Summary
LHP is a suitable protein for studying evolution in flies (Diptera). This blood protein, which occurs at high concentration late in larval development, was purified to homogeneity from 5 species of Drosophilidae and one species each of Tephritidae and Calliphoridae. Rabbit antisera to the purified LHPs allowed immunological comparisons to be made with the micro-complement fixation technique. Various indirect tests indicated that immunological distance is a reliable estimator of the degree of amino acid sequence difference between LHPs from different species. An evolutionary tree for the 7 LHPs was constructed from the immunological distances with the method of Fitch and Margoliash (1967) to provide the branching order and the method of Chakraborty (1977) to provide the branch lengths. A modified method of tree construction allowed LHPs from 10 additional species to be attached to this tree. The resulting LHP tree for 17 species agrees approximately in branching order with that based on Throckmorton's study of 60 anatomical traits. However, the ratio of anatomical change to LHP change along branches within the tree varies widely, confirming the independence of organismal and molecular evolution. The LHP tree thus provides a new perspective on evolution within and among the families of higher Diptera.
Similar content being viewed by others
References
Akam ME, Roberts DB, Wolfe JE (1978)Drosophila hemolymph proteins: Purification, characterization and genetic mapping of larval serum protein 2 inD. melanogaster. Biochem Genet 16:101–119
Ames GF (1974) Resolution of bacterial proteins by polyacrylamide gel electrophoresis on slabs. J Biol Chem 249:634–644
Ashburner M, Novitski E (1976) The genetics and biology ofDrosophila. Academic Press, San Francisco
Ayala FJ (1975) Genetic differentiation during the speciation process. In: Evol Biol 8:1–78
Beverley SM (1979) Ph.D. Thesis, University of California, Berkeley. Dissert Abstr Int B 40:3127B, 1980
Beverley SM, Wilson AC (1977) Purification, characterization and immunological cross-reactivity of a hemolymph protein from Drosophila larvae. Fed Proc 36:927
Borror DJ, DeLong DM, Triplehorn CA (1976) An introduction to the study of insects. Holt, Rinehart and Winston, New York
Chakraborty R (1977) Estimation of time of divergence from phylogenetic studies. Can J Genet Cytol 19:217–223
Champion AB, Prager EM, Wachter D, Wilson AC (1974) Microcomplement fixation. In: Wright CA (ed) Biochemical and immunological taxonomy of animals. Academic Press, London, pp 397–416
Champion AB, Soderberg KL, Wilson AC, Ambler RP (1975) Immunological comparison of azurins of known amino acid sequence. J Mol Evol 5:291–305
Champion AB, Barrett EL, Palleroni NJ, Soderberg KL, Kunisawa R, Contopoulou R, Wilson AC, Doudoroff M (1980) Evolution inPseudomonas fluorescens. J Gen Microbiol 120:485–511
Collier GE, MacIntyre RJ (1977) Micro-complement fixation studies on the evolution of alpha-glycerophosphate dehydrogenase within the genus Drosophila. Proc Nat Acad Sci USA 74:684–688
Collier GE, MacIntyre RJ (1978) Quantitative subunit hybridization ofDrosophila alpha-glycerophosphate dehydrogenase. J Mol Evol 12:172–182
Davidson WS, Flynn TG (1980) Personal communication
Dayhoff MO (1972) Atlas of protein sequence and structure, National Biomedical Research Foundation, Silver Spring Md
Dickerson RE (1971) The structure of cytochrome C and the rate of molecular evolution. J Mol Evol 1:26–45
Duke EJ, Glassman E (1968) Evolution of xanthine dehydrogenase in Drosophila. Genetics 58:101–112
Farris JS (1979) Review of Biosystematics in Agriculture, by Romberger RA, Foote RH, Knutson L, Lentz PL (eds) John Wiley and Sons, New York 1978. Syst Zool 28:239–243
Fink SC, Carlson CW, Gurusiddaiah S, Brosemer RW (1970) Glycerol 3-phosphate dehydrogenase in social bees. J Biol Chem 245:6525–6532
Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–84
Gehring WJ (1978) Insect molecular biology on Crete. Nature 275:364–366
Griffiths GCD (1972) The phylogenetic classification ofDiptera cyclorrhapha. Dr. W. Junk, The Hague, Netherlands
Hennig W (1973) Diptera, in Handbuch der Zoologie, IV: Arthropoda. De Gruyter, New York
Hubby JL (1963) Protein differences inDrosophila, I:Drosophila melanogaster. Genetics 48:871–879
Ibrahimi IM, Prager EM, White TJ, Wilson AC (1979) Amino acid sequence of California quail lysozyme: Effects of evolutionary substitutions on the antigenic structure of lysozyme. Biochemistry 13:2736–2744
Kinnear JF, Thomson JA (1975) Nature, origin and fate of major hemolymph proteins in Calliphora. Insect Biochem 5:531–552
Kunkel JG, Lawler DM (1974) Larval-specific serum protein in the order Dictyoptera — I. Immunologic characterization in larvalBlatella germanica and cross-reaction throughout the order. Comp Biochem Physiol 47B:697–710
Lewontin RC (1974) The genetic basis of evolutionary change. Columbia University Press, New York
MacIntyre RJ, Dean MR, Batt G (1978) Evolution of acid phosphatase-1 in the genusDrosophila. Immunological studies. J Mol Evol 12:121–142
Marchalonis JJ, Weltman JK (1971) Relatedness of proteins: A new method of estimation and its application to immunoglobulins. Comp Biochem Physiol 38B:609–625
