Journal of Molecular Evolution

, Volume 18, Issue 4, pp 225–239

Mitochondrial DNA sequences of primates: Tempo and mode of evolution

  • Wesley M. Brown
  • Ellen M. Prager
  • Alice Wang
  • Allan C. Wilson
Original Articles

Summary

We cloned and sequenced a segment of mitochondrial DNA from human, chimpanzee, gorilla, orangutan, and gibbon. This segment is 896 bp in length, contains the genes for three transfer RNAs and parts of two proteins, and is homologous in all 5 primates. The 5 sequences differ from one another by base substitutions at 283 positions and by a deletion of one base pair. The sequence differences range from 9 to 19% among species, in agreement with estimates from cleavage map comparisons, thus confirming that the rate of mtDNA evolution in primates is 5 to 10 times higher than in nuclear DNA. The most striking new finding to emerge from these comparisons is that transitions greatly outnumber transversions. Ninety-two percent of the differences among the most closely related species (human, chimpanzee, and gorilla) are transitions. For pairs of species with longer divergence times, the observed percentage of transitions falls until, in the case of comparisons between primates and non-primates, it reaches a value of 45. The time dependence is probably due to obliteration of the record of transitions by multiple substitutions at the same nucleotide site. This finding illustrates the importance of choosing closely related species for analysis of the evolutionary process. The remarkable bias toward transitions in mtDNA evolution necessitates the revision of equations that correct for multiple substitutions at the same site. With revised equations, we calculated the incidence of silent and replacement substitutions in the two protein-coding genes. The silent substitution rate is 4 to 6 times higher than the replacement rate, indicating strong functional constraints at replacement sites. Moreover, the silent rate for these two genes is about 10% per million years, a value 10 times higher than the silent rate for the nuclear genes studied so far. In addition, the mean substitution rate in the three mitochondrial tRNA genes is at least 100 times higher than in nuclear tRNA genes. Finally, genealogical analysis of the sequence differences supports the view that the human lineage branched off only slightly before the gorilla and chimpanzee lineages diverged and strengthens the hypothesis that humans are more related to gorillas and chimpanzees than is the orangutan.

Key words

DNA sequencing Transitions Multiplehit corrections Silent substitutions Replacement substitutions Transfer RNA Mutation pressure Functional constraints Hominoid phylogeny Start codons 

