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Molecular evidence from the nuclear genome for the time frame of human evolution

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Abstract

Evolutionary divergence times can be inferred from molecular distances if a molecular clock can be assumed and if the substitution rate can be estimated. We present new evidence from relative rate tests that the rate of substitution at fourfold degenerate sites of nuclear genome-coding DNA is uniform in primate and rodent lineages. We also review recent relative rate test results showing substitution rate uniformity in the nuclear genome of simian primates. DNA distances between a range of mammalian taxa shows that a molecular clock is inconsistent with many assumed divergence times irrespective of the assumed substitution rate. We find that the substitution rate that implies the best compromise fit with divergence times across the range of taxa is 2.0–2.25 × 10-9. This range of substitution rates implies a divergence time of humans and chimpanzees of 4.0-3.6 million years ago. This postdates the occurrence of Ardipithecus ramidus and the earliest occurrence of Australopithecus 0afarensis, suggesting that the common ancestor of humans and chimpanzees was bipedal and that the trait has been lost in chimpanzees rather than gained in humans.

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References

  • Adachi J, Hasegawa M (1995) Improved dating of the human/ chimpanzee separation in the mitochondrial DNA tree: heterogeneity among amino acid sites. J Mol Evol 40:622–628

    Article  PubMed  CAS  Google Scholar 

  • Alpagut B, Andrews P, Fortelius M, Kappelman J, Temizsoy I, Celebi H, Lindsay W (1996) A new specimen of Ankarapithecus meteai from the Sinap Formation of central Anatolia. Nature 382:349–351

    Article  PubMed  CAS  Google Scholar 

  • Ashley MV (1996) Book review: the mammalian molecular clock. J Mammal 77:286–288

    Article  Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolution. Chapman & Hall, New York

    Google Scholar 

  • Benveniste RE (1985) The contributions of retroviruses to the study of mammalian evolution. In: Mclntyre R (ed) Molecular evolutionary genetics. Plenum Press, New York, pp 359–417

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Brownell E (1983) DNA/DNA hybridization studies of muroid rodents: symmetry and rates of molecular evolution. Evolution 37:1034–1051

    Article  CAS  Google Scholar 

  • Bulmer M, Wolfe KH, Sharp PM (1991) Synonymous nucleotide substitution rates in mammalian genes: implications for the molecular clock and the relationship of mammalian orders. Proc Natl Acad Sci USA 88:5974–5978

    Article  PubMed  CAS  Google Scholar 

  • Caccone A, Powell JR (1989) DNA divergence among hominoids. Evolution 43:925–942

    Article  Google Scholar 

  • Catzeflis F, Sheldon FH, Ahlquist JE, Sibley CG (1987) DNA-DNA hybridization evidence of the rapid rate of muroid rodent DNA evolution. Mol Biol Evol 4:242–253

    PubMed  CAS  Google Scholar 

  • Chang HH-J, Shimmin LC, Shyue S, Hewett-Emmett D, Li W-H (1994) Weak male-driven molecular evolution in rodents. Proc Natl Acad Sei USA 91:827–831

    Article  CAS  Google Scholar 

  • Coulondre C, Miller JH, Farabaugh PJ, Gilbert W (1978) Molecular basis of base substitution hotspots in Escherichia coli. Nature 274: 775–780

    Article  PubMed  CAS  Google Scholar 

  • Dene HT, Goodman M, Prychodko W (1975) Immunodiffusion evidence of the phylogeny of the primates. In: Goodman M, Tashian RE (eds) Molecular anthropology. Plenum Press, New York, pp 171–195

    Google Scholar 

  • Dickerson RE (1971) The structure of cytochrome c and the rates of molecular evolution. J Mol Evol 1:26–45

    Article  PubMed  CAS  Google Scholar 

  • Driscoll DJ, Migeon BR (1990) Sex differences in methylation of single-copy genes in human meiotic germ cells: implications for X-chromosome inactivation, parental imprinting, and origin of CpG mutations. Somat Cell Mol Genet 16:267–282

    Article  PubMed  CAS  Google Scholar 

  • Easteal S (1988) Rate constancy of globin gene evolution in placental mammals. Proc Natl Acad Sci USA 85:7622–7626

    Article  PubMed  CAS  Google Scholar 

  • Easteal S (1990) The pattern of mammalian evolution and the relative rate of molecular evolution. Genetics 124:165–173

    PubMed  CAS  Google Scholar 

  • Easteal S, Collet C (1994) Consistent variation in amino-acid substitution rate, despite uniformity of mutation rate: protein evolution in mammals is not neutral. Mol Biol Evol 11:643–647

    PubMed  CAS  Google Scholar 

  • Easteal S, Collet CC, Betty DJ (1995) The mammalian molecular clock. Springer-Verlag, Austin, TX

    Google Scholar 

  • Ellsworth DL, Hewett-Emmett D, Li W-H (1993) Insulin-like growth factor II intron sequences support the Hominoid rate-slowdown hypothesis. Mol Phyl Evol 2:315–321

