Journal of Molecular Evolution

, Volume 57, Issue 5, pp 562–573 | Cite as

Molecular Phylogeny of the Drosophila melanogaster Species Subgroup

Article

Abstract

Although molecular and phenotypic evolution have been studied extensively in Drosophila melanogaster and its close relatives, phylogenetic relationships within the D. melanogaster species subgroup remain unresolved. In particular, recent molecular studies have not converged on the branching orders of the D. yakubaD. teissieri and D. erectaD. orena species pairs relative to the D. melanogasterD. simulansD. mauritianaD. sechellia species complex. Here, we reconstruct the phylogeny of the melanogaster species subgroup using DNA sequence data from four nuclear genes. We have employed “vectorette PCR” to obtain sequence data for orthologous regions of the Alcohol dehydrogenase (Adh), Alcohol dehydrogenase related (Adhr), Glucose dehydrogenase (Gld), and rosy (ry) genes (totaling 7164 bp) from six melanogaster subgroup species (D. melanogaster, D. simulans, D. teissieri, D. yakuba, D. erecta, and D. orena) and three species from subgroups outside the melanogaster species subgroup [D. eugracilis (eugracilis subgroup), D. mimetica (suzukii subgroup), and D. lutescens (takahashii subgroup)]. Relationships within the D. simulans complex are not addressed. Phylogenetic analyses employing maximum parsimony, neighbor-joining, and maximum likelihood methods strongly support a D. yakubaD. teissieri and D. erectaD. orena clade within the melanogaster species subgroup. D. eugracilis is grouped closer to the melanogaster subgroup than a D. mimeticaD. lutescens clade. This tree topology is supported by reconstructions employing simple (single parameter) and more complex (nonreversible) substitution models.

Keywords

Drosophila melanogaster species subgroup Phylogeny Alcohol dehydrogenase Alcohol dehydrogenase related Glucose dehydrogenase rosy 

Notes

Acknowledgements

We are grateful to C. dePamphilis for allowing us use of his automated sequencer and to S. Hauswaldt for technical assistance. We also thank R. DeSalle and K. Montooth for comments on the manuscript and F. Rodríguez-Trelles for advice on use of the GGG95 and SK programs. M. Ashburner kindly provided the D. erecta strain. This research was supported by grants from the Alfred P. Sloan Foundation and the National Science Foundation (DEB-0235472) to HA.