Abbreviations

mtDNA

mitochondrial DNA

bp

base pair

URF

unidentified reading frame

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465Google Scholar
  2. Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) The complete sequence of bovine mitochondrial DNA: conserved features of the mammalian mitochondrial genome. J Mol Biol (in press)Google Scholar
  3. Attardi G, Cantatore P, Ching E, Crews S, Gelfand R, Merkel C, Montoya J, Ojala D (1980) The remarkable features of gene organization and expression of human mitochondrial DNA. In: Kroon AM, Saccone C (eds) The organization and expression of the mitochondrial genome. Elsevier/North Holland Biomedical Press, Amsterdam, pp 103–119Google Scholar
  4. Barrell BG, Anderson S, Bankier AT, de Bruijn MHL, Chen E, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1980) Different patterns of codon recognition by mammalian mitochondrial tRNAs. Proc Natl Acad Sci USA 77:3164–3166Google Scholar
  5. Barrie PA, Jeffreys AJ, Scott AF (1981) Evolution of theβ-globin gene cluster in man and the primates. J Mol Biol 149:319–336Google Scholar
  6. Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180Google Scholar
  7. Brown WM (1980) Polymorphism in mitochondrial DNA of humans as revealed by restriction endonuclease analysis. Proc Natl Acad Sci USA 77:3605–3609Google Scholar
  8. Brown WM (1981) Mechanisms of evolution of animal mitochondrial DNA. Annals NY Acad Sci 361:119–134Google Scholar
  9. Brown WM, George M Jr, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971Google Scholar
  10. Brown WM, Vinograd J (1974) Restriction endonuclease cleavage maps of animal mitochondrial DNAs. Proc Natl Acad Sci USA 71:4617–4621Google Scholar
  11. Brues AM (1977) People and races. Macmillan, New York, pp 1–336Google Scholar
  12. Cann RL, Brown WM, Wilson AC (1982) Evolution of human mitochondrial DNA: Molecular, genetic and anthropological implications. Proc Sixth Internat Congress Human Genetics, Vol I, in pressGoogle Scholar
  13. Castora FJ, Arnheim N, Simpson MV (1980) Mitochondrial DNA polymorphism: Evidence that variants detected by restriction enzymes differ in nucleotide sequence rather than in methylation. Proc Natl Acad Sci USA 77:6415–6419Google Scholar
  14. Cedergren RJ, Sankoff D, LaRue B, Grosjean H (1981) The evolving tRNA molecule. CRC Crit Rev Biochem 11:35–103Google Scholar
  15. Clemmey H (1976) World's oldest animal traces. Nature 261:576–578Google Scholar
  16. Cocks GT, Wilson AC (1972) Enzyme evolution in the Enterobacteriaceae. J Bacteriol 110:793–802Google Scholar
  17. Cordell B, Bell G, Tischer E, DeNoto FM, Ullrich A, Pictet A, Rutter WJ, Goodman HM (1979) Isolation and characterization of a rat insulin gene. Cell 18:533–543Google Scholar
  18. Dayhoff MO (1973) Atlas of protein sequence and structure, Vol 5, Supp I. Nat Biomed Res Found, Georgetown Univ Med Center, Wash DC, p S-101Google Scholar
  19. Dayhoff MO (1976) Atlas of protein sequence and structure, Vol 5, Supp 2. Nat Biomed Res Found, Georgetown Univ Med Center, Wash DC, pp 283–284Google Scholar
  20. de Bruijn MHL, Schreier PH, Eperon IC, Barrell BG, Chen EY, Armstrong PW, Wong JFH, Roe BA (1980) A mammalian mitochondrial serine transfer RNA lacking the “dihydrouridine” loop and stem. Nucleic Acids Res 8:5213–5222Google Scholar
  21. Derancourt J, Lebor AS, Zuckerkandl E (1967) Séquence des acides aminés, séquence des nucléotides et évolution. Bull Soc Chim Biol 49:577–607Google Scholar
  22. De Vos WM, Bakker H, Saccone C, Kroon AM (1980) Further analysis of the type differences of rat liver mitochondrial DNA. Biochim Biophys Acta 607:1–9Google Scholar
  23. Efstratiadis A, Posakony JW, Maniatis T, Lawn RM, O'Connell C, Spritz RA, DeRiel JK, Forget BG, Weissman SM, Slightom JL, Blechl AE, Smithies O, Baralle FE, Shoulders CC, Proudfoot NJ (1980) The structure and evolution of the humanβ-globin gene family. Cell 21: 653–668Google Scholar
  24. Farris JS (1972) Estimating phylogenetic trees from distance matrices. Am Natur 106: 645–668Google Scholar
  25. Ferris SD, Wilson AC, Brown WM (1981a) Evolutionary tree for apes and humans based on cleavage maps of mitochondrial DNA. Proc Natl Acad Sci USA 78:2432–2436Google Scholar
  26. Ferris SD, Brown WM, Davidson WS, Wilson AC (1981b) Extensive polymorphism in the mitochondrial DNA of apes. Proc Natl Acad Sci USA 78:6319–6323Google Scholar
  27. Fitch WM (1980) Estimating the total number of nucleotide substitutions since the common ancestor of a pair of homologous genes: Comparison of several methods and three beta hemoglobin messenger RNAs. J Mol Evol 16:153–209Google Scholar
  28. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284Google Scholar
  29. Freese E, Yoshida A (1965) The role of mutations in evolution. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 341–355Google Scholar
  30. Goddard JM, Masters JN, Jones SS, Ashworth WD, Wolstenholme DR (1981) Nucleotide sequence variants ofRattus norvegicus mitochondrial DNA. Chromosoma 82:595–609Google Scholar
  31. Hanahan D, Meselson M (1980) Plasmid screening at high colony density. Gene 10:63–67Google Scholar
