Journal of Molecular Evolution

, Volume 31, Issue 5, pp 402–423 | Cite as

Evolution of the autosomal chorion cluster inDrosophila. IV. The HawaiianDrosophila: Rapid protein evolution and constancy in the rate of DNA divergence

  • Juan Carlos Martínez-Cruzado


Autosomal chorion geness18, s15, ands19 are shown to diverge at extremely rapid rates in closely related taxa of HawaiianDrosophila. Their nucleotide divergence rates are at least as fast as those of intergenic regions that are known to evolve more extensively between distantly related species. Their amino acid divergence rates are the fastest known to date. There are two nucleotide replacement substitutions for every synonymous one. The molecular basis for observed length and substitution mutations is analyzed. Length mutations are strongly associated with direct repeats in general, and with tandem repeats in particular, whereas the rate for an average transition is twice that for an average transversion.

The DNA sequence of the cluster was used to construct a phylogenetic tree for five taxa of the Hawaiian picture-winged species group ofDrosophila. Assignment of observed base substitutions occurring in various branches of the tree reveals an excess of would-be homoplasies in a centrally localized 1.8-kb segment containing thes15 gene. This observation may be a reflection of ancestral excess polymorphisms in the segment. The chorion cluster appears to evolve at a constant rate regardless of whether the central 1.8-kb segment is included or not in the analysis. Assuming that the time of divergence ofDrosophila grimshawi and theplanitibia subgroup coincides with the emergence of the island of Kauai, the overall rate of base substitution in the cluster is estimated to be 0.8% million years, whereas synonymous sites are substituted at a rate of 1.2%/million years.

Key words

Chorion gene cluster Homomorphism Excess polymorphism Comparative evolutionary rates Molecular clock Transitions and transversions 