References

  1. 1.
    Akashi, H 1995Inferring weak selection from patterns of polymorphism and divergence at “silent” sites in Drosophila DNA.Genetics13910671076PubMedGoogle Scholar
  2. 2.
    Akashi, H 1996Molecular evolution between Drosophila melanogaster and D. simulans: Reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster.Genetics14412971307PubMedGoogle Scholar
  3. 3.
    Altschul, SF, Gish, W, Miller, W, Myers, EW, Lipman, DJ 1990Basic local alignment search tool.J Mol Biol215403410CrossRefPubMedGoogle Scholar
  4. 4.
    Arhontaki, K, Eliopoulos, E, Goulielmos, G, Kastanis, P, Tsakas, S, Loukas, M, Ayala, F 2002Functional constraints of the Cu, Zn superoxide dismutase in species of the Drosophila melanogaster subgroup and phylogenetic analysis.J Mol Evol55745756CrossRefPubMedGoogle Scholar
  5. 5.
    Arnold, C, Hodgson, IJ 1991Vectorette PCR: A novel approach to genomic walking.PCR Methods Appl13942PubMedGoogle Scholar
  6. 6.
    Ashburner, M 1989Drosophila: A laboratory handbook.Cold Spring Harbor LaboratoryCold Spring Harbor, NYGoogle Scholar
  7. 7.
    Ashburner, M, Bodmer, M, Lemeunier, F 1984On the evolutionary relationships of Drosophila melanogaster.Dev Genet4295312Google Scholar
  8. 8.
    Baker, RH, DeSalle, R 1997Multiple sources of character information and the phylogeny of Hawaiian Drosophilids.Syst Biol46654673PubMedGoogle Scholar
  9. 9.
    Barnes, SR, Webb, DA, Dover, G 1978The distribution of satellite and main-band DNA components in the melanogaster species subgroup of Drosophila I. Fractionation of DNA in actinomycin D and distamycin A density gradients.Chromosoma67341363PubMedGoogle Scholar
  10. 10.
    Bettencourt, BR, Feder, ME 2001Hsp70 duplication in the Drosophila melanogaster species group: How and when did two become five?Mol Biol Evol1812721282PubMedGoogle Scholar
  11. 11.
    Bonneton, F, Wegnez, M 1995Developmental variability of metallothionein Mtn gene expression in the species of the Drosophila melanogaster subgroup.Dev Genet16253263PubMedGoogle Scholar
  12. 12.
    Bremer, K 1988The limits of amino-acid sequence data in angiosperm phylogenetic reconstruction.Evolution42795803Google Scholar
  13. 13.
    Bremer, K 1994Branch support and tree stability.Cladistics10295304CrossRefGoogle Scholar
  14. 14.
    Caccone, A, Moriyama, EN, Gleason, JM, Nigro, L, Powell, JR 1996A molecular phylogeny for the Drosophila melanogaster subgroup and the problem of polymorphism data.Mol Biol Evol1312241232PubMedGoogle Scholar
  15. 15.
    Caccone, A, Amato, GD, Powell, JR 1988Rates and patterns of scnDNA and mtDNA divergence within the Drosophila melanogaster subgroup.Genetics118671683PubMedGoogle Scholar
  16. 16.
    Cariou, ML 1987Biochemical phylogeny of the eight species in the Drosophila melanogaster subgroup, including D. sechellia and D. orena.Genet Res50181185PubMedGoogle Scholar
  17. 17.
    Cowling, DE, Burnet, B 1981Courtship songs and genetic control of their acoustic characteristics in sibling species of Drosophila melanogaster subgroup.Anim Behav29924935Google Scholar
  18. 18.
    Daïnou, O, Cariou, ML, David, JR, Hickey, D 1987Amylase gene duplication: An ancestral trait in the Drosophila melanogaster species subgroup.Heredity59245251PubMedGoogle Scholar
  19. 19.
    Eisses, KT, Van Dijk, H, Van Delden, W 1979Genetic differentiation within melanogaster species group of the genus Drosophila (Sophophora).Evolution3310631068Google Scholar
