Summary
Divergence dates among primates were estimated by molecular clock analysis of DNA sequence data. A molecular clock of η-globin pseudogene was calibrated by setting the date of divergence between Catarrhini and Platyrrhini at 38 million years (Myr) ago. The clock gave dates of 25.3±2.4, 11.9±1.7, 5.9±1.2, and 4.9±1.2 Myr ago (± refers to standard error) for the separation of rhesus monkey, orangutan, gorilla, and chimpanzee, respectively, from the line leading to humans. In placing confidence intervals of the estimates in a robust way, a bootstrap method was used. The 95% confidence intervals are 20.5–29.5, 9.0–14.8, 4.1–7.8, and 3.1–7.0 Myr ago for the separation of rhesus monkey, orangutan, gorilla, and chimpanzee, respectively. By a molecular clock dating of the Prosimii-Anthropoidea splitting, it was suggested that the evolutionary rate of the η-globin gene was high early in primate evolution and subsequently decreased in the line of Anthropoidea. And, by a relative rate test using bootstrap sampling, the possibility of further decrease of the rate (more than 10%) in the line of Hominoidea compared with that of Cercopithecoidea was suggested. Therefore, the above dating of the splittings within Hominoidea may be biased slightly toward younger dates. On the other hand, mitochondrial DNA (mtDNA) seems to have evolved in mammals with a more uniform rate than the η-globin gene. The ratio of the dates of orangutan splitting to chimpanzee splitting is larger for the mtDNA clock than that for the η-globin clock, suggesting the possibilities of mt-DNA introgression among the early hominids and the early African apes, and/or of mtDNA polymorphism within the common ancestral species of orangutan and the African apes that obscures the date of the true species separation of orangutans.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Alvarez LW, Alvarez W, Asaro F, Michel HV (1980) Extraterrestrial cause for the Cretaceous-Tertiary extinction. Science 208:1095–1108
Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger E, Young IG (1982) The complete sequence of bovine mitochondrial DNA: conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717
Andrews P (1982) Hominoid evolution. Nature 295:185–186
Andrews P (1985) Family group systematics and evolution among catarrhine primates. In: Delson E (ed) Ancestors—the hard evidence. Alan R Liss, New York, pp 14–22
Andrews P (1986) Molecular evidence for catarrhine evolution. In: Wood B, Martin L, Andrews P (eds) Major topics in primate and human evolution. Cambridge University Press, Cambridge, pp 107–129
Andrews P, Cronin JE (1982) The relationship ofSivapithecus andRamapithecus and the evolution of the orang-utan. Nature 297:541–546
Benveniste RE, Todaro GJ (1976) Evolution of type C viral genes: evidence for an Asian origin of man. Nature 261:101–107
Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180
Bishop MJ, Friday AE (1985) Evolutionary trees from nucleic acid and protein sequences. Proc R Soc Lond B226:271–302
Britten RJ (1986) Rates of DNA sequence evolution differ between taxonomic groups. Science 231:1393–1398
Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequence of primates: tempo and mode of evolution. J Mol Evol 18:225–239
Chang L-YE, Slightom JL (1984) Isolation and nucleotide sequence analysis of the β-type globin pseudogene from human, gorilla and chimpanzee. J Mol Biol 180:767–784
Ciochon RL, Chiarelli AB (1980) Evolutionary biology of the New World monkeys and continental drift. Plenum, New York
Ciochon RL, Corruccini RS (1983) New interpretations of ape and human ancestry. Plenum, New York
Diaconis P, Efron B (1983) Computer-intensive methods in statistics. Sci Am 249:116–130