    Article  CAS  Google Scholar 

  • Francino MF, Chao L, Riley MA, Ochman H (1996) Asymmetries generated by transcription-coupled repair in enterobacterial genes. Science 272:107–109

    Article  PubMed  CAS  Google Scholar 

  • Gingerich PD (1996) Temporal scaling of molecular evolution in primates and other mammals. Mol Biol Evol 3:205–221

    Google Scholar 

  • Goodman M (1963) Serological analysis of the systematics of recent hominoids. Hum Biol 35:377–4136

    PubMed  CAS  Google Scholar 

  • Goodman M (1985) Rates of molecular evolution: the hominoid slowdown. BioEssays 3:9–14

    Article  PubMed  CAS  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  CAS  Google Scholar 

  • Goodman M, Bailey WJ, Hayasaka K, Stanhope MJ, Slightom J, Czelusniak J (1994) Molecular evidence on primate phylogeny from DNA sequences. Am J Phys Anthropol 94:3–24

    Article  PubMed  CAS  Google Scholar 

  • Graur D, Duret L, Gouy M (1996) Phylogenetic position of the order Lagomorpha (rabbits, hares and allies). Nature 379:333–335

    Article  PubMed  CAS  Google Scholar 

  • Groves CP (1989) A theory of human and primate evolution. Oxford University Press, Oxford

    Google Scholar 

  • Gu X, Li W-H (1992) Higher rates of amino acid substitution in rodents than in humans. Mol Phyl Evol 1:211–214

    Article  CAS  Google Scholar 

  • Hammer MF (1995) A recent common ancestry for human Y chromosomes. Nature 378:376–378

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa M (1990) Phylogeny and molecular evolution in primates. Jap J Genet 65:243–265

    Article  CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1989) Estimation of branching dates among primates by molecular clocks of nuclear DNA which slowed down in Hominoidea. J Hum Evol 18:461–476

    Article  Google Scholar 

  • Hedges SB, Parker PH, Sibley CG, Kumar S (1996) Continental breakup and the ordinal diversification of birds and mammals. Nature 381:226–229

    Article  PubMed  CAS  Google Scholar 

  • Herbert G, Easteal S (1996) Relative rates of nuclear DNA evolution in human and Old World monkey lineages. Mol Biol Evol 13:1054–1057

    PubMed  CAS  Google Scholar 

  • Higgins DG, Bleasby AJ, Fuchs R (1992) CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci 7:189–191

    Google Scholar 

  • Horai S, Satta Y, Hayasaka K, Kondo R, Inoue T, Ishida T, Hayashi S, Takahata N (1992) Man’s place in Hominoidea revealed by mitochondrial DNA geneology. J Mol Evol 35: 32–43; Erratum 37: 89 (1993)

    Article  PubMed  CAS  Google Scholar 

  • Horai S, Hayasaka K, Tsugane K, Takahata N (1995) Recent African origin of modern humans revealed by complete sequences of hominoid mitochondrial DNAs. Proc Natl Acad Sci USA 92:532–536

    Article  PubMed  CAS  Google Scholar 

  • Ina Y (1996) Pattern of synonymous and nonsynonymous substitutions: an indicator of mechanisms of molecular evolution. J Genet (in press)

  • Kawamura S, Tanabe H, Watanabe Y, Kurosaki K, Saitou N, Ueda S (1991) Evolutionary rate of immunoglobulin alpha noncoding region is greater in hominoids than in Old World monkeys. Mol Biol Evol 8:743–752

    PubMed  CAS  Google Scholar 

  • Kelley JK, Pilbeam D (1986) The dryopithecines: taxonomy, comparative anatomy, and phylogeny of Miocene large hominoids. In: Swindler DR, Erwin J (eds) Comparative primate biology, vol. 1. Alan R Liss, New York, pp 361–411

    Google Scholar 

  • Ketterling RP, Vielhaber E, Bottema CDK, Schaid DJ, Cohen MP, Sexauer CL, Sommer SS (1993) Germ-line origins of mutation in families with hemophilia B: the sex ratio varies with the type of mutation. Am J Hum Genet 52:152–166

    PubMed  CAS  Google Scholar 

  • Kimbel WH, Johanson DC, Rak Y (1994) The first skull and other new discoveries of Australopithecus afarensis at Hadar, Ethiopia. Nature 368:449–451

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Ohta M (1971) Protein polymorphism as a phase of molecular evolution. Nature 229:467–469

    Article  PubMed  CAS  Google Scholar 

  • Kishino H, Hasegawa M (1990) Converting distance to time: an application to human evolution. Methods Enzymol 183:550–570

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lee AT, DeSimone C, Cerami A, Bucala R (1994) Comparative analysis of DNA mutations in lad transgenic mice with age. FASEB J 8:545–550