  32. Heckman JE, Sarnoff J, Alzner-DeWeerd B, Yin S, RajBhandary UL (1980) Novel features in the genetic code and codon reading patterns inNeurospora crassa mitochondria based on sequences of six mitochondrial tRNAs. Proc Natl Acad Sci USA 77:3159–3163Google Scholar
  33. Holmquist R (1972) Theoretical foundations for a quantitative approach to paleogenetics. Part I: DNA. J Mol Evol 1:115–133Google Scholar
  34. Holmquist R, Jukes TH, Moise H, Goodman M, Moore GW (1976) The evolution of the globin family genes: Concordance of stochastic and augmented maximum parsimony genetic distances forα hemoglobin,β hemoglobin and myoglobin phylogenies. J Mol Biol 105:39–74Google Scholar
  35. Holmquist R, Pearl D (1980) Theoretical foundations for quantitative paleogenetics. Part III: The molecular divergence of nucleic acids and proteins for the case of genetic events of unequal probability. J Mol Evol 16:211–267Google Scholar
  36. Jukes TH (1980) Silent nucleotide substitutions and the molecular evolutionary clock. Science 210:973–978Google Scholar
  37. Jukes TH (1981) Amino acid codes in mitochondria as possible clues to primitive codes. J Mol Evol 18:15–17Google Scholar
  38. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, Vol III, Academic Press, New York, pp 21–132Google Scholar
  39. Kimura M (1981) Possibility of extensive neutral evolution under stabilizing selection with special reference to nonrandom usage of synonymous codons. Proc Natl Acad Sci USA 78:5773–5777Google Scholar
  40. Kluge AG (1982) Reclassification of the great apes. In: Ciochon RL, Corruccini RS (eds) New interpretations of ape and human ancestry. Plenum Press, New York, in pressGoogle Scholar
  41. Köchel HG, Lazarus CM, Basak N, Küntzel H (1981) Mitochondrial tRNA gene clusters inAspergillus nidulans: Organization and nucleotide sequence. Cell 23:625–633Google Scholar
  42. Martin NC, Miller D, Hartley J, Moynihan P, Donelson JE (1980) The tRNAAGYSer and tRNACGYArg genes form a gene cluster in yeast mitochondrial DNA. Cell 19:339–343Google Scholar
  43. Martin SL, Zimmer EA, Davidson WS, Wilson AC, Kan YW (1981) The untranslated regions ofβ-globin mRNA evolve at a functional rate in higher primates. Cell 25:737–741Google Scholar
  44. Maxam AM, Gilbert W (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Meth Enzymology 65:499–560Google Scholar
  45. Nichols BP, Miozzari GF, Van Cleemput M, Bennett GN, Yanofsky C (1980) Nucleotide sequences of the trp G regions ofEscherichia coli, Shigella dysenteriae, Salmonella typhimurium andSerratia marcescens. J Mol Biol 142:503–517Google Scholar
  46. Perler F, Efstratiadis A, Lomedico P, Gilbert W, Kolodner R, Dodgson J (1980) The evolution of genes: The chicken preproinsulin gene. Cell 20: 555–566Google Scholar
  47. Pilbeam D (1979) Recent finds and interpretations of Miocene hominoids. Ann Rev Anthrop 8:333–352Google Scholar
  48. Romer AS (1966) Vertebrate paleontology. Univ of Chicago, Chicago, pp 1–468Google Scholar
  49. Saccone C, Cantatore P, Gadaleta G, Gallerani R, Lanave C, Pepe G, Kroon AM (1981) The nucleotide sequence of the large ribosomal RNA gene and the adjacent tRNA genes from rat mitochondria. Nucleic Acids Res 9:4139–4148Google Scholar
  50. Sarich VM, Wilson AC (1967) Immunological time scale for hominid evolution. Science 158:1200–1203Google Scholar
  51. Singer CE, Smith GR (1972) Histidine regulation inSalmonella typhimurium. XIII. Nucleotide sequence of histidine transfer ribonucleic acid. J Biol Chem 247:2989–3000Google Scholar
  52. Sinha NK, Haimes MD (1981) Molecular mechanisms of substitution mutagenesis, J Biol Chem 256:10671–10683Google Scholar
  53. Smith HO (1980) Recovery of DNA from gels. Meth Enzymology 65:371–380Google Scholar
  54. Sprinzl M, Grueter F, Spelzhaus A, Gauss DH (1980) Compilation of tRNA sequences. Nucleic Acids Res 8:r1-r22Google Scholar
  55. Staden R (1980) A computer program to search for tRNA genes. Nucleic Acids Res 8:817–825Google Scholar
  56. Steel RGD, Torrie JH (1960) Principles and procedures of statistics-with special reference to the biological sciences. McGraw-Hill, New York, pp 1–481Google Scholar
  57. Topal MD, Fresco JR (1976) Complementary base pairing and the origin of substitution mutations. Nature 263:285–289Google Scholar
  58. Walberg MW, Clayton DA (1981) Sequence and properties of the human KB cell and mouse L cell D-loop regions of mitochondrial DNA. Nucleic Acids Res 9:5411–5421Google Scholar
  59. Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639Google Scholar
  60. Zimmer EA (1980) Evolution of primate globin genes. PhD Thesis, Univ of California, Berkeley, pp 1–366Google Scholar

Copyright information

© Springer-Verlag 1982

Authors and Affiliations

  • Wesley M. Brown
    • 1
  • Ellen M. Prager
    • 1
  • Alice Wang
    • 1
  • Allan C. Wilson
    • 1
  1. 1.Department of BiochemistryUniversity of CaliforniaBerkeleyUSA
  2. 2.Division of Biological SciencesUniversity of MichiganAnn ArborUSA
  3. 3.Cetus CorporationBerkeleyUSA

Personalised recommendations