Summary
In this paper, we examine first the steadiness of the rate of evolutionary change in a larval hemolymph protein, LHP, in numerousDrosophila species. We estimated amino acid sequence divergence from immunological distances measured with the quantitative microcomplement fixation technique. Using tests not depending on knowledge of absolute times of divergence, we estimated the variance of the rate of evolutionary change to be at least 4 times as large as that for a process resembling radioactive decay. Thus, the rate of evolution of this protein is as uniform as that of vertebrate proteins. Our analysis indicates no acceleration of protein evolution in the lineages leading to Hawaiian drosophilines. Second, we give an explicit description of a procedure for calculating the absolute value of the mean rate of evolutionary change in this protein. This procedure is suggested for general use in calculating absolute rates of molecular evolution. The mean rate of evolution of LHP is about 1.2 immunological distance units per million years, which probably coreesponds to a unit evolutionary period of 4 million years; LHP thus evolves at a rate comparable to that of mammalian hemoglobins. Finally, we utilize the calibrated rate of LHP evolution to derive a time scale of evolution in the Drosophilidae and higher Diptera.
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References
Akam ME, Roberts DB, Wolfe JE (1978a)Drosophila hemolymph proteins: purification, characterization and genetic mapping of larval serum protein 2 inD. melanogaster. Biochem Genet 16:101–119
Akam ME, Roberts DB, Richards GP, Ashburner M (1978b)Drosophila: the genetics of two major larval proteins. Cell 13: 215–225
Alvarez LW (1983) Experimental evidence that an asteroid impact led to the extinction of many species 65 million years ago. Proc Natl Acad Sci USA 80:627–642
Ayala FJ (1975) Genetic differentiation during the speciation process. Evol Biol 8:1–78
Benjamin DC, Berzofsky JA, East IJ, Gurd FRN, Hannum C, Leach SJ, Margoliash E, Michael JG, Miller A, Prager EM, Reichlin M, Sercarz EE, Smith-Gill SJ, Todd PE, Wilson AC (1984) The antigenic structure of proteins: a reappraisal. Annu Rev Immunol 2:67–101
Beverley SM (1977) Purification, characterization and immunological cross-reactivity of a hemolymph protein fromDrosophila larvae. Fed Proc 36:927
Beverley SM (1979) Molecular evolution inDrosophila. Ph.D. thesis, University of California, Berkeley
Beverley SM (1980) A molecular view of the age and origin of the HawaiianDrosophila. In: Abstracts of the Second International Congress of Systematic and Evolutionary Biology, Vancouver
Beverley SM, Wilson AC (1982) Molecular evolution inDrosophila and higher Diptera. I. micro-complement fixation studies of a larval hemolymph protein. J Mol Evol 18:251–264
Bisbee, A, Baker MA, Wilson AC, Hadji-Azimi T, Fischberg M (1977) Albumin phylogeny for clawed frogs (Xenopus). Science 195:785–787
Bock I, Wheeler MR (1972) TheDrosophila melanogaster species group. In: Wheeler MR (ed) Studies in genetics, vol. 7. University of Texas, Austin, pp 1–102
Borror DJ, DeLong DM, Triplehorn CA (1976) An introduction to the study of insects. Holt, Rinehart & Winston, New York
Bruce EJ, Ayala FJ (1979) Phylogenetic relationships between man and the apes: electrophoretic evidence. Evolution 33: 1040–1056
Carlson SS (1975) The evolution of mouse and rat cytochromesc. Ph.D. thesis, University of California, Berkeley
Carlson SS, Wilson AC, Maxson RD (1978) Do albumin clocks run on time? Science 200:1183–1185
Carson HL (1976) Inference of the time of divergence of someDrosophila species. Nature 259:395–396
Carson HL, Kaneshiro KY (1976)Drosophila of Hawaii: systematics and ecological genetics. Annu Rev Ecol Syst 7:311–345
Carson HL, Hardy DE, Spieth HT, Stone WS (1970) The evolutionary biology of the Hawaiian Drosophilidae. In: Hecht MK, Steere WC (eds) Essays on evolution and genetics in honor of Theodosius Dobzhansky. Appleton-Century-Crofts, New York, pp 437–543