    PubMed  CAS  Google Scholar 

  • Li H-H, Ellsworth DL, Krushkal J, Chang BH-J, Hewett-Emmett D (1996) Rates of nucleotide substitution in primates and rodents and the generation-time effect hypothesis. Mol Phyl Evol 5:182–187

    Article  CAS  Google Scholar 

  • Li W-H (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36:96–99

    Article  PubMed  CAS  Google Scholar 

  • Li W-H, Tanimura M (1987) The molecular clock runs more slowly in man than in apes and monkeys. Nature 326:93–96

    Article  PubMed  CAS  Google Scholar 

  • Li W-H, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol 25:330–342

    Article  PubMed  CAS  Google Scholar 

  • Li W-H, Gouy M, Sharp PM, O’hUigin C, Yang Y-W (1990) Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora and molecular clocks. Proc Natl Acad Sci USA 87:6703–6707

    Article  PubMed  CAS  Google Scholar 

  • Marks J, Schmid CW, Sarich VM (1988) DNA hybridization as a guide to phylogeny: relations of the hominoidea. J Hum Evol 17:769–786

    Article  Google Scholar 

  • Miyata T, Hayashida H, Kuma K, Mitsuyasu K, Yasunga T (1987) Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb Symp Quant Biol 52:863–867

    PubMed  CAS  Google Scholar 

  • Norrell MA, Novacek MJ (1992) Congruence between superpositional and phylogenetic patterns: comparing cladistic patterns with fossil records. Cladistics 8:319–337

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ohta T (1995) Synonymous and nonsynonymous substitutions in mammalian genes and the nearly neutral theory. J Mol Evol 40:56–63

    Article  PubMed  CAS  Google Scholar 

  • O’hUigin C, Li W-H (1992) The molecular clock ticks regularly in muroid rodents and hamsters. J Mol Evol 35:377–384

    PubMed  Google Scholar 

  • Pilbeam D (1996) Genetic and morphological records of the Hominidae and hominid origins: a synthesis. Mol Phyl Evol 5:155–168

    Article  CAS  Google Scholar 

  • Pilbeam D, Walker A (1968) Fossil monkeys from the Miocene of Napak, North-East Uganda. Nature 220:657–660

    Article  PubMed  CAS  Google Scholar 

  • Sarich VM, Wilson AC (1966) Quantitative immunochemistry and the evolution of primate albumins: micro-complement fixation. Science 154:1563–1566

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sarich VM, Schmid CW, Marks J (1989) DNA hybridization as a guide to phylogenics: a critical analysis. Cladistics 5:3–32

    Article  Google Scholar 

  • Shimmin LC, Chang BH-J, Li W-H (1993) Male-driven evolution of DNA sequences. Nature 362:745–747

    Article  PubMed  CAS  Google Scholar 

  • Sibley CG, Ahlquist JE (1984) The phylogeny of the hominoid primates, as indicated by DNA-DNA hybridization. J Mol Evol 20:2–15

    Article  PubMed  CAS  Google Scholar 

  • Sibley CG, Alquist JE (1987) DNA hybridization evidence of hominoid phylogeny: results of an expanded data set. J Mol Evol 26:99–121

    Article  PubMed  CAS  Google Scholar 

  • Siegel S (1956) Nonparametric statistics for the behavioural sciences. McGraw-Hill, Tokyo

    Google Scholar 

  • Simons EL (1972) Primate evolution. Macmillan, New York

    Google Scholar 

  • Smith SW, Overbeek R, Woese CR, Gilbert W, Gillevet PM (1994) The genetic data environment an expandable GUI for multiple sequence analysis. Comput Appl Biosci 10:671–675

    PubMed  CAS  Google Scholar 

  • Tishkoff SA, Dietzsch E, Speed W, Pakstis AJ, Kidd JR et al. (1996) Global patterns of linkage disequilibrium at the CD4 locus and modern human origins. Science 271:1380–1387

    Article  PubMed  CAS  Google Scholar 

  • Vigilant L, Stoneking M, Harpending H, Hawkes K, Wilson AC (1991) African populations and the evolution of human mitochondrial DNA. Science 253:1503–1507

    Article  PubMed  CAS  Google Scholar 

  • White TD, Suwa G, Asfaw B (1994) Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia. Nature 371:280–281

    Article  Google Scholar 

  • White TD, Suwa G, Asfaw B (1995) Australopithecus ramidus, a new species of early hominid from Aramis, Ethiopia (Corrigendum). Nature 375:88

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

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  1. Human Genetics Group, John Curtin School of Medical Research, The Australian National University, ACT0200, Canberra, Australia

    Simon Easteal & Genevierve Herbert

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  1. Simon Easteal
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  2. Genevierve Herbert
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Easteal, S., Herbert, G. Molecular evidence from the nuclear genome for the time frame of human evolution. J Mol Evol 44 (Suppl 1), S121–S132 (1997). https://doi.org/10.1007/PL00000066

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