Journal of Molecular Evolution

, Volume 30, Issue 3, pp 260–266

Primate evolution at the DNA level and a classification of hominoids

  • Morris Goodman
  • Danilo A. Tagle
  • David H. A. Fitch
  • Wendy Bailey
  • John Czelusniak
  • Ben F. Koop
  • Philip Benson
  • Jerry L. Slightom
Article

Summary

The genetic distances among primate lineages estimated from orthologous noncoding nucleotide sequences of β-type globin loci and their flanking and intergenic DNA agree closely with the distances (delta T50H values) estimated by cross hybridization of total genomic single-copy DNAs. These DNA distances and the maximum parsimony tree constructed for the nucleotide sequence orthologues depict a branching pattern of primate lineages that is essentially congruent with the picture from phylogenetic analyses of morphological characters. The molecular evidence, however, resolves ambiguities in the morphological picture and provides an objective view of the cladistic position of humans among the primates. The molecular data group humans with chimpanzees in subtribe Hominina, with gorillas in tribe Hominini, orangutans in subfamily Homininae, gibbons in family Hominidae, Old World monkeys in infraorder Catarrhini, New World monkeys in semisuborder Anthropoidea, tarsiers in suborder Haplorhini, and strepsirhines (lemuriforms and lorisiforms) in order Primates. A seeming incongruency between organismal and molecular levels of evolution, namely that morphological evolution appears to have speeded up in higher primates, especially in the lineage to humans, while molecular evolution has slowed down, may have the trivial explanation that relatively small genetic changes may sometimes result in marked phenotypic changes.

