Journal of Molecular Evolution

, Volume 26, Issue 1–2, pp 157–164 | Cite as

Tempo and mode of sequence evolution in mitochondrial DNA of HawaiianDrosophila

  • Rob DeSalle
  • Toby Freedman
  • Ellen M. Prager
  • Alan C. Wilson


Sequence comparisons were made for up to 667 bp of DNA cloned from 14 kinds of HawaiianDrosophila and five other dipteran species. These sequences include parts of the genes for NADH dehydrogenase (subunits 1, 2, and 5) and rRNA (from the large ribosomal subunit). Because the times of divergence among these species are known approximately, the sequence comparisons give insight into the evolutionary dynamics of this molecule. Transitions account for nearly all of the differences between sequences that have diverged by less than 2%; for these sequences the mean rate of divergence appears to be about 2%/Myr. In comparisons involving greater divergence times and greater sequence divergence, relatively more of the sequence differences are due to transversions. Specifically, the fraction of these differences that are counted as transversions rises from an initial value of less than 0.1 to a plateau value of nearly 0.6. The time required to reach half of the plateau value, about 10 Myr, is similar to that for mammalian mtDNA. The mtDNAs of flies and mammals are also alike in the shape of the curve relating the percentage of positions at which there are differences in protein-coding regions to the time of divergence. For both groups of animals, the curve has a steep initial slope ascribable to fast accumulation of synonymous substitutions and a shallow final slope resulting from the slow accumulation of substitutions causing amino acid replacements. However, the percentage of all sites that can experience a high rate of substitution appears to be only about 8% for fly mtDNA compared to about 20% for mammalian mtDNA. The low percentage of hypervariable sites may be a consequence of a functional constraint associated with the low content of guanine and cytosine in fly mtDNA.

Key words

Dideoxy sequencing Molecular clock Transitions Transversions Biased base composition NADH dehydrogenase Ribosomal RNA genes Phylogenetic tree Functional constraint Mosquito Insects 



mitochondrial DNA


base pair(s)