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  1. Albertini AM, Hofer M, Calos MP, Miller JH (1982) On the formation of spontaneous deletions: the importance of short sequence homologies in the generation of large deletions. Cell 29:319–328PubMedGoogle Scholar
  2. Biggin MD, Gibson JJ, Hong GF (1983) Buffer gradient gels and35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci USA 80:3963–3965PubMedGoogle Scholar
  3. Birky CW, Maruyama T, Fuerst P (1983) An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103: 513–527PubMedGoogle Scholar
  4. Britten RJ (1986) Rates of DNA sequence evolution differ between taxonomic groups. Science 231:1393–1398PubMedGoogle Scholar
  5. 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
  6. Caccone A, DeSalle R, Powell JR (1988) Calibration of the change in thermal stability of DNA duplexes and degree of base pair mismatch. J Mol Evol 27:212–216PubMedGoogle Scholar
  7. Carson HL (1968) The population flush and its genetic consequences. In: Lewontin RC (ed) Population biology and evolution. Syracuse Univ Press, New York, pp 123–137Google Scholar
  8. Carson HL (1971) Polytene chromosome relationships in Hawaiian species ofDrosophila V. Additions to the chromosomal phylogeny of the picture-winged species. Univ Tex Publ 7103:183–191Google Scholar
  9. Carson HL (1975) The genetics of speciation at the diploid level. Am Nat 109:83–92Google Scholar
  10. Carson HL (1982a) Evolution ofDrosophila on the newer Hawaiian volcanoes. Heredity 48:3–25PubMedGoogle Scholar
  11. Carson HL (1982b) Speciation as a major reorganization of polygenic balances. In: Barigozzi C (ed) Mechanisms of speciation. Liss, New York, pp. 411–433Google Scholar
  12. Carson HL (1983) Chromosomal sequences and interisland colonizations in HawaiianDrosophila. Genetics 103:465–482Google Scholar
  13. Carson HL, Bryant PJ (1979) Genetic variation of HawaiianDrosophila. VI. Change in a secondary sexual character as evidence of incipient speciation inDrosophila. Proc Natl Acad Sci USA 57:1280–1285Google Scholar
  14. Carson HL, Kaneshiro KY (1976)Drosophila of Hawaii: systematics and ecological genetics. Annu Rev Ecol Syst 7:311–345Google Scholar
  15. Carson HL, Templeton AR (1984) Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annu Rev Ecol Syst 15:97–131Google Scholar
  16. Carson HL, Yoon JS (1982) Genetics and evolution of HawaiianDrosophila. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics and biology ofDrosophila, vol 3b. Academic Press, New York, pp 298–344Google Scholar
  17. Carson HL, Kaneshiro KY, Val FC (1989) Natural hybridization between the sympatric Hawaiian speciesDrosophila silvestris andDrosophila heteroneura. Evolution 43:190–203Google Scholar
  18. Clary DO, Wolstenholme DR (1987)Drosophila mitochondrial DNA: conserved sequences in the A+T-rich region and supporting evidence for a secondary structure model of the small ribosomal RNA. J Mol Evol 25:116–125PubMedGoogle Scholar
  19. Coyne JA (1976) Lack of genic similarity between two sibling species ofDrosophila as revealed by varied techniques. genetics 84:593–607PubMedGoogle Scholar
  20. Coyne JA, Kreitman M (1986) Evolutionary genetics of two sibling species,Drosophila simulans andD. sechellia. Evolution 40:673–691Google Scholar
  21. de Boer JG, Ripley LS (1988) Anin vitro assay for frameshift mutations: hotspots for deletions of 1 bp by Klenow-fragment polymerase share a consensus DNA sequence. Genetics 118: 181–191PubMedGoogle Scholar
  22. Delidakis C, Kafatos FC (1987) Amplification of a chorion gene cluster inDrosophila is subject to multiplecis-regulatory elements and to long-range position effects. J Mol Biol 197:11–26PubMedGoogle Scholar
  23. Delidakis C, Kafatos FC (1989) Amplification enhancers and replication origins in the autosomal chorion gene cluster ofDrosophila. EMBO J 8:891–901PubMedGoogle Scholar
  24. DeSalle R, Giddings LV (1986) Discordance of nuclear and mitochondrial DNA phylogenies in HawaiianDrosophila. Proc Natl Acad Sci USA 83:6902–6906PubMedGoogle Scholar
  25. DeSalle R, Templeton AR (1988) Founder effects and the rate of mitochondrial DNA evolution in HawaiianDrosophila. Evolution 42:1076–1084Google Scholar
  26. DeSalle R, Giddings LV, Kaneshiro KY (1986) 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
  27. 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
  28. Dickerson RE (1971) The structure of cytochrome c and the rates of molecular evolution. J Mol Evol 1:26–45PubMedGoogle Scholar
  29. Dover G (1982) Molecular drive: a cohesive mode of species evolution. Nature 299:111–117PubMedGoogle Scholar
  30. Efstratiadis A, Posakony JW, Maniatis T, Lawn RM, O'Connell C, Spritz RA, Deriel JK, Forget BG, Weissman SM, Slightom JL, Blechl AE, Smithies O, Baralle FE, Shoulders CC, Proudfoot NJ (1980) The structure and evolution of the human β-globin gene family. Cell 21:653–668PubMedGoogle Scholar
