Skip to main content
SpringerLink
Log in

Molecular evolution among someDrosophila species groups as indicated by two-dimensional electrophoresis

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

The evolutionary and phylogenetic relationships of sevenDrosophila species groups (represented byD. melanogaster, D. mulleri, D. mercatorum, D. robusta, D. virilis, D. immigrans, D. funebris, andD. melanica) were investigated by the use of two-dimensional electrophoresis. The resulting phylogeny is congruent with the current views of evolution among these groups based on morphological characters and immunological distances. Previous studies indicated that the ability of one-dimensional electrophoresis to resolve relationships between distantly related taxa extended to about the Miocene [25 million years (Myr) ago], but the present study demonstrates that two-dimensional electrophoresis is a useful indicator of phylogeny even back to the Paleocene (65 Myr ago). In addition, two-dimensional electrophoresis is shown to be a useful technique for detecting slowly evolving structural proteins such as actins and tropomyosins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams EN (1972) Consensus techniques and the comparison of taxonomic trees. Syst Zool 21:390–397

    Google Scholar 

  • Anderson NG, Anderson NL (1978a) Analytical techniques for cell fractions. XXI. Two-dimensional analysis of serum and tissue proteins: multiple isoelectric focusing. Anal Biochem 85:331–340

    Google Scholar 

  • Anderson NL, Anderson NG (1978b) Analytical techniques for cell fractions. XXII. Two-dimensional analysis of serum and tissue proteins: multiple gradient-slab electrophoresis. Anal Biochem 85:341–354

    Google Scholar 

  • Arnold ML, Baker RJ, Honeycutt RL (1983) Genic differentiation and phylogenetic relationships within two New World bat genera. Biochem Syst Ecol 11:295–303

    Google Scholar 

  • Avise JC (1975) Systematic value of electrophoretic data. Syst Zool 23:465–481

    Google Scholar 

  • Avise JC (1983) Protein variation and phylogenetic reconstruction. In: Oxford GS, Rollinson D (eds) Protein polymorphism: adaptive and taxonomic significance. Academic Press, London, pp 103–130

    Google Scholar 

  • Avise JC, Aquadro CF (1982) A comparative summary of genetic distances in the vertebrates. Evol Biol 15:151–185

    Google Scholar 

  • Avise JC, Patton JC, Aquadro CF (1980) Evolutionary genetics of birds. I. Relationships among north American thrushes and allies. Auk 97:135–147

    Google Scholar 

  • Ayala FJ (1982) Of clocks and clades, or a story of old told by genes of now. In: Nitecki MH (eds) Biochemical aspects of evolutionary biology. University of Chicago Press, Chicago, pp 257–301

    Google Scholar 

  • Ayala FJ (1986) On the virtues and pitfalls of the molecular evolutionary clock J Hered 77:226–235

    Google Scholar 

  • Bautch VL, Storti RV (1983) Identification of a cytoplasmic tropomyosin gene linked to two muscle tropomyosin genes inDrosophila. Proc Natl Acad Sci USA 80:7123–7127

    Google Scholar 

  • Bautch VL, Storti RV, Mischke D, Pardue ML (1982) Organization and expression ofDrosophila tropomyosin genes. J Mol Biol 162:231–250

    Google Scholar 

  • Baverstock PR, Cole SR, Richardson BJ, Watts CHS (1979) Electrophoresis and cladistics. Syst Zool 28:214–219

    Google Scholar 

  • Berlocher SH (1984) Insect molecular systematics. Annu Rev Entomol 29:403–433

    Google Scholar 

  • Beverley SM, Wilson AC (1982) Molecular evolution inDrosophila and the higher Diptera. I. Micro-complement fixation studies of a larval hemolymph protein. J Mol Evol 18:251–264

    Google Scholar 

  • Beverley SM, Wilson AC (1984) Molecular evolution inDrosophila and the higher Diptera. II. A time scale for fly evolution. J Mol Evol 21:1–13

