 97. New York: Academic Press 1965

    Google Scholar 

  • Zuckerkandl, E., Schroeder, W. A.: Nature192, 984 (1961)

    Google Scholar 

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  1. John Barnabas

    Present address: Department of Biochemistry, Ahmednagar College, Ahmednagar, MS, India

Authors and Affiliations

  1. Department of Anatomy, Wayne State University, Medical Research Building 550 E Canfield Avenue, 48201, Detroit, Michigan, USA

    Morris Goodman, G. William Moore & John Barnabas

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

    Genji Matsuda

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Goodman, M., Moore, G.W., Barnabas, J. et al. The phylogeny of human globin genes investigated by the maximum parsimony method. J Mol Evol 3, 1–48 (1974). https://doi.org/10.1007/BF01795974

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