Journal of Molecular Evolution

, Volume 33, Issue 4, pp 379–394 | Cite as

Molecular evolution and phylogeny of theDrosophila virilis species group as inferred by two-dimensional electrophoresis

  • Greg S. Spicer
Article

Summary

Systematic relationship among the 12 species of theDrosophila virilis species group, andDrosophila robusta, were investigated by the use of two-dimensional electrophoresis (2-DE). A total of 389 protein characters (about 200 loci) were scored and analyzed both phylogenetically and phenetically. The resulting phylogeny was found to be largely concordant with the current views of evolution among these species based on other independent morphological, chromosomal, electrophoretic, and immunological data sets, although some notable differences were observed. The 2-DE data also appeared to be useful for constructing a molecular clock to date the absolute times of divergence among the species. It appears from this analysis that the evolution of the major clades within the species group occurred about 20 million years ago. Previous suggestions that the rate of molecular evolution was different between the virilis and montana phylads was not confirmed. The technique of 2-DE seems to be an excellent tool for reconstructing phylogenies and should be particularly valuable for examining relatively closely related species.

Key words

Drosophila systematics Two-dimensional electrophoresis Phylogenetic analysis Molecular clock 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson NG, Anderson NL (1978a) Analytical techniques for cell fractions. XXI. Two-dimensional analysis of serum and tissue proteins: multiple isoelectric focusing. Anal Biochem 85:331–340PubMedGoogle Scholar
  2. Anderson NL (1988) Two-dimensional electrophoresis. Operation of the ISO-DALT system. Large Scale Biology Press, Washington DC, p 162Google Scholar
  3. 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 85:341–354PubMedGoogle Scholar
  4. Aquadro CF, Avise JC (1981) Genetic divergence between rodent species assessed by using two-dimensional electrophoresis. Proc Natl Acad Sci USA 78:3784–3788PubMedGoogle Scholar
  5. Avise JC (1983) Protein variation and phylogenetic reconstruction. In: Oxford GS, Rollinson D (eds) Protein polymorphism: adaptive and taxonomic significance. Academic Press, London, pp 103–130Google Scholar
  6. Avise JC (1985) Systematic value of electrophoretic data. Syst Zool 23:465–481Google Scholar
  7. Ayala FJ (1986) On the virtues and pitfalls of the molecular evolutionary clock. J Hered 77:226–235PubMedGoogle Scholar
  8. Baverstock PR, Cole SR, Richardson BJ, Watts CHS (1979) Electrophoresis and cladistics. Syst Zool 28:214–219Google Scholar
  9. 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 18:251–264PubMedGoogle Scholar
  10. Beverley SM, Wilson AC (1984) Molecular evolution inDrosophila and the higher Diptera. I. A time scale for fly evolution. J Mol Evol 21:1–13PubMedGoogle Scholar
  11. Coyne JA, Orr HA (1989) Patterns of speciation inDrosophila. Evolution 43:362–381Google Scholar
  12. DeSalle R, Freedman T, Prager EM, Wilson AC (1987) Tempo and mode of sequence evolution in mitochondrial DNA of HawaiianDrosophila. J Mol Evol 26:157–164PubMedGoogle Scholar
  13. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791Google Scholar
  14. Goldman D, Giri PR, O'Brien SJ (1987) The phylogeny of the hominoid primates as indicated by two-dimensional electrophoresis. Proc Natl Acad Sci USA 84:3307–3311PubMedGoogle Scholar
  15. Goldman D, Giri PR, O'Brien SJ (1989) Molecular genetic-distance estimates among the Ursidae as indicated by one- and two-dimensional protein electrophoresis. Evolution 43: 282–295Google Scholar
  16. Grimaldi DA (1990) A phylogenetic, revised classfication of genera in the Drosophilidae (Diptera). Bull Am Mus Nat Hist 197:1–139Google Scholar
  17. Guevara J, Johnston DA, Ramagali LS, Martin BA, Capetillo S, Rodriguez LS (1982) Quantitative aspects of silver deposition in proteins resolved in complex polyacrylamide gels. Electrophoresis 3:197–205Google Scholar
  18. Hendy MD, Penny D (1982) Branch and bound algorithms to determine minimal evolutionary trees. Math Biosci 59:277–290Google Scholar
  19. Hubby JL, Throckmorton LH (1965) Protein differences inDrosophila. II. Comparative species genetics and evolutionary problems. Genetics 52:203–215Google Scholar
  20. Imajoh S (1981) Application of two-dimensional electrophoresis to the analysis of speciation inAnopheles hyrcanus complex. Seikagaku (Biochemistry) 53:159–164 [in Japanese]Google Scholar
  21. Lanyon SM (1988) The stochastic mode of molecular evolution: what consequences for systematic investigations? Auk 105:565–573Google Scholar
  22. Lee TJ, Pak JH (1986) Biochemical phylogeny of theDrosophila auroria complex. Drosophila Inform Serv 63:81Google Scholar
  23. Lee WH, Watanabe TK (1987) Evolutionary genetics of theDrosophila melanogaster subgroup. I. Phylogenetic relationships based on matings, hybrids and proteins. Jpn J Genet 62:225–239Google Scholar
  24. Lundberg JG (1972) Wagner networks and ancestors. Syst Zool 18:1–32Google Scholar
  25. Margush T, McMorris FR (1981) Consensus n-trees. Bull Math Biol 43:239–244Google Scholar
  26. Mickevich MF, Johnson MS (1976) Congruence between morphological and allozyme data in evolutionary inference and character evolution. Syst Zool 25:260–270Google Scholar