    Google Scholar 

  • Beverley SM, Wilson AC (1985) Ancient origin for Hawaiian Drosophilinae inferred from protein comparisons. Proc Natl Acad Sci USA 82:4753–4757

    Google Scholar 

  • Bush GL, Kitto GB (1978) Application of genetics to insect systematics and analysis of species differences. In: Romberger JA, Foote RH, Knutson L, Lentz PD (eds) Beltsville symposia in agricultural research, vol 2. Wiley, New York, pp 89–118

    Google Scholar 

  • Buth DG (1984) The application of electrophoretic data i systematic studies. Annu Rev Ecol Syst 15:501–522

    Google Scholar 

  • Collier GE, MacIntyre RJ (1977) Microcomplement fixation studies on the evolution of α-glycerophosphate dehydrogenase within the genusDrosophila. Proc Natl Acad Sci USA 74:684–688

    Google Scholar 

  • Coulthart MB (1986) Variation and evolution in proteins of theDrosophila male reproductive tract. Thesis, McMaster University, Hamilton, Ontario

    Google Scholar 

  • Coyne JA, Eanes WF, Ramshaw JAM, Koehn RK (1979) Electrophoretic heterogeneity of α-glycerophosphate dehydrogenase among many species ofDrosophila. Syst Zool 28:164–175

    Google Scholar 

  • Cracraft J (1983) Cladistic analysis and vicariance biogeography. Am Sci 71:273–281

    Google Scholar 

  • Dickerson RE (1971) The structure of cytochrome c and the rates of molecular evolution. J Mol Evol 1:26–45

    Google Scholar 

  • Duke EJ, Glassman E (1968) Evolution of xanthine dehydrogenase inDrosophila. Genetics 58:101–112

    Google Scholar 

  • Entingh TD (1970) DNA hybridization in the genusDrosophila. Genetics 66:55–68

    Google Scholar 

  • Farris JS (1972) Estimating phylogenetic trees from distance matrices. Am Nat 106:645–668

    Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Google Scholar 

  • Fine RE, Blitz AL (1975) A chemical comparison of tropomyosins from muscle and non-muscle tissues. J Mol Biol 95:447–454

    Google Scholar 

  • Firtel RA (1981) Multigene families encoding actin and tubulin. Cell 24:6–7

    Google Scholar 

  • Fitch WM (1976) Molecular evolutionary clocks. In: Ayala FJ (ed) Molecular evolution. Sinauer, Sunderland MA, pp 160–178

    Google Scholar 

  • Fyrberg EA (1984) Structural and functional analyses ofDrosophila melanogaster actin genes. In: Maclean N (ed) Oxford surveys of eukaryotic genes. Oxford University Press, Oxford, pp 61–86

    Google Scholar 

  • Fyrberg EA, Kindle KL, Davidson N (1980) The actin genes ofDrosophila: a dispersed multigene family. Cell 19:365–378

    Google Scholar 

  • Fyrberg EA, Mahaffey JW, Bond BJ, Davidson N (1983) Transcripts of the sixDrosophila actin genes accumulate in a stageand tissue-specific manner. Cell 33:115–123

    Google Scholar 

  • Goodman M (1976) Protein sequences in phylogeny. In: Ayala FJ (ed) Molecular evolution. Sinauer, Sunderland MA, pp 141–159

    Google Scholar 

  • Goodman M (1981) Decoding the pattern of protein evolution. Prog Biophys Mol Biol 37:105–164

    Google Scholar 

  • Hennig W (1966) Phylogenetic systematics. University of Illinois Press, Urbana, p 263

    Google Scholar 

  • Hightower RC, Meagher RB (1986) The molecular evolution of actin. Genetics 114:315–332

