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Journal of Molecular Evolution

, Volume 3, Issue 4, pp 243–262 | Cite as

Slow evolution of transferrin and albumin in birds according to micro-complement fixation analysis

  • Ellen M. Prager
  • Alan H. Brush
  • Richard A. Nolan
  • Mikiye Nakanishi
  • Allan C. Wilson
Article

Summary

Rabbit antisera were prepared to purified ovotransferrin from chicken (order Galliformes) and red-winged blackbird (order Passeriformes) and to purified serum albumin from chicken and rhea (order Rheiformes). Quantitative microcomplement fixation was used to compare these proteins immunologically with those of representatives of all 27 orders of birds. The average interordinal immunological distances were 123 units for transferrin and 53 units for albumin.

Extensive intraordinal comparisons of transferrin among 51 species within the order Galliformes and 33 species within the order Passeriformes were also carried out. Values ranging from 0–75 immunological distance units were found within each order.

Rabbit antisera to purified alligator albumin were also prepared and shown to react with representatives of all 27 orders of birds, the average immunological distance being 166 units.

When the data presented here are considered in relation to the fossil record of birds, it appears that transferrin and albumin have evolved more slowly in birds than in other vertebrates. If prevailing interpretations of the fossil record are correct, transferrin has evolved 2–4 times as fast in mammals and snakes as in birds, while serum albumin has evolved about 3 times as fast in mammals, iguanids, crocodilians, and frogs as in birds. Published immunological and sequence comparisons of lysozyme and cytochromec are also consistent with a slower rate of evolution in birds than in other vertebrates. The implications of a general slowdown in the evolution of bird proteins are discussed.

Key words

Transferrin Albumin Micro-Complement Fixation Protein Evolution Evolutionary Rates Birds Crocodilians 