  31. Eickbush TH, Burke WD (1985) Silkmoth chorion gene families contain patchwork patterns of sequence homology. Proc Natl Acad Sci USA 82:2814–2818PubMedGoogle Scholar
  32. Farabaugh PJ, Schmeissner U, Hoffer M, Miller JH (1978) Genetic studies of thelac repressor. VII. On the molecular nature of spontaneous hotspots in thelac I gene ofEscherichia coli. J Mol Biol 126:847–863PubMedGoogle Scholar
  33. Fenerjian MG, Martinez-Cruzado JC, Swimmer C, King D, Kafatos FC (1989) Evolution of the autosomal chorion locus inDrosophila. II. Chorion gene expression and sequence comparisons of thes16 ands19 genes in evolutionarily distantly related species. J Mol Evol 29:108–125PubMedGoogle Scholar
  34. Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284PubMedGoogle Scholar
  35. Frendewey D, Keller W (1985) Stepwise assembly of a pre-mRNA splicing complex requires U-snRNPs and specific intron sequences. Cell 42:355–367PubMedGoogle Scholar
  36. Funkhouser JG, Barnes IL, Naughton JJ (1968) The determination of a series of ages of Hawaiian volcanoes by the potassium-argon method. Pac Sci 22:369–372Google Scholar
  37. Gillespie JH (1986) Natural selection and the molecular clock. Mol Biol Evol 3:138–155PubMedGoogle Scholar
  38. Hayashida H, Miyata T (1983) Unusual evolutionary conservation and frequent DNA segment exchange in class I genes of the major histocompatibility complex. Proc Natl Acad Sci USA 80:2671–2675PubMedGoogle Scholar
  39. Henikoff S (1987) Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol 155:156–165PubMedGoogle Scholar
  40. Hunt JA, Carson HL (1982) Evolutionary relationships of four species of HawaiianDrosophila as measured by DNA reassociation. Genetics 104:353–364Google Scholar
  41. Hunt JA, Hall TJ, Britten RJ (1981) Evolutionary distances in HawaiianDrosophila measured by DNA reassociation. J Mol Evol 17:361–367PubMedGoogle Scholar
  42. Iatrou K, Tsitilou SG, Kafatos FC (1984) DNA sequence transfer between two high-cysteine chorion gene families in the silkmothBombyx mori. Proc Natl Acad Sci USA 81:4452–4456PubMedGoogle Scholar
  43. Jones CW, Kafatos FC (1982) Accepted mutations in a gene family: evolutionary diversification of duplicated DNA. J Mol Evol 19:87–103PubMedGoogle Scholar
  44. Jones CW, Rosenthal N, Rodakis GC, Kafatos FC (1979) Evolution of two major chorion multigene families as inferred from clone cDNA and protein sequences. Cell 18:1317–1332PubMedGoogle Scholar
  45. Jukes TH (1987) Transitions, transversions, and the molecular evolutionary clock. J Mol Evol 26:87–98PubMedGoogle Scholar
  46. Jukes TH, Bhushan V (1986) Silent nucleotide substitutions and G+C content of some mitochondrial and bacterial genes. J Mol Evol 24:39–44PubMedGoogle Scholar
  47. Kaneshiro KY (1976) Ethological isolation and phylogeny in theplanitibia subgroup of HawaiianDrosophila. Evolution 30:740–745Google Scholar
  48. Kaneshiro KY, Kurihara JS (1982) Sequential differentiation of sexual behavior in populations ofDrosophila silvestris. Pac Sci 35:177–183Google Scholar
  49. Kaneshiro KY, Val FC (1977) Natural hybridization between a sympatric pair of HawaiianDrosophila. Am Nat 111:897–902Google Scholar
  50. Kaplan N, Langley CH (1979) A new estimate of sequence divergence of mitochondrial DNA using restriction endonuclease mapping. J Mol Evol 13:295–304PubMedGoogle Scholar
  51. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedGoogle Scholar
  52. Lecanidou R, Rodakis GC, Eickbush TH, Kafatos FC (1986) Evolution of the silkmoth chorion gene superfamily: gene families CA and CB. Proc Natl Acad Sci USA 83:6514–6518PubMedGoogle Scholar
  53. Lerman LS (1963) The structure of the DNA-acridine complex. Proc Natl Acad Sci USA 49:94–102PubMedGoogle Scholar
  54. Levine J, Spradling A (1985) DNA sequence of a 3.8 kilobase pair region controllingDrosophila chorion gene amplification. Chromosoma 92:136–142PubMedGoogle Scholar
  55. Levinson A, Silver D, Seed B (1984) Minimal size plasmids containing an M13 origin for production of single-stranded transducing particles. J Mol Appl Genet 2:507–517PubMedGoogle Scholar
  56. Li W-H, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol 25:330–342PubMedGoogle Scholar
  57. Loukas M, Kafatos FC (1986) The actin loci in the genusDrosophila: establishment of chromosomal homologies among distantly related species byin situ hybridization. Chromosoma 94:297–308Google Scholar
  58. Magni GE (1963) The origin of spontaneous mutations during meiosis. Proc Natl Acad Sci USA 50:975–980PubMedGoogle Scholar
  59. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NYGoogle Scholar
  60. Martínez-CruZado JC, Swimmer C, Fenerjian MG, Kafatos FC (1988) Evolution of the autosomal chorion locus inDrosophila. I. General organization of the locus and sequence comparisons of geness15 ands19 in evolutionarily distant species. Genetics 119:663–677PubMedGoogle Scholar
