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On the molecular evolutionary clock

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Summary

The conceptual framework surrounding the origin of the molecular evolutionary clock and circumstances of this origin are described. In regard to the quest for the best available molecular clocks, a return to protein clocks is conditionally recommended. On the basis of recent data and certain considerations, it is pointed out that the realm of neutrality in evolution is probably less extensive than is now commonly thought, in the three distinct senses of the term neutrality—neutrality as nonfunctionality of mutations, neutrality as equifunctionality of mutations, and neutrality as a mode of fixation of mutations. The possibility is raised that complex sets of interacting components forming a system that is bounded with respect to its environment may quite generally display an intrinsic trend to a quasi-clockwise evolutionary behavior.

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References

  • Anfinsen CB (1959) The molecular basis of evolution. John Wiley & Sons, New York

    Google Scholar 

  • Avise JC (1974) Systematic value of electrophoretic data. Syst Zool 23:465–481

    Google Scholar 

  • Ayala FJ (1974) Biological evolution: natural selection or random walk? Am Sci 62:692–701

    PubMed  Google Scholar 

  • Ayala FJ (1986) On the virtues and Pitfalls of the molecular evolutionary clock. J Hered 77:226–235

    PubMed  Google Scholar 

  • Baldwin E (1964) An introduction to comparative biochemistry. Cambridge University Press, Cambridge, England

    Google Scholar 

  • Bernardi G, Bernardi G (1986) Compositional constraints and genome evolution. J Mol Evol 24:1–11

    PubMed  Google Scholar 

  • Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, Cuny G, Meunier-Rotival M, Rodier F (1985) The mosaic genome of warm-blooded vertebrates. Science 228:953–958

    PubMed  Google Scholar 

  • Boyden AA (1958) Comparative serology: aims, methods and results. In: Cole W (ed) Serological and biochemical comparisons of proteins. Rutgers University Press, New Brunswick NJ

    Google Scholar 

  • Britten RJ (1986) Rates of DNA sequence evolution differ between taxonomic groups. Science 231:1393–1398

    PubMed  Google Scholar 

  • Brown H, Sanger F, Kitai R (1955) The structure of pig and sheep insulins. Biochem J 60:556–565

    PubMed  Google Scholar 

  • Buonagurio DA, Nakada S, Parvin JD, Krystal M, Palese P, Fitch WM (1986) Evolution of human influenza A viruses over 50 years: a rapid uniform rate of change in NS gene. Science 232:980–982

    PubMed  Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1964) Analysis of human evolution. In: Genetics today, Proc XI int Congr Genetics. Pergamon, Oxford, England, pp 923–933

    Google Scholar 

  • Chang L-YE, Slightom J (1984) Isolation and nucleotide sequence analysis of the β-type globin pseudogene from human, gorilla and chimpanzee. J Mol Biol 180:767–784

    Article  PubMed  Google Scholar 

  • Cherry LM, Case SM, Wilson AC (1978) Frog perspective on the morphological difference between humans and chimpanzees. Science 200:209–211

    PubMed  Google Scholar 

  • Clarke AR, Wigley DB, Chia WN, Barstow D, Atkinson T, Holbrook JJ (1986) Site-directed mutagenesis reveals role of mobile arginine residue in lactate dehydrogenase catalysis. Nature 324:699–702

    Article  PubMed  Google Scholar 

  • Derancourt J, Lebor AS, Zuckerkandl E (1967) Séquence des acides aminés, séquence des nucléotides et évolution. Bull Soc Chim Biol 49:577–607

    PubMed  Google Scholar 

  • DiMichele L, Powers DA (1982) Physiological basis for swimming endurance differences between LDH-B genotypes ofFundulus heteroclitus. Science 216:1014–1016

    PubMed  Google Scholar 

  • DiMichele L, Powers DA, DiMichele JA (1986) Developmental and physiological consequences of genetic variation at enzyme synthesizing loci inFundulus heteroclitus. Am Zool 26:201–208

    Google Scholar 

  • Doolittle RF, Blomback B (1964) Amino-acid sequence investigations of fibrinopeptides from various mammals: evolutionary implications. Nature 202:147–152

    PubMed  Google Scholar 

  • Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and gene evolution. Nature 284:601–603

    Article  PubMed  Google Scholar 

  • Dover G (1982) Molecular drive: a cohesive mode of species evolution. Nature 299:111–117