  20. 20.
    Felsenstein, J 1981Evolutionary trees from DNA sequences: a maximum likelihood approach.J Mol Evol17368376PubMedGoogle Scholar
  21. 21.
    Felsenstein, J 1985Confidence limits on phylogenies: An approach using the bootstrap.Evolution39783791Google Scholar
  22. 22.
    Felsenstein, J 1993PHYLIP, phylogenetic inference package and documentation.Distributed by the author, Department of Genetics, University of WashingtonSeattleGoogle Scholar
  23. 23.
    Fitch, WM 1971Towards defining the course of evolution: Minimum change for a specific tree topology.Syst Zool20406416Google Scholar
  24. 24.
    Gailey, DA, Ho, SK, Ohshima, S, Liu, JH, Eyassu, M, Washington, MA, Yamamoto, D, Davis, T 2000A phylogeny of the Drosophilidae using the sex-behaviour gene fruitless.Hereditas1338183PubMedGoogle Scholar
  25. 25.
    Galtier, N 2001Maximum-likelihood phylogenetic analysis under a covarion-like model.Mol Biol Evol18866873PubMedGoogle Scholar
  26. 26.
    Galtier, N, Gouy, M 1995Inferring phylogenies from DNA sequences of unequal base compositions.Proc Natl Acad Sci USA921131711321PubMedGoogle Scholar
  27. 27.
    Galtier, N, Gouy, M 1998Inferring pattern and process: Maximum-likelihood implementation of a nonhomogeneous model of DNA sequence evolution for phylogenetic analysis.Mol Biol Evol15871879PubMedGoogle Scholar
  28. 28.
    Galtier, N, Tourasse, N, Gouy, M 1999A nonhyperthermophilic common ancestor to extant life forms.Science283220221CrossRefPubMedGoogle Scholar
  29. 29.
    Gentile, KL, Burke, WD, Eickbush, TH 2001Multiple lineages of R1 retrotransposable elements can coexist in the rDNA loci of Drosophila.Mol Biol Evol18235245PubMedGoogle Scholar
  30. 30.
    Goldman, N, Anderson, JP, Rodrigo, AG 2000Likelihood-based tests of topologies in phylogenetics.Syst Biol49652670PubMedGoogle Scholar
  31. 31.
    Goto, SG, Kimura, MT 2001Phylogenetic utility of mitochondrial COI and nuclear Gpdh genes in Drosophila.Mol Phylogenet Evol18404422CrossRefPubMedGoogle Scholar
  32. 32.
    Harr, B, Zangerl, B, Schlotterer, C 2000Removal of microsatellite interruptions by DNA replication slippage: phylogenetic evidence from Drosophila.Mol Biol Evol1710011009PubMedGoogle Scholar
  33. 33.
    Hasegawa, M, Hashimoto, T, Adachi, J, Iwabe, N, Miyata, T 1993Early branchings in the evolution of eukaryotes: Ancient divergence of entamoeba that lacks mitochondria revealed by protein sequence data.J Mol Evol36380388PubMedGoogle Scholar
  34. 34.
    Hecker, KH, Roux, KH 1996High and low annealing temperatures increase both specificity and yield in touchdown and stepdown PCR.Biotechniques20478485PubMedGoogle Scholar
  35. 35.
    Higgins, DG, Sharp, PM 1988CLUSTAL: A package for performing multiple sequence alignment on a microcomputer.Gene73237244PubMedGoogle Scholar
  36. 36.
    Inomata, N, Tachida, H, Yamazaki, T 1997Molecular evolution of the Amy multigenes in the subgenus Sophophora of Drosophila.Mol Biol Evol14942950PubMedGoogle Scholar
  37. 37.
    Jeffs, PS, Holmes, EC, Ashburner, M 1994The molecular evolution of the alcohol dehydrogenase and alcohol dehydrogenase-related genes in the Drosophila melanogaster species subgroup.Mol Biol Evol11287304PubMedGoogle Scholar
  38. 38.
    Jordan, IK, McDonald, JF 1998Evolution of the copia retrotransposon in the Drosophila melanogaster species subgroup.Mol Biol Evol1511601171PubMedGoogle Scholar
  39. 39.
    Jukes, TH, Cantor, CR 1969