Champion AB, Soderberg KL, Wilson AC, Ambler RP (1975) Immunological comparison of azurins of known amino acid sequence: dependence of cross-reactivity upon sequence resemblance. 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
Cohn VH, Thompson MA, Moore GP (1984) Nucleotide sequence comparison of the Adh gene in three Drosophilids. J Mol Evol 20:31–37
Collier GE, MacIntyre RJ (1977) Micro-complement fixation studies on the evolution of alpha-glycerophosphate dehydrogenase within the genusDrosophila. Proc Natl Acad Sci USA 74:684–688
Cracraft J (1974) Continental drift, paleoclimatology, and the evolution and biogeography of birds. J Zool 169:455–545
Dalrymple GB, Silver EA (1973) Origin of the Hawaiian islands. Am Sci 61:294–308
Dickerson RE (1971) The structure of cytochrome c and the rate of molecular evolution. J Mol Evol 1:26–45
Dobzhansky T, Ayala FJ, Stebbins GL, Valentine JW (1977) Evolution. WH Freeman, San Francisco, pp 308–313
Fitch WM (1980) Estimating the total number of nucleotide substitutions since the common ancestor of a pair of homologous genes: comparison of several methods and three betahemoglobin messenger RNAs. J Mol Evol 16:153–204
Fitch WM, Margoliash E (1970) The usefulness of amino acid and nucleotide sequences in evolutionary studies. Evol Biol 4:67–109
Fitch WM, Markowitz E (1970) An improved method for determining codon variability and its application to the rate of fixation of mutations in evolution. Biochem Genet 4:579–593
Gillespie JH, Langley CH (1979) Are evolutionary rates really variable? J Mol Evol 13:27–34
Gribbin JR, Cherfas J (1982) The monkey puzzle. Pantheon Books, New York, p 127
Harrison RA (1959) Acalypterate Diptera of New Zealand. NZ Dept Sci Ind Res Bull 128:1–382
Hennig W (1960) Die Dipteren-Fauna von Neuseeland als systematisches und tiergeographisches Problem. Beitr Entomol 10:221–329
Hennig W (1973) Diptera. In Kukenthal W (ed): Handbuch der Zoologie, IV: Arthropoda. de Gruyter, New York, pp 1–377
Hubby JL (1963) Protein differences inDrosophila, I:Drosophila melanogaster. Genetics 48:871–879
Hunt JA, Hall TJ, Britten RJ (1981) Evolutionary distances in HawaiianDrosophila measured by DNA reassociation. J Mol Evol 17:365–367
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 18:2736–2744
Kimura M (1979) Model of effectively neutral mutations in which selective constraint is incorporated. Proc Natl Acad Sci USA 76:3440–3444
Kumura M, Ohta T (1971) On the rate of molecular evolution. J Mol Evol 1:1–17
King M-C, Wilson AC (1975) Evolution at two levels in humans and chimpanzees. Science 188:107–116
Laird CD, McCarthy BJ (1968) Magnitude of interspecific nucleotide sequence variability inDrosophila. Genetics 60:303–322
Langley CH, Fitch WM (1974) An examination of the constancy of the rate of molecular evolution. J Mol Evol 3:161–167
MacDonald GA, Abbott AT (1970) Volcanoes in the sea. In: The geology of Hawaii. University of Hawaii Press, Honolulu, pp 3–7; 263–285
Maxson LR, Wilson AC (1975) Relation between albumin evolution and organismal evolution in treefrogs (Hylidae). Syst Zool 24:1–15
McAlpine JF (1970) First record of calypterate flies in the Mesozoic era. Entomol 102:342–346
McAlpine JF (1973) A fossil ironomyiid fly from Canadian amber. Can Entomol 105:105–111
McAlpine JF, Martin JEH (1966) Systematics of Sciadoceridae and relations with descriptions of two new genera from Ca-nadian amber and erection of family Ironomyiidae. Can Entomol 99:225–236
Munn EA, Greville GD (1969) The soluble proteins of developingCalliphora erythrocephala, particularly calliphorin, and similar proteins in other insects. J Insect Physiol 15:1935–1950
Nei M (1971) Interspecific gene differences and evolutionary time estimated from electrophoretic data on protein identity. Am Nat 105:385–398
Nei M (1975) Molecular population genetics and evolution. North-Holland, Amsterdam
Nei M (1977) Standard error of immunological dating of evolutionary time. J Mol Evol 9:203–211
Nei M, Graur D (1984) Extent of protein polymorphism and the neutral mutation theory. Evol Biol 17 (in press)
Nozawa K, Shotake T, Kawamoto Y, Tanabe Y (1982) Electrophoretically estimated genetic distance and divergence time between chimpanzee and man. Primates 23:432–443