    Article  PubMed  Google Scholar 

  • Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Zool 19:99

    PubMed  Google Scholar 

  • Fitch WM (1976) Molecular evolutionary clocks. In: Ayala FJ (ed) Molecular evolution. Sinauer Associates, Sunderland MA, pp 160–178

    Google Scholar 

  • Fitch WM, Atchley WR (1985a) Evolution in inbred strains of mice appears rapid. Science 228:1169–1175

    PubMed  Google Scholar 

  • Fitch WM, Atchley WR (1985b) Letter. Science 230:1408–1409

    Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284

    PubMed  Google Scholar 

  • Florkin M (1944) L'evolution biochemique. Masson, Paris

    Google Scholar 

  • Gasser SM, Laemmli UK (1986) Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes ofD. malanogaster. Cell 46:521–530

    Article  PubMed  Google Scholar 

  • Gillespie JH (1984) The molecular clock may be an episodic clock. Proc Natl Acad Sci USA 81:8009–8013

    PubMed  Google Scholar 

  • Gillespie JH (1986) Natural selection and the molecular clock. Mol Biol Evol 3:138–155

    PubMed  Google Scholar 

  • Gingerich PD (1983) Rates of evolution: effects of time and temporal scaling. Science 222:159–161

    Google Scholar 

  • Goodman M (1962) Evolution of the immunologic species specificity of human serum proteins. Human Biol 34:104–150

    PubMed  Google Scholar 

  • Goodman M (1963) Serological analysis of the systematics of recent hominoids. Human Biol 35:377–436

    PubMed  Google Scholar 

  • Goodman M, Braunitzer G, Stangl A, Schrank B (1983) Evidence on human origins from haemoglobins of African apes. Nature 303:546–548

    Article  PubMed  Google Scholar 

  • Gould SJ, Eldredge N (1977) Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology 3:115–151

    Google Scholar 

  • Hartl D, Dykhuizen D (1979) A selectively driven molecular clock. Nature 281:230–231

    Article  PubMed  Google Scholar 

  • Holmquist GP (1987) DNA sequences in G-bands and R-bands. In: Adolph KW (ed) Chromosome and chromatin structure. CRC Press, Boca Raton FL (in press)

    Google Scholar 

  • Imanaka T, Shibazaki M, Takagi M (1986) A new way of enhancing the thermostability of proteases. Nature 324:695–697

    Article  PubMed  Google Scholar 

  • Ingram VM (1961) Gene evolution and the haemoglobins. Nature 139:704–708

    Google Scholar 

  • Itano HA (1957) The human hemoglobins: their properties and genetic control. Adv Protein Chem 12:215–268

    Google Scholar 

  • Jukes TH (1963) Some recent advances in studies of the transcription of the genetic message. Adv Biol Med Phys 9:1–41

    Google Scholar 

  • Kettler MK, Ghent AW, Whitt GS (1986) A comparison of phylogenies based on structural and tissue-expressional differences of enzymes in a family of teleost fishes (Salmoniformes: Umbridae). Mol Biol Evol 3:485–498

    Google Scholar 

  • Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624–626

    PubMed  Google Scholar 

  • Kimura M (1969) The rate of molecular evolution considered from the standpoint of population genetics. Proc Natl Acad Sci USA 63:1181–1188

    PubMed  Google Scholar 

  • Kimura M (1979) The neutral theory of molecular evolution. Sci Am 241:94–104

    Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge, England

    Google Scholar 

  • Kimura M, Ohta T (1974) On some principles governing molecular evolution. Proc Natl Acad Sci USA 71:2848–2852

    PubMed  Google Scholar 

  • King JL, Jukes TH (1969) Non-Darwinian evolution. Science 164:788–798

    PubMed  Google Scholar 

  • King M-C, Wilson AC (1975) Evolution at two levels in humans and chimpanzees. Science 188:107–116

    PubMed  Google Scholar 

  • Koehn RK, Zera AJ, Hall JG (1983) Enzyme polymorphism and natural selection. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer Associates, Sunderland MA, pp 115–136

    Google Scholar 

  • Laird CD, McConaughy BL, McCarthy BJ (1969) Rate of fixation of nucleotide substitutions in evolution. Nature 224: 149–154

    PubMed  Google Scholar 

  • Li W-H, Wu C-I, Luo C-C (1985) A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2:150–174