    Evolution of protein molecules.

    Munro, HN eds. Mammalian protein metabolism.Academic PressNew York21132
    Google Scholar
  40. 40.
    Kopp, A, True, JR 2002Phylogeny of the Oriental Drosophila melanogaster species group: A multilocus reconstruction.Syst Biol51786805CrossRefPubMedGoogle Scholar
  41. 41.
    Lachaise, D, Cariou, ML, David, JR, Lemeunier, F, Tsacas, L, Ashburner, M 1988Historical Biogeography of the Drosophilamelanogaster species subgroup.Evol Biol22159225Google Scholar
  42. 42.
    Lachaise, D, Harry, M, Solignac, M, Lemeunier, F, Benassi, V, Cariou, ML 2000Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from Sao Tome.Proc R Soc Lond B Biol Sci26714871495CrossRefPubMedGoogle Scholar
  43. 43.
    Lemeunier, F, Ashburner, M 1976Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences.Proc R Soc Lond B Biol Sci193275294PubMedGoogle Scholar
  44. 44.
    Lemeunier, F, Ashburner, M 1984Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora) IV. The chromosomes of two new species.Chromosoma (Berl)89343351Google Scholar
  45. 45.
    Lemeunier, F, David, JR, Tsacas, L, Ashburner, M 1986

    The melanogaster species group.