O'Brien SJ, MacIntyre RJ (1969) An analysis of gene-enzyme variability in natural populations ofDrosophila melanogaster andD. simulans. Am Nat 103:97–103
Ohta T (1976) Role of very slightly deleterious mutations in molecular evolution. Theor Popul Biol 10:254–275
Patrusky B (1979) Molecular evolution: a quantifiable contribution. Mosaic 10:12–22
Patterson JT, Stone WS (1952) Evolution in the genusDrosophila. Macmillan, New York
Prager CM, Wilson AC (1971) The dependence of immunological cross-reactivity upon sequence resemblance among lysozymes. I: Micro-complement fixation studies. J Biol Chem 246:5978–5989
Prager EM, Wilson AC (1976) Congruency of phylogenies derived from different proteins. J Mol Evol 9:45–57
Prager EM, Fowler DP, Wilson AC (1976) Rates of evolution in conifers (Pinaceae). Evolution 30:637–649
Roberts DB, Wolfe J, Akam M (1977) The developmental profile of two major haemolymph proteins fromDrosophila melanogaster. J Insect Physiol 23:871–878
Rohdendorf B (1974) The historical development of Diptera. University of Alberta Press, Edmonton, Canada
Sarich WM (1977) Rates, sample sizes, and the neutrality hypothesis for electrophoresis in evolutionary studies. Nature 265:24–28
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
Sarich VM, Cronin JE (1980) South American mammal molecular systematics, evolutionary clocks, and continental drift. In: Ciochon RL, Chiarelli AB (eds) Evolutionary biology of the New World monkeys and continental drift. Plenum Press, New York, pp 399–421
Sarich VM, Wilson AC (1966) Quantitative immunochemistry and the evolution of primate albumins: microcomplement fixation. Science 154:1563–1566
Sarich VM, Wilson AC (1967) Rates of albumin evolution in primates. Proc Natl Acad Sci USA 58:142–148
Sarich VM, Wilson AC (1973) Generation time and genomic evolution in primates. Science 179:1144–1147
Sneath PHA (1980) The estimation of differences in protein evolution rates. Proc Geol Assoc 91:71–79
Sneath PHA, Sokal RR (1973) Numerical taxonomy. WH Freeman, San Francisco
Tarling, DH (1980) The geological evolution of South America with special reference to the last 200 million years. In: Ciochon RL, Charelli AB (eds) Evolutionary biology of the New World monkeys and continental drift. Plenum Press, New York, pp 1–41
Throckmorton LH (1975) The phylogeny, ecology and geography ofDrosophila. In: King RC (ed) Handbook of genetics, vol 3. Plenum Press, New York, pp 421–469
Uzzell T, Corbin KW (1971) Fitting discrete probability distributions to evolutionary events. Science 172:1089–1096
Wallace DG, Boulter D (1976) Immunological comparisons of higher plant plastocyanins. Phytochemistry 15:137–141
Wallace DG, King M-C, Wilson AC (1973) Albumin differences among ranid frogs: taxonomic and phylogenetic implications. Syst Zool 22:1–13
Wheeler MR (1963) A note on some fossil Drosophilidae from the amber of Chiapas, Mexico. J Paleontol 37:123–124
Wheeler MR (1981) The Drosophilidae: a taxonomic overview. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics of biology ofDrosophila, vol 3a. Academic Press, New York, pp 1–97
White TJ, Wilson AC (1978) Molecular anthropology. Evolution 32:693–694
Wilson AC (1975) Evolutionary importance of gene regulation. In: Stadler Symposium, vol. 7. University of Missouri Agricultural Experiment Station, Columbia, Missouri, p. 117–132
Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639
Yang SY, Soule M, Gorman GC (1974)Anolis lizards of the Eastern Caribbean: a case study in evolution, I. Genetic relationships, phylogeny and colonization sequence of theroquet group. Syst Zool 23:387–399
Zwiebel LJ, Cohn VH, Wright DR, Moore GP (1982) Evolution of single-copy DNA and the ADH gene in seven drosophilids. J Mol Evol 19:62–71
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Beverley, S.M., Wilson, A.C. Molecular evolution inDrosophila and the higher diptera. J Mol Evol 21, 1–13 (1984). https://doi.org/10.1007/BF02100622
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DOI: https://doi.org/10.1007/BF02100622