    PubMed  Google Scholar 

  • Manuelidis L (1984) Different central nervous system cell types display distinct and nonrandom arrangements of satellite DNA sequences. Proc Natl Acad Sci UA 81:3123–3127

    Google Scholar 

  • Margoliash E (1963) Primary structure and evolution of cytochrome c. Proc Natl Acad Sci USA 50:672–679

    PubMed  Google Scholar 

  • Mas MT, Chen CY, Hitzeman RA (1986) Active human-yeast chimeric phosphoglycerate kinases engineered by domain interchange. Science 233:788–790

    PubMed  Google Scholar 

  • Mayr E (1982) The growth of biological thought; diversity, evolution, and inheritance. Harvard University Press, Cambridge MA

    Google Scholar 

  • Maxson LR, Wilson AC (1975) Albumin evolution and organismal evolution in tree frogs (Hylidae) Syst Zool 24:1–15

    Google Scholar 

  • Nevo E, Lavie B, Ben-Shlomo R (1983) Selection of allelic isozyme polymorphisms in marine organisms: pattern, theory, and application. In: Rattazzi MC, Scandalios JG, Whitt GS (eds) Isozymes, current topics in biological and medical research, vol 10. Genetics and evolution. Alan R Liss, New York, pp 69–92

    Google Scholar 

  • Nuttall GHF (1904) Blood immunity and blood relationship. Cambridge University Press, Cambridge, England

    Google Scholar 

  • Ohta T (1973) Slightly deleterious mutant substitutions in evolution. Nature 246:96–98

    Article  PubMed  Google Scholar 

  • Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607

    Article  PubMed  Google Scholar 

  • Parker HR, Philipp DP, Whitt GS (1985) Gene regulatory divergence among species estimated by altered developmental patterns in interspecific hybrids. Mol Biol Evol 2:217–250

    PubMed  Google Scholar 

  • Pauling L, Zuckerkandl E, (1963) Chemical paleogenetics: molecular “restoration studies” of extinct forms of life. Acta Chem Scand [B] 17:9–16

    Google Scholar 

  • Perler F, Efstratiadis A (1980) The evolution of genes: the chicken preproinsulin gene. Cell 20:555–566

    Article  PubMed  Google Scholar 

  • Perutz MF (1983) Species adaptation in a protein molecule. Mol Biol Evol 1:1–28

    PubMed  Google Scholar 

  • Perutz MF, Kendrew JC, Watson HC (1965) Structure and function of haemoglobin. II. Some relations between polypeptide chain configuration and amino acid sequence. J Mol Biol 13:669–678

    Google Scholar 

  • Petit C, Zuckerkandl E (1976) Evolution, genetique des populations, evolution moleculaire. Hermann, Paris

    Google Scholar 

  • Philipp DP, Childers WF, Whitt GS (1985) Correlations of allele frequences with physical and environmental variables for populations of largemouth bass,Micropterus salmoides (Lacepede). J Fish Biol 27:347–365

    Google Scholar 

  • Powers DA, DiMichele L, Place AR (1983) The use of enzyme kinetics to predict differences in cellular metabolism, developmental rate, and swimming performance between LDH-B genotypes of the fish,Fundulus heteroclitus. In: Rattazzi MC, Scandalios JG, Whitt GS (eds) Isozymes, current topics in biological and medical research, vol 10. Genetics and evolution. Alan R Liss, New York, pp 147–170

    Google Scholar 

  • Reichert ET, Brown AP (1909) The differentiations and specificity of corresponding proteins. In: Carnegie Inst Washington 116, 338 pp

  • Sarich VM, Wilson AC (1967a) Rates of albumin evolution in primates. Proc Natl Acad Sci USA 58:142–148

    PubMed  Google Scholar 

  • Sarich VM, Wilson AC (1967b) Immunological time scale for hominid evolution. Science 158:1200–1203

    PubMed  Google Scholar 

  • Sarich VM, Wilson AC (1973) Generation time and genomic evolution in primates. Science 179:1144–1147

    PubMed  Google Scholar 

  • Selander RK, Johnson WE (1973) Genetic variation among vertebrate species. Annu Rev Ecol Syst 4:75

    Article  Google Scholar 

  • Sibley CG, Ahlquist JE (1984) The phylogeny of the hominoid primates, as indicated by DNA-DNA hybridization. J Mol Evol 10:2–15