    Google Scholar 

  • Hillis DM (1985) Evolutionary genetics of the Andean lizard genusPholidobolus (Sauria: Gymnophthalmidae): phylogeny, biogeography, and a comparison of tree construction techniques. Syst Zool 34:109–126

    Google Scholar 

  • Hillis DM, Frost JS, Wright DA (1983) Phylogeny and biogeography of theRana pipiens complex: a biochemical evaluation. Syst Zool 32:132–143

    Google Scholar 

  • Honeycutt RL, Williams SL (1982) Genic differentiation in pocket gophers of the genusPappogeomys, with comments on intergeneric relationships in the subfamily Geomyinae. J Mammal 63:208–217

    Google Scholar 

  • Jungblut P, Klose J (1985) Genetic variability of proteins from mitochondria and mitochondrial fractions of mouse organs. Biochem Genet 23:227–245

    Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge, p 367

    Google Scholar 

  • Klose J (1982) Genetic variability of soluble proteins studied by two-dimensional elecrophoresis on different inbred mouse strains and on different mouse organs. J Mol Evol 18:315–328

    Google Scholar 

  • Klose J, Feller M (1981) Genetic variability of proteins from plasma membranes and cytosols of mouse organs. Biochem Genet 19:859–870

    Google Scholar 

  • Lanyon SM (1985) Molecular perspective on higher-level relationships in the Tyrannoidea (Aves). Syst Zool 34:404–418

    Google Scholar 

  • Lee TJ, Pak JH (1986) Biochemical phylogeny of theDrosophila auraria complex. Drosophila Inf Serv 63:81

    Google Scholar 

  • Leigh Brown AJ, Langley CH (1979) Reevaluation of level of genic heterozygosity in natural population ofDrosophila melanogaster by two-dimensional electrophoresis. Proc Natl Acad Sci USA 76:2381–2384

    Google Scholar 

  • Lundberg JG (1972) Wagner networks and ancestors. Syst Zool 18:1–32

    Google Scholar 

  • MacIntyre RJ, Collier GE (1986) Protein evolution in the genusDrosophila. In: Ashburner M, Carson HL, Thompson JN (eds) The genetics and biology ofDrosophila, vol 3e. Academic Press, London, pp 39–146

    Google Scholar 

  • MacIntyre RJ, Dean MR (1978) Evolution of acid phosphatase-1 in the genusDrosophila as estimated by subunit hybridization. Interspecific tests. J Mol Evol 12:143–171

    Google Scholar 

  • MacIntyre RJ, Dean MR, Batt G (1978) Evolution of acid phosphatase-1 in the genusDrosophila. Immunological studies. J Mol Evol 12:121–142

    Google Scholar 

  • Matson RH (1984) Applications of electrophoretic data in avian systematics. Auk 101:717–729

    Google Scholar 

  • Maxson LR, Maxson RD (1979) Comparative albumin and biochemical evolution in plethodontid salamanders. Evolution 33:1057–1062

    Google Scholar 

  • McLellan T, Inouye LS (1986) The sensitivity of isoelectric focusing and electrophoresis in the detection of sequence differences in proteins. Biochem Genet 24:571–577

    Google Scholar 

  • McLellan T, Ames GF, Kikaido K (1983) Genetic variation in proteins: comparison of one-dimensional and two-dimensional gel electrophoresis. Genetics 104:381–390

    Google Scholar 

  • Mickevich MF (1978) Taxonomic congruence. Syst Zool 27:143–158

    Google Scholar 

  • Mickevich MF, Johnson MS (1976) Congruence between morphological and allozyme data in evolutionary inference and character evolution. Syst Zool 25:260–270

    Google Scholar 

  • Mickevich MF, Mitter C (1981) Treating polymorphic characters in systematics: a phylogenetic treatment of electrophoretic data. In: Funk VA, Brooks DR (eds) Advances in cladistics. New York Botanical Garden, New York, pp 45–58

    Google Scholar 

  • Miyamoto MM (1981) Congruence among character sets in phylogenetic studies of the frog genusLeptodactylus. Syst Zool 30:281–290