  61. McDougall I (1964) Potassium-argon ages from lavas of the Hawaiian Islands. Geol Soc Am Bull 75:107–128Google Scholar
  62. McDougall I (1979) Age of shield-building volcanism of Kauai and linear migration of volcanism in the Hawaiian island chain. Earth Planet Sci Lett 46:31–42Google Scholar
  63. Miyata T, Yasunaga T, Nishida T (1980) Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci USA 77:7328–7332PubMedGoogle Scholar
  64. Müller HJ (1940) Bearings of theDrosophila work on systematics. In: Hurley J (ed) New systematics. Clarendon Press, Oxford, pp 185–268Google Scholar
  65. Nei M, Tajima F (1983) Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105:207–217PubMedGoogle Scholar
  66. Perler F, Efstratiadis A, Lomedico P, Gilbert W, Kolodner R, Dodgson J (1980) The evolution of genes: the chicken preproinsulin gene. Cell 20:555–566PubMedGoogle Scholar
  67. Powell JR (1983) Interspecific cytoplasmic gene flow in the absence of nuclear gene flow: evidence fromDrosophila. Proc Natl Acad Sci USA 80:492–495PubMedGoogle Scholar
  68. Pustell J, Kafatos FC (1984) A convenient and adaptable package of computer programs for DNA and protein sequence management, analysis and homology determination. Nucleic Acids Res 12:643–655PubMedGoogle Scholar
  69. Riley MA (1989) Nucleotide sequence of theXdh region inDrosophila pseudoobscura and an analysis of the evolution of synonymous codons. Mol Biol Evol 6:33–52PubMedGoogle Scholar
  70. Rodakis GC, Lecanidou R, Eickbush TH (1984) Diversity in a chorion multigene family created by a tandem duplication and a putative gene-conversion event. J Mol Evol 20:265–273PubMedGoogle Scholar
  71. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467PubMedGoogle Scholar
  72. Sharp PM, Li W-H (1989) On the rate of DNA sequence evolution inDrosophila. J Mol Evol 28:398–402PubMedGoogle Scholar
  73. Shoemaker JS, Fitch WM (1989) Evidence from nuclear sequences that invariable sites should be considered when sequence divergence is calculated. Mol Biol Evol 6:270–289PubMedGoogle Scholar
  74. Spieth HT (1982) Behavioral biology and evolution of the Hawaiian picture-winged species group ofDrosophila. Evol Biol 14:351–437Google Scholar
  75. Staden R (1982) Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Res 10:4731–4751PubMedGoogle Scholar
  76. Staden R (1984) A computer program to enter DNA gel reading data into a computer. Nucleic Acids Res 12:499–504PubMedGoogle Scholar
  77. Streisinger G, Okada Y, Emrich J, Newton J, Tsugita A, Terzhagi E, Inouye M (1966) Frameshift mutations and the genetic code. Cold Spring Harbor Symp Quant Biol 31:77–84PubMedGoogle Scholar
  78. Swimmer C, Delidakis C, Kafatos FC (1989) Amplificationcontrol element ACE-3 is important but not essential for autosomal chorion gene amplification. Proc Natl Acad Sci USA 86:8823–8827PubMedGoogle Scholar
  79. Swimmer C, Fenerfian MG, Martínez-Cruzado JC, Kafatos FC (1990) Evolution of the autosomal chorion gene cluster inDrosophila. III. Comparison of thes18 gene in evolutionarily distant species and interspecific control of chorion gene amplification. J Mol Biol (in press)Google Scholar
  80. Swofford DL (1985) Phylogenetic analysis using parsimony (PAUP), version 2.4. Illinois Natural History Survey, Champaign ILGoogle Scholar
  81. Takahata N, Slatkin M (1984) Mitochondrial gene flow. Proc Natl Acad Sci USA 81:1764–1767PubMedGoogle Scholar
  82. Templeton AR (1980) The theory of speciation via the founder principle. Genetics 94:1011–1038PubMedGoogle Scholar
  83. Ticher A, Graur D (1989) Nucleic acid composition, codon usage, and the rate of synonymous substitution in proteincoding genes. J Mol Evol 28:286–298PubMedGoogle Scholar
  84. Whiting JH, Pliley MD, Farmer JL, Jeffery DE (1989)In situ hybridization analysis of chromosomal homologies inDrosophila melanogaster andDrosophila virilis. Genetics 122:99–109PubMedGoogle Scholar
  85. Wilson AC, Carlson SS, White SJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639PubMedGoogle Scholar
  86. 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
  87. Wong Y-C, Pustell J, Spoerel N, Kafatos FC (1985) Coding and potential regulatory sequences of a cluster of chorion genes inDrosophila melanogaster. Chromosoma 92:124–135PubMedGoogle Scholar
  88. Wu C-I, Li W-H (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745PubMedGoogle Scholar
  89. Zuckerkandl E (1986) Polite DNA: functional density and functional compatibility in genomes. J Mol Evol 24:12–27PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1990

Authors and Affiliations

  • Juan Carlos Martínez-Cruzado
    • 1
  1. 1.Museum of Comparative ZoologyHarvard UniversityCambridgeUSA

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