Skip to main content
SpringerLink
Log in

Improved dating of the human/chimpanzee separation in the mitochondrial DNA tree: Heterogeneity among amino acid sites

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The internal branch lengths estimated by distance methods such as neighbor joining are shown to be biased to be short when the evolutionary rate differs among sites. The variable-invariable model for site heterogeneity fits the amino acid sequence data encoded by the mitochondrial DNA from Hominoidea remarkably well. By assuming the orangutan separation to be 13 or 16 Myr old, a maximum-likelihood analysis estimates a young date of 3.6 ± 0.6 or 4.4 ± 0.7 Myr (±1 SE) for the human/chimpanzee separation, and these estimates turn out to be robust against differences in the assumed model for amino acid substitutions. Although some uncertainties still exist in our estimates, this analysis suggests that humans separated from chimpanzees some 4–5 Myr ago.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adachi J, Hasegawa M (1992) Computer science monographs, No. 27. MOLPHY: programs for molecular phylogenetics, I.—PROTML: maximum likelihood inference of protein phylogeny. Institute of Statistical Mathematics, Tokyo

    Google Scholar 

  • Adachi J, Cao Y, Hasegawa M (1993) Tempo and mode of mitochondrial DNA evolution in vertebrates at the amino acid sequence level: rapid evolution in warm-blooded vertebrates. J Mol Evol 36:270–281

    Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Contr AC-19:716–723

    Google Scholar 

  • Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith ALH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–464

    Google Scholar 

  • Andrews P, Cronin JE (1982) The relationships of Sivapithecus and Ramapithecus and the evolution of the orang-utan. Nature 297:541–546

    Google Scholar 

  • Andrews P (1992) Evolution and environment in the Hominoidea. Nature 360:641–646

    Google Scholar 

  • Bailey WJ, Hayasaka K, Skinner CG, Kehoe S, Sieu LC, Slightom JL, Goodman M (1992) Reexamination of the African hominoid trichotomy with additional sequences from the primate β-globin gene cluster. Mol Phyl Evol 1:97–135

    Google Scholar 

  • Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239

    Google Scholar 

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

    Google Scholar 

  • Cann RL, Stoneking M, Wilson AC (1987) Mitochondrial DNA and human evolution. Nature 325:31–36

    Google Scholar 

  • Cao Y, Adachi J, Yano T, Hasegawa M (1994a) Phylogenetic place of guinea pigs: no support of the rodent polyphyly hypothesis from maximum likelihood analyses of multiple protein sequences. Mol Biol Evol 11:593–604

    Google Scholar 

  • Cao Y, Adachi J, Janke A, Pääbo S, Hasegawa M (1994b) Phylogenetic relationships among eutherian orders estimated from inferred sequences of mitochondrial proteins: instability of a tree based on a single gene. J Mol Evol 39:519–527

    Google Scholar 

  • Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in proteins. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation, Washington DC, pp 345–352

    Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Fitch WM, Markowitz E (1970) An improved method for determining codon variability in a gene and its application to the rate of fixations of mutations in evolution. Biochem Genet 4:579–593

    Google Scholar 

  • Goldman N (1993) Statistical tests of models of DNA substitution. J Mol Evol 36:182–198

    Google Scholar 

  • Gonzalez IL, Sylvester JE, Smith TF, Stambolian D, Schmickel RD (1990) Ribosomal RNA gene sequences and hominoid phylogeny. Mol Biol Evol 7:203–219

    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

    Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1987) Man's place in Hominoidea as inferred from molecular clocks of DNA. J Mol Evol 26:132–147

    Google Scholar 

  • Hasegawa M, Kishino H, Hayasaka K, Horai S (1990) Mitochondrial DNA evolution in primates: transition rate has been extremely low in lemur. J Mol Evol 31:113–121

    Google Scholar 

  • Hasegawa M (1991) Molecular phylogeny and man's place in Hominoidea. J Anthrop Soc Nippon 99:49–61

    Google Scholar 

  • Hasegawa M, Horai S (1991) Time of the deepest root for polymorphism in human mitochondrial DNA. J Mol Evol 32:37–42

    Google Scholar 

  • Hasegawa M, Cao Y, Adachi J, Yano T (1992) Rodent polyphyly? Nature 355:595–595

    Google Scholar 

  • Hasegawa M, Hashimoto T, Adachi J, Iwabe N, Miyata T (1993a) Early divergences in the evolution of eukaryotes: ancient divergence of Entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Evol 36:380–388

    Google Scholar 

  • Hasegawa M, Di Rienzo A, Kocher TD, Wilson AC (1993b) Toward a more accurate time scale for the human mitochondrial DNA tree. J Mol Evol 37:347–354

    Google Scholar 

  • Hashimoto T, Otaka E, Adachi J, Mizuta K, Hasegawa M (1993) The giant panda is most close to a bear, judged by α- and β-hemoglobin sequences. J Mol Evol 36:282–289