    Google Scholar 

  • Mogmi K, Fujita SC, Hotta Y (1982) Identification ofDrosophila indirect flight muscle myofibrillar proteins by means of two-dimensional electrophoresis. J Biochem 91:643–650

    Google Scholar 

  • Neel JV, Baier L, Hanash S, Erickson RP (1985) Frequency of polymorphisms for alleles encoding for liver proteins of domesticated mice. J Hered 76:314–320

    Google Scholar 

  • Nei M (1972) Genetic distances between populations. Am Nat 106:283–292

    Google Scholar 

  • Nevo E (1978) Genetic variation in natural populations: patterns and theory. Theor Pop Biol 13:121–177

    Google Scholar 

  • O'Brien SJ, MacIntyre RJ (1978) Genetics and biochemistry of enzymes and specific proteins ofDrosophila. In: Ashburner M, Wright TRF (eds) The genetics and biology ofDrosophila, vol 2a. Academic Press, London, pp 395–551

    Google Scholar 

  • O'Farrell PH (1975) High resolution two-dimensional electrophoresis. J Biol Chem 250:4007–4021

    Google Scholar 

  • Ohnishi S, Leigh Brown AJ, Voelker RA, Langley CH (1982) Estimation of genetic variability in natural populations ofDrosophila simulans by two-dimensional and starch gel electrophoresis. Genetics 100:127–136

    Google Scholar 

  • Ohnishi S, Kawanishi M, Watanabe TK (1983a) Biochemical phylogenies ofDrosophila: protein differences detected by twodimensional electrophoresis. Genetica 61:55–63

    Google Scholar 

  • Ohnishi S, Kim K, Watanabe TK (1983b) Biochemical phylogeny of theDrosophila montium species subgroup. J Jpn Genet 58:141–151

    Google Scholar 

  • Patton JC, Avise JC (1983) An empirical evaluation of qualitative Hennigian analyses of protein electrophoretic data. J Mol Evol 19:244–254

    Google Scholar 

  • Powell JR (1975) Protein variation in natural populations of animals. Evol Biol 8:79–119

    Google Scholar 

  • Rohlf FJ (1982) Consensus indices for comparing classifications. Math Biosci 59:131–144

    Google Scholar 

  • Rohlf FJ, Kishpaugh J, Kirk D (1981) Numerical taxonomy system of multivariate statistical programs (NT-SYS). State University of New York, Stony Brook

    Google Scholar 

  • Sarich VM (1977) Electrophoresis in evolutionary studies: rates, sample sizes, and the neutrality hypothesis. Nature 265:24–28

    Google Scholar 

  • Sites JW, Greenbaum IF, Bickham JW (1981) Biochemical systematics of neotropical turtles of the genusRhinoclemmys (Emydidae: Batagurinae). Herpetologica 37:256–264

    Google Scholar 

  • Sites JW, Bickham JW, Pytel BA, Greenbaum IF, Bates BA (1984) Biochemical characters and the reconstruction of turtle phylogenies: relationships among batagurine genera. Syst Zool 33:137–158

    Google Scholar 

  • Skibinski DOF, Ward RD (1981) Relationship between allozyme heterozygosity and rates of divergence. Genet Res 38:71–92

    Google Scholar 

  • Skibinski DOF, Ward RD (1982) Correlations between heterozygosity and evolutionary rate of proteins. Nature 298:490–492

    Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy. WH Freeman, San Francisco, p 573

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Taxonomic congruence in the Leptopodomorpha re-examined. Syst Zool 30:309–325

    Google Scholar 

  • Sokal RR, Sneath PHA (1963) Principles of numerical taxonomy. WH Freeman, San Francisco, p 359

    Google Scholar 

  • Spicer GS (1985) Systematics of theDrosophila virilis species group as assessed by two-dimensional electrophoresis. Thesis, Texas Tech University, Lubbock