  27. 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. Allen Press, Lawrence KS, pp 45–58Google Scholar
  28. Nei M (1971) Interspecific gene differences and evolutionary time estimated from electrophoretic data on protein identity. Am Nat 105:385–398Google Scholar
  29. Nei M (1972) Genetic distances between populations. Am Nat 106:283–292Google Scholar
  30. O'Farrell PH (1975) High resolution two-dimensional electrophoresis. J Biol Chem 250:4007–4021PubMedGoogle Scholar
  31. Ohnishi S, Watanabe TK (1984) Systematics of theDrosophila montium species subgroup: a biochemical approach. Zool Sci (Japan) 1:801–807Google Scholar
  32. Ohnishi S, Kawanishi M, Watanabe TK (1983a) Biochemical phylogenies ofDrosophila: protein differences detected by two-dimensional electrophoresis. Genetica 61:55–63Google Scholar
  33. Ohnishi S, Kim K, Watanabe TK (1983b) Biochemical phylogeny of theDrosophila montium species subgroup. Jpn J Genet 58:141–151Google Scholar
  34. Ostrega MS (1985) Restriction endonuclease analysis of the relatedness ofD. montana andD. virilis line. Drosophila Inform Serv 61:132–133Google Scholar
  35. Patton JC, Avise JC (1983) An empirical evaluation of qualitative Hennigian analyses of protein electrophoretic data. J Mol Evol 19:244–254PubMedGoogle Scholar
  36. Reinbold SL, Collier GE (1990) Molecular systematics of theDrosophila virilis species group (Diptera, Drosophilidae). Ann Entomol Soc Am 83:467–474Google Scholar
  37. Rohlf FJ (1982) Consensus indices for comparing classifications. Math Biosci 59:131–144Google Scholar
  38. Rohlf FJ (1988) NTSYS-pc. Numerical taxonomy and multivariate analysis system (ver 1.40). Exeter Publications, Setauket NYGoogle Scholar
  39. Sanderson MJ (1989) Confidence limits on phylogenies: the bootstrap revisited. Cladistics 5:113–129Google Scholar
  40. Sneath PHA, Sokal RR (1973) Numerical taxonomy. WH Freeman, San Francisco, p 573Google Scholar
  41. Sokal RR, Rohlf FJ (1981) Taxonomic congruence in the Leptopodomorpha re-examined. Syst Zool 30:309–325Google Scholar
  42. Sokal RR, Sneath PHA (1963) Principles of numerical taxonomy. WH Freeman, San Francisco, p 359Google Scholar
  43. Spicer GS (1988a) Molecular evolution among someDrosophila species as indicated by two-dimensional electrophoresis. J Mol Evol 27:250–260PubMedGoogle Scholar
  44. Spicer GS (1988b) The separation of whale myoglobins with two-dimensional electrophoresis. Biochem Genet 26:645–655PubMedGoogle Scholar
  45. Spicer GS (1988c) The effects of culture media on the two-dimensional electrophoretic protein pattern ofDrosophila virilis. Drosophila Inform Serv 67:74–75Google Scholar
  46. Spicer GS (1990) TheDrosophila virilis species group: molecular evolution, phylogeny, morphological evolution, and evolutionary genetics. PhD Dissertation, University of Chicago, Chicago ILGoogle Scholar
  47. Spicer GS (1992) Reevaluation of the phylogeny of theDrosophila virilis species group (Drosophilidae: Diptera). Ann Entomol Soc Amer 85: in press.Google Scholar
  48. Spieth HT (1979) Thevirilis group ofDrosophila and the beaverCastor. Am Nat 114:312–316Google Scholar
  49. Swofford DL (1989) PAUP. Phylogenetic analysis using parsimony (ver 3.0d). Illinois Natural History Survey, Champaign ILGoogle Scholar
  50. Takai K, Kanda T (1986) Phylogenetic relationships among theAnopheles hyrcanus species group based on the degree of hybrid development and comparison with phylogenies by other methods. Jpn J Genet 61:295–314Google Scholar
  51. Thorpe JP (1982) The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. Annu Rev Syst Ecol 13:139–168Google Scholar
  52. Thorpe PA, Dickinson WJ (1988) The use of regulatory patterns in constructing phylogenies. Syst Zool 37:97–105Google Scholar
  53. Throckmorton LH (1975) The phylogeny, ecology and geography ofDrosophila. In: King RC (ed) Handbook of genetics, vol 3. Plenum, New York, pp 421–469Google Scholar
  54. Throckmorton LH (1977)Drosophila systematics and biochemical evolution. Annu Rev Ecol Syst 8:235–254Google Scholar
  55. Throckmorton LH (1978) Molecular phylogenetics. In: Romberger JA, Foote RH, Knutson L, Lentz PD (eds) Beltsville symposia in agricultural research, vol 2. John Wiley and Sons, New York, pp 221–239Google Scholar
  56. Throckmorton LH (1982) Thevirilis species group. In: Ashburner M, Novistky E (eds) The genetics and biology ofDrosophila, vol. 3B. Academic Press, London, pp 227–297Google Scholar
  57. Wake DB, Maxson LR, Wurst GZ (1978) Genetic differentiation, albumin evolution, and their biogeographic implications in plethodontid salamanders of California and southern Europe. Evolution 32:529–539Google Scholar
  58. Whitt GS (1987) Species differences in isozyme tissue patterns: their utility for systematic and evolutionary analysis. In: Rattazzi MC, Scandalios JG, Whitt GS (eds) Isozymes: current topics in biological and medical research, vol 10. Alan R Liss, New YorkGoogle Scholar
  59. Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1991

Authors and Affiliations

  • Greg S. Spicer
    • 1
    • 2
  1. 1.Linus Pauling Institute of Science and MedicinePalo Alto
  2. 2.Committee on Evolutionary BiologyUniversity of ChicagoChicagoUSA

Personalised recommendations