Summary
Molecular biology has resurrected C. Darwin and T.H. Huxley's question about the origin of humans, but the precise branching pattern and dating remain controversial. To settle this issue, a large amount of sequence information is required. We determined mitochondrial (mt) DNA sequences for five hominoids; pygmy and common chimpanzees, gorilla, orangutan, and siamang. The common region compared with the known human sequence is 4759 by long, encompassing genes for 11 transfer RNAs and 6 proteins. Because of the high substitution rates in mammalian mtDNA and an unprecedentedly large region compared, the sequence differences clearly indicate that the closest relatives to human are chimpanzees rather than gorilla. For dating the divergences of human, chimpanzee, and gorilla, we used only unsaturated parts of sequence differences in which the mtDNA genealogy is not obscured by multiple substitutions. The result suggests that gorilla branched off 7.7 ± 0.7 million years (Myr) ago and human 4.7 ± 0.5 Myr ago; the time difference between these divergences being as long as 3 Myr.
Similar content being viewed by others
References
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 290:457–465
Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) Complete sequence of bovine mitochondrial DNA: conserved features of the mammalian mitochondrial genome. J Mol Biol. 156:683–717
Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180
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
Caccone A, Powell JR (1989) DNA divergence among hominoids. Evolution 43:925–942
Darwin C (1859) The origin of species by means of natural selection. John Murray, London
Djian P, Green H (1989) Vectorial expansion of the involucrin gene and the relatedness of the hominoids. Proc Natl Acad Sci USA 86:8447–8451
Felsenstein J (1990) PHYLIP manual version 3.3. University Herbarium, University of California, Berkeley
Foran DR, Hixson JE, Brown WM (1988) Comparison of ape and human sequences that regulate mitochondrial DNA transcription and D-loop DNA synthesis. Nucleic Acids Res 16: 5841–5861
Gibbons A (1990) Our chimp cousins get that much closer. Science 250:376
Gonzalez IL, Sylvester JE, Smith TF, Stambolian D, Schmickel RD (1990) Ribosomal RNA gene sequences and hominoid phylogeny. Mol Biol Evol 7:203–219
Goodman M, Braunitzer G, Stangl A, Schrank B (1983) Evidence on human origin from haemoglobins of African apes. Nature 303:546–548
Goodman M, Koop BF, Czelusniak J, Fitch DHA, Tagle DA, Slightom JL (1989) Molecular phylogeny of the family of apes and humans. Genome 31:316–335
Gould SJ (1980) Our natural place. In: Hen's teeth and horse's toes. W. W. Norton, New York, p 241
Hasegawa M, Kishino H (1991) DNA sequence analysis and evolution of Hominoidea. In: Kimura M, Takahata N (eds) New aspects of the genetics of molecular evolution. Springer/Verlag, Tokyo, p 303
Hixson JE, Brown WM (1986) A comparison of the small ribosomal RNA genes from the mitochondrial DNA of great apes and humans: sequence, structure, evolution, and phylogenetic implications. Mol Biol Evol 3:1–18
Huxley TH (1894) Evolution and ethics and other essays. D. Appleton, New York
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
Kimura M (1987) Molecular evolutionary clock and the neutral theory. J Mol Evol 26:24–33
Koop BF, Goodman M, Xu P, Chan K, Slightom JL (1986) Primate η-globin DNA sequences and man's place among the great apes. Nature 319:234–238
Koop BF, Tagle DA, Goodman M, Slightom JL (1989) A molecular view of primate phylogeny and important systematic and evolutionary questions. Mol Biol Evol 6:580–612
Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132
Lewin R (1988) In the age of mankind. Smithsonian Book, Washington DC
Li W-H, Luo C-C, Wu C-I (1985) Evolution of DNA sequences. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 1–94
Mellars P, Stringer C (1989) The human revolution: behavioral and biological perspectives on the origin of modern humans. Princeton University Press, Princeton NJ
Miyamoto MM, Slightom JL, Goodman M (1987) Phylogenetic relations of humans and African apes from DNA sequences in the ψη-globin region. Science 238:369–373
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5:568–583
Pilbeam DR (1984) The descent of hominoids and hominids. Sci Am 250:60–69
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
Saiki RK, Gelfand DH, Stoffen S, Scharf SH, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplifications of DNA with a thermostable DNA polymerase. Science 239:487–491
Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sanger F, Nicklen S, Coulson AR (1977) DNA sequence with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467
Sarich VM, Wilson AC (1967) Immunological time scale for hominoid evolution. Science 158:1200–1203
Sibley CG, Ahlquist JE (1984) The phylogeny of the hominoid primates, as indicated by DNA hybridization. J Mol Evol 20: 2–15
Sibley CG, Comstock JA, Ahlquist JE (1990) DNA hybridization evidence of hominoid phylogeny: a reanalysis of the data. J Mol Evol 30:202–236
Stringer CB (1990) The emergence of modern humans. Sci Am 263:68–74
Takahata N (1989) Gene genealogy in three related populations: consistency probability between gene and population trees. Genetics 122:957–966
Takahata N, Tajima F (1991) Sampling errors in phylogeny. Mol Biol Evol 8:494–502
Takahata N, Satta Y, Klein J (1992) Polymorphism and balancing selection at the major histocompatibility complex loci. Genetics 130:925–938
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
Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson Y, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166
Author information
Authors and Affiliations
Additional information
Offprint requests to: S. Horai
Rights and permissions
About this article
Cite this article
Horai, S., Satta, Y., Hayasaka, K. et al. Man's place in hominoidea revealed by mitochondrial DNA genealogy. J Mol Evol 35, 32–43 (1992). https://doi.org/10.1007/BF00160258
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00160258