    Google Scholar 

  • Sibley CG, Ahlquist JE (1986) Reconstructing bird phylogeny by comparing DNA's. Sci Am 254:82–92

    Google Scholar 

  • Simpson GG (1953) The major features of evolution. Columbia University Press, New York

    Google Scholar 

  • Sneath PHA (1966) Relations between chemical structure and biological activity in peptides. J Theor Biol 12:157–195

    Article  PubMed  Google Scholar 

  • Sneath PHA (1980) The estimation of differences in protein evolution rates. Proc Geol Assoc 91:71–79

    Google Scholar 

  • Stenzel P (1974) Opossum Hb chain sequence and neutral mutation theory. Nature 252:62–63

    Article  PubMed  Google Scholar 

  • Strauss F, Varshavsky A (1984) A protein binds to a satellite DNA repeat at three specific sites that would be brought into mutual proximity by DNA folding in the nucleosome. Cell 37:889–901

    Article  PubMed  Google Scholar 

  • Swadesh M (1950) Salishan internal relationships. Int J Am Linguistics 16:157–167

    Article  Google Scholar 

  • Taylor WR (1986) The classification of amino acid conservation. J Theor Biol 119:205–218

    PubMed  Google Scholar 

  • Turner CG (1986) Dentochronological separation estimates for Pacific Rim populations. Science 232:1140–1142

    Google Scholar 

  • Vawter L, Brown WM (1986) Nuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science 234:194–196

    PubMed  Google Scholar 

  • Vogel H, Zuckerkandl E (1971a) Randomness and “thermodynamics” of molecular evolution. In: Schoffeniels E (ed) Biochemical evolution and the origin of life. North-Holland, Amsterdam, pp 352–365

    Google Scholar 

  • Vogel H, Zuckerkandl E (1971b) The evolution of polarity relations in globins. In: Neyman J (ed) Darwinian, Neo-Darwinian, and non-Darwinian evolution, Proc. 6th Berkeley Symp. Mathematical Statistics and Probability, vol 5. University of California Press, Berkeley, pp 155–176

    Google Scholar 

  • Walker R (1983) The molecular biology of enzyme synthesis; regulatory mechanisms of enzyme adaptation. John Wiley & Sons, New York

    Google Scholar 

  • Wallace DG, Maxson LR, Wilson AC (1971) Albumin evolution in frogs: a test of the clock hypothesis. Proc Natl Acad Sci USA 68:3127–3129

    PubMed  Google Scholar 

  • Wallace DG, King M-C, Wilson AC (1973) Albumin differences among ranid frogs: taxonomic and phylogenetic implications. Syst Zool 22:1–13

    Google Scholar 

  • Whitt GS (1983) Isozymes as probes and participants in developmental and evolutionary genetics. In: Rattazzi MC, Scandalios JG, Whitt GS (eds) Isozymes, current topics in biological and medical research, vol 10. Genetics and evolution. Alan R Liss, New York, pp 1–40

    Google Scholar 

  • Wilson AC (1975) Evolutionary importance of gene regulation. Stadler Symposium, University of Missouri 7:117–134

    Google Scholar 

  • Wilson AC, Maxson LR, Sarich VM (1974) Two types of molecular evolution. Evidence from studies of interspecific hybridization. Proc Natl Acad Sci USA 71:2843–2847

    PubMed  Google Scholar 

  • Wistow GJ, Mulders JWM, de Jong WW (1987) The enzyme lactate dehydrogenase as a structural protein in avian and crocodilian lenses. Nature 326:622–624

    Article  PubMed  Google Scholar 

  • Wu C-I, Li W-H (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745

    PubMed  Google Scholar 

  • Yokoyama S, Gojobori T (1987) Molecular evolution and phylogeny of the human AIDS viruses LAV, HTLV-III, and ARV. J Mol Evol 24:330–336

    PubMed  Google Scholar 

  • Zimmer EA, Martin SL, Beverly SM, Kan YW, Wilson AC (1980) Rapid duplication and loss of genes coding for the α-chains of hemoglobin. Proc Natl Acad Sci USA 77:2158–2162

    PubMed  Google Scholar 

  • Zuckerkandl E (1963) Perspectives in molecular anthropology. In: Washburn SL (ed) Classification and human evolution. Aldine, Chicago, pp 243–272