Easteal S (1985) Generation time and the rate of molecular evolution. Mol Biol Evol 2:450–453
Efron B (1979) Bootstrap methods: another look at the jackknife. Ann Stat 7:1–26
Efron B, Gong G (1983) A leisurely look at the bootstrap, the jackknife, and cross-validation. Am Stat 37:36–48
Eldredge N, Gould SJ (1972) Punctuated equilibria: an alternative to phyletic gradualism. In: Schopf TJM (ed) Models in paleobiology. Freeman, Cooper and Co, San Francisco, pp 82–115
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Ferris SD, Wilson AC, Brown WM (1981) Evolutionary tree for apes and humans based on cleavage maps of mitochondrial DNA. Proc Natl Acad Sci USA 78:2432–2436
Ferris SD, Sage RD, Huang C-M, Nielsen JT, Ritte U, Wilson AC (1983) Flow of mitochondrial DNA across a species boundary. Proc Natl Acad Sci USA 80:2290–2294
Fitch WM (1986) Commentary. Mol Biol Evol 3:296–298
Gillespie JH, Langley CH (1979) Are evolutionary rates really variable? J Mol Evol 13:27–34
Gingerich PD (1984) Primate evolution: evidence from fossil record, comparative morphology, and molecular biology. Yearb Phys Anthropol 27:57–72
Gingerich PD (1986) Temporal scaling of molecular evolution in primates and other mammals. Mol Biol Evol 3:205–221
Goodman M (1963) Man's place in the phylogeny of the primates as reflected in serum proteins. In: Washburn SL (ed) Classification and human evolution. Aldine, Chicago, pp 204–224
Goodman M, Braunitzer G, Stangl A, Schrank B (1983) Evidence on human origins from haemoglobins of African apes. Nature 303:546–548
Goodman M, Koop BF, Czelusniak J, Weiss ML, Slightom JL (1984) The η-globin gene: its long evolutionary history in the β-globin gene family of mammals. J Mol Biol 180:803–823
Harris S, Barrie PA, Weiss ML, Jeffreys AJ (1984) The primate ψβ1 gene: an ancient β-globin pseudogene. J Mol Biol 180: 785–801
Hasegawa M, Yano T (1984) Phylogeny and classification of Hominoidea as inferred from DNA sequence data. Proc Jpn Acad 60B:389–392
Hasegawa M, Yano T, Kishino H (1984) A new molecular clock of mitochondrial DNA and the evolution of hominoids. Proc Jpn Acad 60B:95–98
Hasegawa M, Kishino H, Yano T (1985) Dating of the humanape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Hixson JE, Brown WM (1986) A comparison of the small ribosomal RNA genes from the mitochondrial DNA of the great apes and humans: sequence, structure, evolution, and phylogenetic implications. Mol Biol Evol 3:1–18
Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624–626
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
Kohne DE (1970) Evolution of higher-organism DNA. Quart Rev Biophys 3:327–375
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
Kortlandt A (1972) New perspectives on ape and human evolution. University of Amsterdam, Amsterdam
Langley CH, Fitch WM (1974) An examination of the constancy of rate of molecular evolution. J Mol Evol 3:161–177
Leakey LSB (1970) The relationship of African apes, man, and Old World monkeys. Proc Natl Acad Sci USA 67:746–748
Loh DY, Baltimore D (1984) Sexual preference of apparent gene conversion events in MHC genes of mice. Nature 309: 639–640
Lovejoy CO, Burstein AH, Heiple KG (1972) Primate phylogeny and immunological distance. Science 176:803–805
Martin L (1985) Significance of enamel thickness in hominoid evolution. Nature 314:260–263
Martin L (1986) Relationships among extant and extinct great apes and humans. In: Wood B, Martin, L, Andrews P (eds) Major topics in primate and human evolution. Cambridge University Press, Cambridge, pp 161–187
Nei M, Tajima F (1985) Evolutionary change of restriction cleavage sites and phylogenetic inference for man and apes. Mol Biol Evol 2:189–205