Maurer HR (1971) Disc electrophoresis and related techniques of polyacrylamide gel electrophoresis. De Gruyter, Berlin
Maxson LR, Wilson AC (1975) Albumin evolution and organismal evolution in tree frogs (Hylidae). Syst Zool 24:1–15
Mayer MM (1961) In: Kabat EA, Mayer MM (eds) Experimental immunochemistry. Charles Thomas, Springfield, Ill
Metzger H, Shapiro MB, Mosimann JE, Vinton JE (1968) Assessment of compositional relatedness of proteins. Nature 219:1166–1168
Munn EA, Feinstein A, Greville GD (1971) The isolation and properties of the protein Calliphorin. Biochem J 124:367–74
Nakanishi M (1971) Albumin evolution in birds and crocodilians. Master's thesis, University of California, Berkeley
Oldroyd H (1964) The natural history of flies. W.W. Norton, New York
Prager EM, Wilson AC (1971a) The dependence of immunological cross-reactivity upon sequence resemblence among lysozymes. I: Micro-complement fixation studies. J Biol. Chem. 246:5978–5989
Prager EM, Wilson AC (1971b) The dependence of immunological cross-reactivity upon sequence resemblance among lysozymes. II: comparison of precipitin and micro-complement fixation results. J Biol Chem 246:7010–1017
Prager EM, Wilson AC (1976) Congruency of phylogenies derived from different proteins. J Mol Evol 9:45–57
Prager EM, Wilson AC (1978) Construction of phylogenetic trees for proteins and nucleic acids: empirical evaluation of alternative matrix methods. J Mol Evol 11:129–142
Prager EM, Brush AH, Nolan RA, Nakanishi M, Wilson AC (1974) Slow evolution of transferrin and albumin in birds according to micro-complement fixation analysis. J Mol Evol 3:243–262
Prager EM, Fowler DP, Wilson AC (1976) Rates of evolution in conifers (Pinaceae). Evolution 30:637–648
Prager EM, Welling GW, Wilson AC (1978) Comparison of various immunological methods for distinguishing among mammalian pancreatic ribonucleases of known amino acid sequence. J Mol Evol 10:293–307
Prager EM, Wilson AC, Perin J-P, Jolles P (1978) Further studies of an anomalous cross-reaction involving worm and vertebrate lysozymes. Immunochemistry 15:577–583
Putnam FW (1975) The plasma proteins. Academic Press, New York, Chapters 1, 2, and 6
Rapp JH, Borsos T (1970) The molecular basis of complement action. Appleton-Century-Crofts, New York
Reichlin M, Nisonoff A, Margoliash E (1970) Immunological activity of cytochrome c, III: Enhancement of antibody detection and immune response initiation by cytochrome polymers. J Biol Chem 245:947–954
Roberts DB, Wolfe J, Akam ME (1977) The developmental profiles of two major hemolymph proteins fromD. melanogaster. J Insect Physiol 23:871–878
Rohdendorf B (1974) The historical development of Diphtera. University of Alberta Press, Canada
Sarich VM, Wilson AC (1966) Quantitative immunochemistry and the evolution of primate albumins: micro-complement fixation. Science 154:1563–1566
Sarich VM, Cronin JE (1976) Molecular Systematics of the Primates. In: Goodman M, Tashian R (eds) Molecular Anthropology. Plenum Press, New York, pp 141–170
Steyskal GC (1974) Recent advances in the primary classification of the Diptera. Ann Ent Soc Amer 67:513–517
Thomson JA (1975) Major patterns of gene activity during development in holometabolous insects. Adv Insect Physiol 11:321–398
Thomson JA, Radok KR, Shaw DC, Whitten MJ, Foster GG, Birt LM (1976) Genetics of lucilin, a storage protein from the sheep blowflyLucilia cuprina. Biochem Genet 14:145–160
Throckmorton LH (1962) The problem of phylogeny in the genus Drosophila. In: Wheeler MR (ed) Studies in genetics. University of Texas Press Austin, 2:207–343
Throckmorton LH (1968) Concordance and discordance of taxonomic characters in Drosophila classification. Syst Zool 17:355–387
Throckmorton LH (1975) The phylogeny, ecology and geography ofDrosophila. In: King RC (ed) Handbook of genetics 3:421–469
Throckmorton LH (1978) Molecular phylogenetics. In: Romberger, RA, Foote RH, Knutson L, Lentz PL (eds) Beltsville Symposia II: Biosystematics in agriculture. John Wiley and Sons, New York, pp 221–240
Wallace DG, Boulter D (1976) Immunological comparisons of higher plant plastocyanins. Phytochemistry 15:137–141
Wallace, DG, Wilson AC (1972) Comparison of frog albumins with other verterates. J Mol Evol 2:72–86
White TJ, Ibrahimi IM, Wilson AC (1978) Evolutionary substitutions and the antigenic structure of globular proteins. Nature 274:92–94
Williams CA, MW Chase (1971) Methods in immunology and immunochemistry. Vol III, Academic Press, New York
Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Ann Rev Biochem 46:573–639
Wolfe J, Akam ME, Roberts DB (1977) Biochemical and immunological studies on larval serum protein 1, the major hemolymph protein ofD. melanogaster third-instar larvae. Eur J Biochem 79:47–53
Wyatt GR, Pan MD (1978) Insect plasma proteins. Ann Rev Biochem 47:779–817
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Beverley, S.M., Wilson, A.C. Molecular evolution inDrosophila and higher diptera. J Mol Evol 18, 251–264 (1982). https://doi.org/10.1007/BF01734103
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01734103