NADH dehydrogenase


ribosomal RNA


DNA encoding rRNA


million years


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aquadro CF, Kaplan N, Risko KJ (1984) An analysis of the dynamics of mammalian mitochondrial DNA sequence evolution. Mol Biol Evol 1:423–434PubMedGoogle Scholar
  2. Beverley SM, Wilson AC (1982) Molecular evolution inDrosophila and higher Diptera. I. Micro-complement fixation studies of a larval hemolymph protein. J Mol Evol 18:251–264CrossRefPubMedGoogle Scholar
  3. Beverley SM, Wilson AC (1984) Molecular evolution inDrosophila and the higher Diptera. II. A time scale for fly evolution. J Mol Evol 21:1–13PubMedGoogle Scholar
  4. Beverley SM, Wilson AC (1985) Ancient origin for Hawaiian Drosophilinae inferred from protein comparisons. Proc Natl Acad Sci USA 82:4753–4757PubMedGoogle Scholar
  5. Bodmer M Ashburner M (1984) Conservation and change in the DNA sequences coding for alcohol dehydrogenase in sibling species ofDrosophila. Nature 309:425–430PubMedGoogle Scholar
  6. Brown GG, Simpson MV (1982) Novel features of animal mtDNA evolution as shown by sequences of two rat cytochrome oxidase subunit II genes. Proc Natl Acad Sci USA 79:3246–3250Google Scholar
  7. Brown WM (1983) Evolution of animal mitochondrial DNA. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer, Sunderland MA, pp 62–88Google Scholar
  8. Brown WM (1985) The mitochondrial genome of animals. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 95–130Google Scholar
  9. Brown WM, George M Jr, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76: 1967–1971PubMedGoogle Scholar
  10. Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239PubMedGoogle Scholar
  11. Carson HL (1976) Inference of the time of origin of someDrosophila species. Nature 259:395–396CrossRefPubMedGoogle Scholar
  12. Carson HL (1982) Evolution of Drosophila on the newer Hawaiian volcanoes. Heredity 48:3–25PubMedGoogle Scholar
  13. Carson HL, Kaneshiro KY (1976)Drosophila of Hawaii: systematics and ecological genetics. Annu Rev Ecol Syst 7:311–345CrossRefGoogle Scholar
  14. Carson HL, Hardy DE, Spieth HT, Stone WS (1970) The evolutionary biology of the Hawaiian Drosophilidae. In: Hecht MK, Steere WC (eds) Essays in evolution and genetics in honor of Theodosius Dobzhansky. Appleton-Century-Crofts, New York, pp 437–543Google Scholar
  15. Clary DO, Wolstenholme DR (1985a) The ribosomal RNA genes ofDrosophila mitochondrial DNA. Nucleic Acids Res 13:4029–4045PubMedGoogle Scholar
  16. Clary DO, Wolstenholme DR (1985b) The mitochondrial DNA molecule ofDrosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271PubMedGoogle Scholar
  17. Clary DO, Goddard JM, Martin SC, Fauron CM-R, Wolstenholme DR (1982)Drosophila mitochondrial DNA: a novel gene order. Nucleic Acids Res 10:6619–6637PubMedGoogle Scholar
  18. de Bruijn MHL (1983)Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature 304:234–241CrossRefPubMedGoogle Scholar
  19. DeSalle R, Giddings LV (1986) Discordance of nuclear and mitochondrial DNA phylogenies in HawaiianDrosophila. Proc Natl Acad Sci USA 83:6902–6906PubMedGoogle Scholar
  20. DeSalle R, Giddings LV, Templeton AR (1986a) Mitochondrial DNA variability in natural populations of HawaiianDrosophila. I. Methods and levels of variability inD. silvestris andD. heteroneura populations. Heredity 56:75–85PubMedGoogle Scholar
  21. DeSalle R, Giddings LV, Kaneshiro KY (1986b) Mitochondrial DNA variability in natural populations of HawaiianDrosophila. II. Genetic and phylogenetic relationships of natural populations ofD. silvestris andD. heteroneura. Heredity 56:87–96PubMedGoogle Scholar
  22. Greenberg BD, Newbold JE, Sugino A (1983) Intraspecific nucleotide sequence variability surrounding the origin of replication in human mitochondrial DNA. Gene 21:33–49CrossRefPubMedGoogle Scholar
  23. Hennig W (1973) Diptera (Zweiflüger). In: Kükenthal W (ed) Handbuch der Zoologie IV:2:2:31. Arthropoda, Insecta, ed 2. W de Gruyter, Berlin, pp 1–337Google Scholar
  24. Higuchi R, Bowman B, Freiberger M, Ryder OA, Wilson AC (1984) DNA sequences from the quagga, an extinct member of the horse family. Nature 312:282–284CrossRefPubMedGoogle Scholar
  25. Higuchi RG, Wrischnik LA, Oakes E, George M, Tong B, Wilson AC (1987) Mitochondrial DNA of the extinct quagga: relatedness and extent of post-mortem change. J Mol Evol 25:283–287PubMedGoogle Scholar
  26. Holmquist R (1976) Solution to a gene divergence problem under arbitrary stable nucleotide transition probabilities. J Mol Evol 8:337–349CrossRefPubMedGoogle Scholar
  27. Holmquist R (1983) Transitions and transversions in evolutionary descent: an approach to understanding. J Mol Evol 19:134–144CrossRefPubMedGoogle Scholar
  28. HsuChen C-C, Koten RM, Dubin DT (1984) Sequences of the coding and flanking regions of the large ribosomal subunit RNA gene of the mosquito mitochondria. Nucleic Acids Res 12:7771–7785PubMedGoogle Scholar
  29. Johnson WE, Carson HL, Kaneshiro KY, Steiner WWM, Cooper MM (1975) Genetic variation in Hawaiian Drosophila II. Allozymic differentiation in theD. planitibia subgroup. In: Markert CL (ed) Isozymes IV: genetics and evolution. Academic Press, New York, pp 563–584Google Scholar
  30. Jukes TH (1982) Silent nucleotide substitutions in evolution. Presented at the Meeting of the Society for the Study of Evolution and The American Society of Naturalists, June 23, 1982, Stony Brook NYGoogle Scholar
  31. Powell JR, Caccone A, Amato GD, Yoon C (1986) Rates of nucleotide substitution inDrosophila mitochondrial DNA and nuclear DNA are similar. Proc Natl Acad Sci USA 83:9090–9093PubMedGoogle Scholar
  32. Solignac M, Monnerot M, Mounolou J-C (1986) Mitochondrial DNA evolution in themelanogaster species subgroup ofDrosophila. J Mol Evol 23:31–40PubMedGoogle Scholar
  33. Swofford DL (1985) Phylogenetic analysis using parsimony (PAUP), version 2.4. Illinois Natural History Survey, Champaign ILGoogle Scholar
  34. Topal MD, Fresco JR (1976) Complementary base pairing and the origin of substitution mutations. Nature 263:285–289CrossRefPubMedGoogle Scholar
  35. Vawter L, Brown WM (1986) Nuclear and mitochondrial DNA comparitions reveal extreme rate variation in the molecular clock. Science 234:194–196PubMedGoogle Scholar
  36. Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, Helm-Bychowski KM, Higuchi RG, Palumbi SR, Prager EM, Sage RD, Stoneking M (1985) Mitochondrial DNA and two perspectives on evolutionary genetics, Biol J Linn Soc 26:375–400Google Scholar
  37. Wolstenholme DR, Clary DO (1985) Sequence evolution ofDrosophila mitochondrial DNA. Genetics 109:725–744PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1987

Authors and Affiliations

  • Rob DeSalle
    • 1
  • Toby Freedman
    • 1
  • Ellen M. Prager
    • 1
  • Alan C. Wilson
    • 1
  1. 1.Department of BiochemistryUniversity of CaliforniaBerkeleyUSA

Personalised recommendations