Novacek MJ (1982) Information for molecular studies from anatomical and fossil evidence on higher eutherian phylogeny. In: Goodman M (ed) Macromolecular sequences in systematic and evolutionary biology. Plenum, New York, pp 3–41
Ohta T (1973) Slightly deleterious mutant substitutions, in evolution. Nature 246:96–98
Ohta T, Kimura M (1971) On the constancy of the evolutionary rate of cistrons. J Mol Evol 1:18–25
Pickford M (1985)Kenyapithecus: a review of its status based on newly discovered fossils from Kenya. In: Tobias PV (ed) Hominid evolution—past, present and future. Alan R Liss, New York, pp 107–112
Pielou EC (1979) Interpretation of paleoecological similarity matrices. Paleobiology 5:435–443
Pilbeam D (1982) New hominoid skull material from the Miocene of Pakistan. Nature 295:232–234
Pilbeam D (1985) Patterns of hominoid evolution. In: Delson E (ed) Ancestors—the hard evidence. Alan R Liss, New York, pp 51–59
Ruvolo M, Smith TF (1986) Phylogeny and DNA-DNA hybridization. Mol Biol Evol 3:285–289
Saitou N (1986) On the delta Q-test of Templeton. Mol Biol Evol 3:282–284
Sarich VM, Cronin JE (1977) Generation length and rates of hominoid molecular evolution. Nature 269:354
Sarich VM, Wilson AC (1967a) Immunological time scale for hominid evolution. Science 158:1200–1203
Sarich VM, Wilson AC (1967b) Rates of albumin evolution in primates. Proc Natl Acad Sci USA 58:142–148
Savage DE, Russell RE (1983) Mammalian paleofaunas of the world. Addison-Wesley, London
Sibley CG, Ahlquist JE (1984) The phylogeny of the hominoid primates, as indicated by DNA-DNA hybridization. J Mol Evol 20:2–15
Simons EL (1981) Man's immediate forerunner's. Philos Trans R Soc Lond B Biol Sci 292:21–41
Sloan RE, Rigby JK Jr, Van Valen LM, Gabriel D (1986) Gradual dinosaur extinction and simultaneous ungulate radiation in the Hell Creek Formation. Science 232:629–633
Sneath PHA (1980) The estimation of differences in protein evolution rates. Proc Geol Assoc 91:71–79
Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460
Takahata N, Nei M (1985) Gene genealogy and variance of interpopulational nucleotide differences. Genetics 110:325–344
Takahata N, Slatkin M (1984) Mitochondrial gene flow. Proc Natl Acad Sci USA 81:1764–1767
Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221–244
Templeton AR (1985) The phylogeny of the hominoid primates: a statistical analysis of the DNA-DNA hybridization data. Mol Biol Evol 2:420–433
Templeton AR (1986) Further comments on the statistical analysis of DNA-DNA hybridization data. Mol Biol Evol 3:290–295
Uzzell T, Pilbeam D (1971) Phyletic divergence dates of hominoid primates: a comparison of fossil and molecular data. Evolution 25:615–635
Vogel F, Kopun M, Rathenberg R (1976) Mutation and molecular evolution. In: Goodman M, Tashian RE (eds) Molecular anthropology. Plenum, New York, pp 13–33
Washburn SL (1985) Human evolution after Raymond Dart. In: Tobias PV (ed) Hominid evolution—past, present and future. Alan R Liss, New York, pp 3–18
Willison KR (1985) Sex and frequency of gene conversion in meiosis. Nature 313:604
Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639
Winter RM, Tuddenham EGD, Goldman E, Matthews KB (1983) A maximum likelihood estimate of the sex ratio of mutation rates in haemophilia A. Hum Genet 64:156–159
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
Yunis JJ, Prakash O (1982) The origin of man: a chromosomal pictorial legacy. Science 215:1525–1530
Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic, New York, pp 97–166
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Hasegawa, M., Kishino, H. & Yano, Ta. Man's place in Hominoidea as inferred from molecular clocks of DNA. J Mol Evol 26, 132–147 (1987). https://doi.org/10.1007/BF02111287
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02111287