  • Zuckerkandl E (1964a) Controller-gene diseases: the operon model as applied to β-thalassemia, familial fetal hemoglobinemia and the normal switch from the production of fetal hemoglobin to that of adult hemoglobin. J Mol Biol 8:128–147

    Google Scholar 

  • Zuckerkandl E (1964b) Further principles of chemical paleogenetics as applied to the evolution of hemoglobin. In: Peeters H (ed) Protides of the biological fluids. Elsevier, Amsterdam, pp 102–109

    Google Scholar 

  • Zuckerkandl E (1965) The evolution of hemoglobin. Sci Am 212(5):110–118

    Google Scholar 

  • Zuckerkandl E (1968) Hemoglobins, Haeckel's “biogenetic law,” and molecular aspects of development. In: Rich A, Davidson N (eds) Structural chemistry and molecular biology: a volume dedicated to Linus Pauling by his students, colleagues, and friends. WH Freeman, San Francisco, pp 256–274

    Google Scholar 

  • Zuckerkandl E (1972) Some aspects of protein evolution. Biochimie 54:1095–1102

    PubMed  Google Scholar 

  • Zuckerkandl E (1975) The appearance of new structures and functions in proteins during evolution. J Mol Evol 7:1–57

    Article  PubMed  Google Scholar 

  • Zuckerkandl E (1976a) Evolutionary processes and evolutionary noise at the molecular level. I. Functional density in proteins. J Mol Evol 7:167–183

    Article  PubMed  Google Scholar 

  • Zuckerkandl E (1976b) Evolutionary processes and evolutionary noise at the molecular level. II. A selectionist model for random fixations in proteins. J Mol Evol 7:269–311

    Article  PubMed  Google Scholar 

  • Zuckerkandl E (1976c) Programs of gene action and progressive evolution. In: Goodman M, Tashian RE (eds) Molecular anthropology-genes and proteins in the evolutionary ascent of the primates. Plenum, New York, pp 387–447

    Google Scholar 

  • Zuckerkandl E (1978a) Multilocus enzymes, gene regulation, and genetic sufficiency. J Mol Evol 12:57–89

    Article  PubMed  Google Scholar 

  • Zuckerkandl E (1978b) Molecular evolution as a pathway to man. Z Morphol Anthropol 69:117–142

    PubMed  Google Scholar 

  • Zuckerkandl E (1983) Topological and quantitative relationships in evolving genomes. In: Helene C (ed) Structure, dynamics, interactions and evolution of biological macromolecules. Reidel, Dordrecht, pp 395–412

    Google Scholar 

  • Zuckerkandl E (1986) Polite DNA: functional density and functional compatibility in genomes. J Mol Evol 24:12–27

    PubMed  Google Scholar 

  • Zuckerkandl E, Pauling L (1962) Molecular disease, evolution, and genic heterogeneity. In: Kasha M, Pullman B (eds) Horizons in biochemistry. Academic Press, New York, p 189

    Google Scholar 

  • Zuckerkandl E, Pauling L (1964) Molecules as documents of evolutionary history. In: Problems of evolutionary and technical biochemistry. Science Press, Academy of Sciences of the USSR, pp 54–62 (in Russian); republished in English (1965a), J Theor Biol 8:357–366

  • Zuckerkandl E, Pauling L (1965b) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–165

    Google Scholar 

  • Zuckerkandl E, Schroeder WA (1961) Amino acid composition of the polypeptide chains of gorilla haemoglobin. Nature 192: 984–985

    Google Scholar 

  • Zuckerkandl E, Jones RT, Pauling L (1960) A comparison of animal hemoglobins by tryptic peptide pattern analysis. Proc Natl Acad Sci USA 46:1349–1360

    Google Scholar 

  • Zuckerkandl E, Derancourt J, Vogel H (1971) Mutational trends and random processes in the evolution of informational macromolecules. J Mol Biol 59:473–490

    Article  PubMed  Google Scholar 

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  1. Linus Pauling Institute of Science and Medicine, 440 Page Mill Road, 94306, Palo Alto, California, USA

    Emile Zuckerkandl

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Zuckerkandl, E. On the molecular evolutionary clock. J Mol Evol 26, 34–46 (1987). https://doi.org/10.1007/BF02111280

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