Abstract
Kimura mistook ambiguous maximum parsimony codons for wrong codons. The maximum parsimony method performed well as judged by the two classes of serine codons (which can not be connected by silent mutations) on comparing the parsimony codons for serines in human, rabbit, and mouseα hemoglobin chains to actual codons determined by nucleotide sequencing. In genealogical reconstructions involving 247 eucaryotic globins, the maximum parsimony distances separating the contemporary sequences show that Kimura's Poisson and Dayhoff's PAM estimates of rate of globin evolution miss most of the superimposed replacements and are therefore seriously in error. Nor is Kimura's constant rate assumption and his belief in a single origin of myoglobin supported. Lamprey myoglobin appears to be most like lamprey hemoglobin, while gnathostome myoglobin seems closest to gnathostome hemoglobin. It was found that the three types of gnathostome globins (Mb,α Hb,β Hb) evolved between the shark-boney vertebrate and bird-mammal ancestors at a much faster rate than from the latter ancestor to the present. The data indicate that rates were exceedingly fast during the origin of these globin chains because a high proportion of substitutions were adaptive. It was concluded that wherever strong stabilizing selection acts on a protein, somewhere in the past positive Darwinian selection must have spread the amino acid substitutions now being preserved.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Baba ML, Darga LL, Goodman M, Czelusniak J (1980) Evolution of cytochromec investigated by the maximum parsimony method. J Mol Evol (In press)
Braunitzer G, Fujuki H (1969) Zur evolution der vertebraten die konstitution und tertiärstruktur des hämoglobins des flußneunauges. Naturwissenschaften 56:322:323
Czelusniak J, Goodman M, Moore GW (1978) On investigating the statistical properties of the populous path algorithm by computer simulation. J Mol Evol 11:75–85
Dayhoff MO (1972) Atlas of protein sequence and structure, vol 5. National Biomedical Research Foundation, Washington, DC
Dayhoff MO (1978) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation, Washington, DC
Dickerson RE (1971) The structure of cytochromec and the rates of molecular evolution. J Mol Evol 1:26–45
Fisher WK, Nash AR, Thompson EOP (1977) Haemoglobins of the shark,Heterodontus portusjacksoni. III. Amino acid sequence of theβ chain. Aust J Biol Sci 30:487–506
Fisher WK, Thompson EOP (1979) Myoglobin of the sharkHeterodontus portusjacksoni: isolation and amino acid sequence. Aust J Biol Sci 32:277–294
Goodman M (1981) Decoding the pattern of protein evolution. Prog Biophys Mol Biol (in press)
Goodman M, Czelusniak J (1980) Mode, tempo, and role of natural selection in the evolution of heme proteins. Protides of the Biological Fluids 28:57–60
Goodman M, Moore GW, Barnabas J, Matsuda G (1974) The phylogeny of human globin genes investigated by the maximum parsimony method. J Mol Evol 3:1–48
Goodman M, Moore GW (1975) Darwinian evolution in the genealogy of haemoglobin. Nature 253:603–608
Goodman M, Czelusniak J, Moore GW, Matsuda G (1979a) Fitting the gene lineage into its species lineage: A parsimony strategy illustrated by cladograms constructed from globin sequences. Syst Zool 28:132–163
Goodman M, Pechére JF, Haiech J, Demaille JG (1979b) Evolutionary diversification of structure and function in the family of intracellular calcium-binding proteins. J Mol Evol 13:331–352
Heindell HC, Liu A, Paddock GV, Studnicka GM, Salser WA (1978) The primary sequence of rabbitα-globin in RNA. Cell 15:43–54
Holmquist R (1979) The method of parsimony: an experimental test and theoretical analysis of the adequacy of molecular restoration studies. J Mol Biol 135:939–958
Kimura M (1969) The rate of molecular evolution considered from the standpoint of population genetics. Proc Natl Acad Sci USA 63:1181–1188
Kimura M (1979) The neutral theory of molecular evolution. Sci Am 241 (No. 5, Nov.):94–104
Kimura M (1981) Was globin evolution very rapid in its early stages?: A dubious case against the rate-constancy hypothesis. J Mol Evol 17:110–113
Li SL, Riggs A (1970) The amino acid sequence of hemoglobin V from the lampreyPetromyzon marinus. J Biol Chem 245:6149–6169
Liljeqvist G, Braunitzer G, Paléus S (1979) Hämoglobine, XXVII Die sequence der monomeren hämoglobine III vonMyxine glutinosa L: ein neurer hämkomplex: E7 glutamin, Ell isoleucin. Hoppe-Seyler's Z Physiol Chem 360:125–135
Moore GW (1977) Proof of the populous path algorithm for missing mutations in parsimony trees. J Theor Biol 66:95–106
Moore GW, Barnabas J, Goodman M (1973) A method for constructing maximum parsimony ancestral amino acid sequences on a given network. J Theor Biol 38:459–485
Nash AR, Fisher WK, Thompson EOP (1976) Haemoglobins of the shark,Heterodontus portusjacksoni. II. Amino acid sequence of theα-chain. Aust J Biol Sci 29:73–97
Nishioka Y, Leder P (1979) The complete sequence of a chromosomal mouseα-globin gene reveals elements conserved throughout vertebrate evolution. Cell 18:875–882
Romero-Herrera AE, Lieska N, Nasser S (1979) Characterization of the myoglobin ofPetromyzon marinus. 14:259–266
Von Ehrenstein G (1966) Translational variations in the amino acid sequence of theα-chain of rabbit hemoglobin. Cold Spring Harbour Symp Quant Biol 31:705–714
Wilson JT, Wilson LB, Reddy VB, Cavallesco C, Ghosh PK, de Riel JK, Forget BG, Weissman SM (1980) Nucleotide sequence of the coding portion of humanα globin messenger RNA. J Biol Chem 255:2807–2815
Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, p 97
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Goodman, M. Globin evolution was apparently very rapid in early vertebrates: A reasonable case against the rate-constancy hypothesis. J Mol Evol 17, 114–120 (1981). https://doi.org/10.1007/BF01732683
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF01732683