    Google Scholar 

  • Hashimoto T, Nakamura Y, Nakamura F, Shirakura T, Adachi J, Goto N, Okamoto K, Hasegawa M (1994) Protein phylogeny gives a robust estimation for early divergences of eukaryotes: phylogenetic place of a mitochondria-lacking protozoan, Giardia lamblia. Mol Biol Evol 11:65–71

    Google Scholar 

  • Hayasaka K, Gojobori T, Horai S (1988) Molecular phylogeny and evolution of primate mitochondrial DNA. Mol Biol Evol 5:626–644

    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 genealogy. J Mol Evol 35:32–43; Erratum 37:89–89 (1993)

    Google Scholar 

  • Jones DT, Taylor WR, Thomton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol III. Academic Press, New York, pp 21–132

    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

    Google Scholar 

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

    Google Scholar 

  • Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29:170–179

    Google Scholar 

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

    Google Scholar 

  • Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 30:151–160

    Google Scholar 

  • Kocher TD, Wilson AC (1991) Sequence evolution of mitochondrial DNA in humans and chimpanzees: control region and a protein-coding region. In: Osawa S, Honjo T (eds) Evolution of life: fossils, molecules, and culture. Springer-Verlag, Tokyo, pp 391–413

    Google Scholar 

  • Maeda N, Wu C-I, Bliska J, Reneke J (1988) Molecular evolution of intergenic DNA in higher primates: pattern of DNA changes, molecular clock, and evolution of repetitive sequences. Mol Biol Evol 5:1–20

    Google Scholar 

  • McCrossin ML, Benefit BR (1993) Recently recovered Kenyapithecus mandible and its implications for great ape and human origins. Proc Natl Acad Sci USA 90:1962–1966

    Google Scholar 

  • Miyamoto MM, Slightom JL, Goodman M (1987) Phylogenetic relations of humans and African apes from DNA sequences in the ωη-globin region. Science 238:369–373

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Pesole G, Ebisá E, Preparata G, Saccone C (1992) The evolution of the mitochondrial D-loop region and the origin of modern man. Mol Biol Evol 9:587–598

    Google Scholar 

  • Pilbeam D (1988) Human origins and evolution. In: Fabian AC (ed) Origins. Cambridge University Press, Cambridge, pp 89–114

    Google Scholar 

  • Reeves JH (1992) Heterogeneity in the substitution process of amino acid sites of proteins coded for by mitochondrial DNA. J Mol Evol 35:17–31

    Google Scholar 

  • Ruvolo M, Disotell TR, Allard MW, Brown WM, Honeycutt RL (1991) Resolution of the African hominoid trichotomy by use of a mitochondrial gene sequence. Proc Natl Acad Sci USA 88:1570–1574

    Google Scholar 

  • Ruvolo M, Zehr S, von Dornum M, Pan D, Chang B, Lin J (1993) Mitochondrial COII sequences and modern human origins. Mol Biol Evol 10:1115–1135

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

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

    Google Scholar 

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

    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

    Google Scholar 

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

    Google Scholar 

  • Sibley CG, Comstock JA, Ahlquist JE (1990) DNA hybridization evidence of hominoid phylogeny: a reanalysis of the data. J Mol Evol 30:202–236

    Google Scholar 

  • Sidow A, Nguyen T, Speed TP (1992) Estimating the fraction of invariable codons with a capture-recapture method. J Mol Evol 35: 253–260

    Google Scholar 

  • Takahata N (1985) Population genetics of extranuclear genomes: a model and review. In: Ohta T, Aoki K (eds) Population genetics and molecular evolution. Japan Sci Soc Press, Tokyo, pp 195–212

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    Google Scholar 

  • Thorne AG, Wolpoff MH (1992) The multiregional evolution of humans. Sci Am 266(4):76–83

    Google Scholar 

  • Ueda S, Watanabe Y, Saitou N, Omoto K, Hayashida H, Miyata T, Hisajima H, Honjo T (1989) Nucleotide sequences of immunoglobulin-epsilon pseudogenes in man and apes and their phylogenetic relationships. J Mol Biol 205:85–90

    Google Scholar 

  • Yang Z (1993) Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Mol Biol Evol 10:1396–1401

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Statistical Science, The Graduate University for Advanced Studies, 4-6-7 Minami-Azabu, Minato-ku, 106, Tokyo, Japan

    Jun Adachi & Masami Hasegawa

  2. The Institute of Statistical Mathematics, 4-6-7 Minami-Azabu, Minato-ku, 106, Tokyo, Japan

    Masami Hasegawa

Authors
  1. Jun Adachi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masami Hasegawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Correspondence to: M. Hasewaga

Rights and permissions

Reprints and permissions

About this article

Cite this article

Adachi, J., Hasegawa, M. Improved dating of the human/chimpanzee separation in the mitochondrial DNA tree: Heterogeneity among amino acid sites. J Mol Evol 40, 622–628 (1995). https://doi.org/10.1007/BF00160510

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00160510

Key words

Search

Navigation