    Google Scholar 

  • Storti RV, Horovitch SJ, Scott MP, Rich A, Pardue ML (1978) Myogenesis in primary cell cultures fromDrosophila melanogaster: protein synthesis and actin heterogeneity during development. Cell 13:589–598

    Google Scholar 

  • Swofford DL (1982) Consensus tree program (CONTREE) for ANSII standard Fortran 77. Illinois Natural History Survey, Champaign

    Google Scholar 

  • Swofford DL (1984) Phylogenetic analysis using parsimony (ver 2.3.1). Illinois Natural History Survey, Champaign

    Google Scholar 

  • Takahata N, Nei M (1985) Gene genealogy and variance of interpopulational nucleotide differences. Genetics 110:325–344

    Google Scholar 

  • Thorpe JP (1982) The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. Annu Rev Syst Ecol 13:139–168

    Google Scholar 

  • Throckmorton LH (1962) The problem of phylogeny in the genusDrosophila. Univ Tex Publ 6205:207–343

    Google Scholar 

  • Throckmorton LH (1969) Concordance and discordance of taxonomic characters inDrosophila classification. Syst Zool 17:355–387

    Google Scholar 

  • Throckmorton LH (1975) The phylogeny, ecology and geography ofDrosophila. In: King RC (ed) Handbook of genetics, vol 3. Plenum, New York, pp 421–469

    Google Scholar 

  • Throckmorton LH (1978) Molecular phylogenetics. In: Romberger JA, Foote RH, Knutson L, Lentz PD (eds) Beltsville symposia in agricultural research, vol 2. Wiley, New York, pp 221–239

    Google Scholar 

  • Throckmorton LH (1982) Pathways of evolution in the genuDrosophila and the founding of therepleta group. In: Barker JFS, Starmer WT (eds) Ecological genetics and evolution. Academic Press, Australia, pp 33–47

    Google Scholar 

  • Tobin SL, Zulauf E, Sanchez F, Craig EA, McCarthy BJ (1980) Multiple actin-related sequences in theDrosophila melanogaster genome. Cell 19:121–131

    Google Scholar 

  • Tollaksen SL, Anderson NL, Anderson NG (1984) Operation of the ISO-DALT system, ed 7. Argonne National Laboratory Report Publ ANL-BIM-84-1, Argonne National Laboratory, Argonne IL

    Google Scholar 

  • Vilageliu L, Gonzalez-Duarte R (1984) Alcohol dehydrogenase fromDrosophila funebris andDrosophila immigrans: molecular and evolutionary aspects. Biochem Genet 22:797–815

    Google Scholar 

  • Wake DB, Maxson LR, Wurst GZ (1978) Genetic differentiation, albumin evolution, and their biogeographic implications in plethodontid salamanders of California and southern Europe. Evolution 32:529–539

    Google Scholar 

  • Watterson GA (1985) Estimating species divergence times using multi-locus data. In: Ohta T, Aoki K (eds) Population genetics and molecular evolution. Springer-Verlag, Berlin, pp 163–183

    Google Scholar 

  • Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    Google Scholar 

Download references

Author information

Author notes

  1. Greg S. Spicer

    Present address: Linus Pauling Institute, 440 Page Mill Road, 94306, Palo Alto, California, USA

Authors and Affiliations

  1. Division of Biological and Medical Research, Argonne National Laboratory, 60439, Argonne, Illinois, USA

    Greg S. Spicer

  2. Committee on Evolutionary Biology, University of Chicago, 60637, Chicago, Illinois, USA

    Greg S. Spicer

Authors
  1. Greg S. Spicer
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spicer, G.S. Molecular evolution among someDrosophila species groups as indicated by two-dimensional electrophoresis. J Mol Evol 27, 250–260 (1988). https://doi.org/10.1007/BF02100081

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02100081

Key words

Search

Navigation