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References

  1. Abrahamson, S., Bender, M. A., Conger, A. D., Wolff, S.: Nature245, 460 (1973)Google Scholar
  2. Aisen, P., Leibman, A., Pinkowitz, R. A., Pollack, S.: Biochemistry12, 3679 (1973)Google Scholar
  3. Arnheim, N., Jr., Wilson, A. C.: J. Biol. Chem.242, 3951 (1967)Google Scholar
  4. Augusteyn, R. C.: Biochim. Biophys. Acta303, 1 (1973)Google Scholar
  5. Azari, P. R., Feeney, R. E.: J. Biol. Chem.232, 293 (1958)Google Scholar
  6. Bates, G. W., Billups, C., Saltman, P.: J. Biol. Chem.242, 2810 (1967)Google Scholar
  7. Brodkorb, P.: Bull. Fla. State Mus. Biol. Ser.8, 195 (1964)Google Scholar
  8. Brodkorb, P.: In: Avian biology, Vol.1. D. S. Farner, J. R. King, Eds., p. 19. New York: Academic Press 1971Google Scholar
  9. Brush, A. H.: Occ. Pap. U. Conn. Zool.1, 243 (1970)Google Scholar
  10. Champion, A. B., Prager, E. M., Wachter, D., Wilson, A. C.: In: Biochemical and immunological taxonomy of animals. C. A. Wright, Ed., p. 397. London Academic Press 1974Google Scholar
  11. Clark, J. R., Osuga, D. T., Feeney, R. E.: J. Biol. Chem.238, 3621 (1963)Google Scholar
  12. Cracraft, J.: J. Zool. (Lond.)169, 455 (1973)Google Scholar
  13. Dayhoff, M. O. (Ed.): Atlas of protein sequence and structure, Vol. 5. Washington, D. C.: National Biomedical Research Foundation, Georgetown University Medical Center 1972Google Scholar
  14. Dickerson, R. E.: J. Mol. Evol.1, 26 (1971)Google Scholar
  15. Feeney, R. E., Allison, R. G.: Evolutionary biochemistry of proteins. New York: Wiley 1969Google Scholar
  16. Feeney, R. E., Anderson, J. S., Azari, P. R., Bennett, N., Rhodes, M. B.: J. Biol. Chem.235, 2307 (1960)Google Scholar
  17. Feeney, R. E., Komatsu, S. K.: In: Structure and bonding, Vol.1, C. K. Jørgensen, J. B. Neilands, R. S. Nyholm, D. Reinen, R. J. P. Williams, Eds., p. 149. Berlin: Springer 1966Google Scholar
  18. Fisher, J. M. M.: In: The fossil record, W. B. Harland, C. H. Holland, M. R. House, N. F. Hughes, A. B. Reynolds, M. J. S. Rudwick, G. E. Satterthwaite, L. B. H. Tarlo, E. C. Willey, Eds., pp. 133 and 733. London: Geological Society of London 1967Google Scholar
  19. Gorman, G. C., Wilson, A. C., Nakanishi, M.: Syst. Zool.20, 167 (1971)Google Scholar
  20. Hanke, N., Prager, E. M., Wilson, A. C.: J. Biol. Chem.248, 2824 (1973)Google Scholar
  21. Hermann, J., Jollès, J., Buss, D. H., Jollès, P.: J. Mol. Biol.79, 587 (1973)Google Scholar
  22. Kohne, D. E.: Quart. Rev. Biophys.3, 327 (1970)Google Scholar
  23. Lillegraven, J. A.: Univ. of Kansas Paleontological Contributions, No. 50 (1969)Google Scholar
  24. Mao, S.-H., Dessauer, H. C.: Comp. Biochem. Physiol.40A, 669 (1971)Google Scholar
  25. Markussen, J., Sundby, F.: Internat. J. Peptide Prot. Chem.5, 37 (1973)Google Scholar
  26. Matsuda, G., Maita, T., Mizuno, K., Ota, H.: Nature New Biology244, 244 (1973)Google Scholar
  27. Miller, H. T., Feeney, R. E.: Arch. Biochem. Biophys.108, 117 (1964)Google Scholar
  28. Nakanishi, M.: Master's Thesis, University of California, Berkeley (1971)Google Scholar
  29. Nolan, C., Margoliash, E.: Ann. Rev. Biochem.37, 727 (1968)Google Scholar
  30. Nolan, R. A., Brush, A. H., Arnheim, N., Wilson, A. C.: Condor76 (in press, 1974)Google Scholar
  31. Ostrom, J. H.: Nature242, 136 (1973)Google Scholar
  32. Osuga, D. T., Feeney, R. E.: Arch. Biochem. Biophys.124, 560 (1968)Google Scholar
  33. Prager, E. M., Arnheim, N., Mross, G. A., Wilson, A. C.: J. Biol. Chem.247, 2905 (1972)Google Scholar
  34. Prager, E. M., Wilson, A. C.: J. Biol. Chem.246, 5978 (1971a)Google Scholar
  35. Prager, E. M., Wilson, A. C.: J. Biol. Chem.246, 7010 (1971b)Google Scholar
  36. Romer, A. S.: Vertebrate paleontology, 3rd edition. Chicago: University of Chicago Press 1966Google Scholar
  37. Salthe, S. N., Kaplan, N. O.: Evol.20, 603 (1966)Google Scholar
  38. Sarich, V. M.: Syst. Zool.18, 286 (1969)Google Scholar
  39. Sarich, V. M.: In: Old world monkeys: evolution, systematics, and behavior, J. R. Napier, P. H. Napier, Eds., p. 175. New York: Academic Press 1970Google Scholar
  40. Sarich, V. M.: Biochem. Genet.7, 253 (1972)Google Scholar
  41. Sarich, V. M.: Nature245, 218 (1973)Google Scholar
  42. Sarich, V. M., Wilson, A. C.: Sci.154, 1563 (1966)Google Scholar
  43. Sarich, V. M., Wilson, A. C.: Proc. Nat. Acad. Sci. USA58, 142 (1967a)Google Scholar
  44. Sarich, V. M., Wilson, A. C.: Sci.158, 1200 (1967b)Google Scholar
  45. Sarich, V. M., Wilson, A. C.: Sci.179, 1144 (1973)Google Scholar
  46. Sill, W. D.: Copeia1968, 76 (1968)Google Scholar
  47. Simons, E. L.: Primate evolution: an introduction to man's place in nature. New York: Macmillan 1972Google Scholar
  48. Sparrow, A. H., Price, H. J., Underbrink, A. G.: In: Evolution of genetic systems, H. H. Smith, Ed., p. 451. New York: Gordon and Breach 1972Google Scholar
  49. Sundby, F., Frandsen, E. K., Thomsen, J., Kristiansen, K., Brunfeldt, K.: FEBS Letters26, 289 (1972)Google Scholar
  50. Walker, A. D.: Nature237, 257 (1972)Google Scholar
  51. Wallace, D. G., King, M.-C., Wilson, A. C.: Syst. Zool.22, 1 (1973)Google Scholar
  52. Wallace, D. G., Maxson, L. R., Wilson, A. C.: Proc. Nat. Acad. Sci. USA68, 3127 (1971)Google Scholar
  53. Wallace, D. G., Wilson, A. C.: J. Mol. Evol.2, 72 (1972)Google Scholar
  54. Wetter, L. R., Cohn, M., Deutsch, H. F.: J. Immunol.70, 507 (1953)Google Scholar
  55. Williams, J.: Biochem. J.83, 355 (1962)Google Scholar
  56. Williams, J.: Biochem. J.108, 57 (1968)Google Scholar
  57. Wilson, A. C., Kaplan, N. O.: In: Taxonomic biochemistry and serology, C. A. Leone, Ed., p. 321. New York: Ronald Press 1964Google Scholar
  58. Wilson, A. C., Kaplan, N. O., Levine, L., Pesce, A., Reichlin, M., Allison, W. S.: Fed. Proc.23, 1258 (1964)Google Scholar
  59. Wilson, A. C., Prager, E. M.: In: Lysozyme, E. F. Osserman, R. E. Canfield, S. Beychok, Eds., p.127. New York: Academic Press 1974Google Scholar

Copyright information

© Springer-Verlag 1974

Authors and Affiliations

  • Ellen M. Prager
    • 1
  • Alan H. Brush
    • 1
  • Richard A. Nolan
    • 1
  • Mikiye Nakanishi
    • 1
  • Allan C. Wilson
    • 1
  1. 1.Department of BiochemistryUniversity of CaliforniaBerkeleyUSA

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