Key words

Noncoding nucleotide sequences DNA hybridization Primate phylogeny Maximum parsimony Cladistic classification 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aiello LC (1986) The relationships of the Tarsiiformes: a review of the case for the Haplorhini. In: Wood B, Martin L, Andrews P (eds) Major topics in primate and human evolution. Cambridge University Press, Cambridge, pp 47–65Google Scholar
  2. Bonner TI, Heinemann R, Todaro GJ (1980) Evolution of DNA sequence has been retarded in Malagasy lemurs. Nature 286: 420–423PubMedGoogle Scholar
  3. Caccone A, Powell JR (1989) DNA divergence among hominoids. Evolution 43:925–942Google Scholar
  4. Darwin C (1859) The origin of species by means of natural selection or the preservation of favored races in the struggle for life. Doubleday, Garden City. Reprinted editionGoogle Scholar
  5. Fitch DHA, Mainone C, Slightom JL, Goodman M (1988) The spider monkey ψη-globin gene and surrounding sequences: recent or ancient insertion of lines and sines? Genomics 3: 237–255PubMedGoogle Scholar
  6. Fitch DHA, Mainone C, Goodman M, Slightom JL (1989) Molecular history of gene conversions in the primate fetal γ-globin genes: nucleotide sequences from the common gibbon,Hylobates lar. J Biol Chem (in press)Google Scholar
  7. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284PubMedGoogle Scholar
  8. Fleagle JG (1988) Primate adaptation and evolution. Academic Press, San DiegoGoogle Scholar
  9. Goodman M (1962) Immunochemistry of the primates and primate evolution. Ann NY Acad Sci 102:219–234PubMedGoogle Scholar
  10. 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 204–234Google Scholar
  11. Goodman M, Koop BF, Czelusniak J, Fitch DHA, Tagle DA, Slightom JL (1989) Molecular phylogeny of the family of apes and humans. Genome 31:316–335PubMedGoogle Scholar
  12. Holmquist R, Miyamoto MM, Goodman M (1988) Analysis of higher-primate phylogeny from transversion differences in nuclear and mitochondrial DNA by Lake's methods of evolutionary parsimony and operator metrics. Mol Biol Evol 5: 217–236PubMedGoogle Scholar
  13. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–123Google Scholar
  14. 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 319:234–238PubMedGoogle Scholar
  15. Koop BF, Tagle DA, Goodman M, Slightom JL (1989) A molecular view of primate phylogeny and important systematic and evolutionary questions. Mol Biol Evol 6:580–612PubMedGoogle Scholar
  16. 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 5:1–20PubMedGoogle Scholar
  17. Margot JB, Demero GW, Hardison RC (1989) Complete nucleotide sequence of the rabbit β-like globin gene cluster. J Mol Biol 205:15–40PubMedGoogle Scholar
  18. Miyamoto MM, Slightom JL, Goodman M (1987) Phylogenetic relations of humans and African apes from DNA sequence in the ψη-globin region. Science 238:369–373PubMedGoogle Scholar
  19. Miyamoto MM, Koop BF, Slightom JL, Goodman M, Tennant MR (1988) Molecular systematics of higher primates: genealogical relations and classification. Proc Natl Acad Sci USA 85:7627–7631PubMedGoogle Scholar
  20. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  21. Sarich VM, Schmid CW, Marks J (1989) DNA hybridization as a guide to phylogenies: a critical analysis. Cladistics 5:3–32Google Scholar
  22. Sibley CG, Ahlquist JE (1984) The phylogeny of hominoid primates, as indicated by DNA-DNA hybridization. J Mol Evol 20:2–15PubMedGoogle Scholar
  23. Sibley CG, Ahlquist JE (1987) DNA hybridization evidence of hominoid phylogeny: results from an expanded data set. J Mol Evol 26:99–121PubMedGoogle Scholar
  24. Simons EL, Rasmussen DT (1989) Cranial morphology ofAegyptopithecus andTarsius and the question of the tarsier-anthropoidean clade. Am J Phys Anthropol 79:1–23PubMedGoogle Scholar
  25. Simpson GG (1945) The principles of classification and a classification of mammals. Bull Am Mus Nat Hist 85:1–350Google Scholar
  26. Simpson GG (1961) Principles of animal taxonomy. Columbia University Press, New YorkGoogle Scholar
  27. Simpson GG (1963) The meaning of taxonomic statements. In: Washburn SL (ed) Classification and human evolution. Aldine, Chicago, pp 1–31Google Scholar
  28. Slightom JL, Koop BF, Xu P, Goodman M (1988) Rhesus fetal globin genes: concerted gene evolution in the descent of higher primates. J Biol Chem 263:12427–12438PubMedGoogle Scholar
  29. Tagle DA, Koop BF, Goodman M, Slightom JL, Hess DL, Jones RJ (1988) Embryonic ∈ and γ globin genes of a prosimian primate (Galago crassicaudatus): nucleotide and amino acid sequences, developmental regulation, and phylogenetic footprints. J Mol Biol 203:439–455PubMedGoogle Scholar
  30. 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 205:85–90PubMedGoogle Scholar
  31. Williams SA, Goodman M (1989) A statistical test that supports a human/chimpanzee clade based on non-coding DNA sequence data. Mol Biol Evol 6:325–330PubMedGoogle Scholar
  32. Zuckerkandl E (1963) Perspectives in molecular anthropology. In: Washburn SL (ed) Classification and human evolution. Aldine, Chicago, pp 243–272Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1990

Authors and Affiliations

  • Morris Goodman
    • 1
  • Danilo A. Tagle
    • 2
  • David H. A. Fitch
    • 1
  • Wendy Bailey
    • 2
  • John Czelusniak
    • 1
  • Ben F. Koop
    • 2
  • Philip Benson
    • 1
  • Jerry L. Slightom
    • 1
    • 3
  1. 1.Department of Anatomy and Cell BiologyWayne State University School of MedicineDetroitUSA
  2. 2.Department of Molecular Biology and GeneticsWayne State University School of MedicineDetroitUSA
  3. 3.Division of Molecular BiologyThe Upjohn CompanyKalamazooUSA
  4. 4.Division of BiologyCalifornia Institute of TechnologyPasadenaUSA

Personalised recommendations