    Ashburner, MCarson, HLThompson, JN eds. The genetics and biology of Drosophila.London147256
    Google Scholar
  46. 46.
    Lockhart, PJ, Howe, CJ, Bryant, DA, Beanland, TJ, Larkum, AW 1992Substitutional bias confounds inference of cyanelle origins from sequence data.J Mol Evol34153162PubMedGoogle Scholar
  47. 47.
    Lockhart, PJ, Stell, MA, Hendy, MD, Penny, D 1994Recovering evolutionary tress under a more realistic model of sequence evolution.Mol Biol Evol11605612Google Scholar
  48. 48.
    Loomis, WF, Smith, DW 1990Molecular phylogeny of Dictyostelium discoideum by protein sequence comparison.Proc Natl Acad Sci USA8790939097PubMedGoogle Scholar
  49. 49.
    Matsuo, Y 2000Molecular evolution of the histone 3 multigene family in the Drosophila melanogaster species subgroup.Mol Phylogenet Evol16339343CrossRefPubMedGoogle Scholar
  50. 50.
    Moriyama, EN, Gojobori, T 1992Rates of synonymous substitution and base composition of nuclear genes in Drosophila.Genetics130855864PubMedGoogle Scholar
  51. 51.
    Munté, A, Aguadé, M, Segarra, C 2001Changes in the recombinational environment affect divergence in the yellow gene of Drosophila.Mol Biol Evol1810451056PubMedGoogle Scholar
  52. 52.
    Nigro, L, Solignac, M, Sharp, PM 1991Mitochondrial DNA sequence divergence in the melanogaster and oriental species subgroups of Drosophila.J Mol Evol33156162PubMedGoogle Scholar
  53. 53.
    Ohnishi, S, Kawanishi, M, Watanabe, TK 1983Biochemical phylogenies of Drosophila: Protein differences detected by two-dimensional electrophoresis.Genetica65563Google Scholar
  54. 54.
    Okuyama, E, Shibata, H, Tachida, H, Yamazaki, T 1996Molecular evolution of the 5′-flanking regions of the duplicated Amy genes in Drosophila melanogaster species subgroup.Mol Biol Evol13574583PubMedGoogle Scholar
  55. 55.
    Parsch, J, Meiklejohn, CD, Hauschteck-Jungen, E, Hunziker, P, Hartl, DL 2001Molecular evolution of the ocnus and janus genes in the Drosophila melanogaster species subgroup.Mol Biol Evol18801811PubMedGoogle Scholar
  56. 56.
    Pelandakis, M, Solignac, M 1993Molecular phylogeny of Drosophila based on ribosomal RNA sequences.J Mol Evol37525543PubMedGoogle Scholar
  57. 57.
    Pelandakis, M, Higgins, DG, Solignac, M 1991Molecular phylogeny of the subgenus Sophophora of Drosophila derived from large subunit of ribosomal RNA sequences.Genetica848794PubMedGoogle Scholar
  58. 58.
    Powell, JR 1997Progress and prospects in evolutionary biology: The Drosophila model.Oxford University PressNew YorkGoogle Scholar
  59. 59.
    Powell, JR, DeSalle, R 1995Drosophila molecular phylogenies and their uses.Evol Biol2887138Google Scholar
  60. 60.
    Rambaut, A, Grassly, NC 1997Seq-Gen: An application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees.Comput Appl Biosci13235238PubMedGoogle Scholar
  61. 61.
    Rifkin, SA, Kim, J, White, KP 2003Evolution of gene expression in the Drosophila melanogaster subgroup.Nat Genet33138144CrossRefPubMedGoogle Scholar
  62. 62.
    Riley, J, Butler, R, Ogilvie, D, Finniear, R, Jenner, D, Powell, S, Anand, R, Smith, JC, Markham, AF 1990A novel, rapid method for the isolation of terminal sequences from yeast artificial chromosome (YAC) clones.Nucleic Acids Res1828872890PubMedGoogle Scholar
  63. 63.
    Ross, JL, Fong, PP, Cavener, DR 1994Correlated evolution of the cis-acting regulatory elements and developmental expression of the Drosophila Gld gene in seven species from the subgroup melanogaster.Dev Genet153850PubMedGoogle Scholar
  64. 64.
    Russo, CA, Takezaki, N, Nei, M 1995Molecular phylogeny and divergence times of Drosophilid species.Mol Biol Evol12391404PubMedGoogle Scholar
  65. 65.
    Rzhetsky, A, Nei, M 1995Tests of applicability of several substitution models for DNA sequence data.Mol Biol Evol12131151PubMedGoogle Scholar
  66. 66.
    Saccone, C, Pesole, G, Preparata, G 1989DNA microenvironments and the molecular clock.J Mol Evol29407411PubMedGoogle Scholar
  67. 67.
    Saitou, N, Nei, M 1987The neighbor-joining method: A new method for reconstructing phylogenetic trees.Mol Biol Evol4406425PubMedGoogle Scholar
  68. 68.
    Santamaria, P 1975Transplantation of nuclei between eggs of different species of Drosophila.Wilhelm Roux Arch1788998Google Scholar
  69. 69.
    Schawaroch, V 2002Phylogeny of a paradigm lineage: The Drosophila melanogaster species group (Diptera: Drosophilidae).Biol Linn Soc762137CrossRefGoogle Scholar
  70. 70.
    Schlötterer, C, Hauser, MT, von Haeseler, A, Tautz, D 1994Comparative evolutionary analysis of rDNA ITS regions in Drosophila.Mol Biol Evol11513522PubMedGoogle Scholar
  71. 71.
    Shibata, H, Yamazaki, T 1995Molecular evolution of the duplicated Amy locus in the Drosophila melanogaster species subgroup: Concerted evolution only in the coding region and an excess of nonsynonymous substitutions in speciation.Genetics141223236PubMedGoogle Scholar
  72. 72.
    Solignac, M, Monnerot, M, Mounolou, JC 1986Mitochondrial DNA evolution in the melanogaster species subgroup of Drosophila.J Mol Evol233140PubMedGoogle Scholar
  73. 73.
    Sorenson, MD 1999TreeRot, version 2.Boston UniversityBoston, MAGoogle Scholar
  74. 74.
    Sullivan, W, Ashburner, M, Hawley, R 2000Drosophila protocols.Cold Spring Harbor LaboratoryCold Spring Harbor, NYGoogle Scholar
  75. 75.
    Swofford, DL 2000PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4.Sinauer AssociatesSunderland, MAGoogle Scholar
  76. 76.
    Takano-Shimizu, T 1999Local recombination and mutation effects on molecular evolution in Drosophila.Genetics15312851296PubMedGoogle Scholar
  77. 77.
    Takano-Shimizu, T 2001Local changes in GC/AT substitution biases and in crossover frequencies on Drosophila chromosomes.Mol Biol Evol18606619PubMedGoogle Scholar
  78. 78.
    Tamura, K 1992Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases.Mol Biol Evol9678687PubMedGoogle Scholar
  79. 79.
    Tamura, K, Nei, M 1993Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees.Mol Biol Evol10512526PubMedGoogle Scholar
  80. 80.
    Tarrio, R, Rodriguez-Trelles, F, Ayala, FJ 2001Shared nucleotide composition biases among species and their impact on phylogenetic reconstructions of the Drosophilidae.Mol Biol Evol1814641473PubMedGoogle Scholar
  81. 81.
    Terzian, C, Ferraz, C, Demaille, J, Bucheton, A 2000Evolution of the Gypsy endogenous retrovirus in the Drosophila melanogaster subgroup.Mol Biol Evol17908914PubMedGoogle Scholar
  82. 82.
    Toda, M 1991Drosophilidae (Diptera) in Myanmar (Burma) VII. The Drosophila melanogaster species-group, excepting the D. montium species-subgroup.Oriental Insects256994Google Scholar
  83. 83.
    Tsacas, L, Bocquet, C 1976L’espèce chez les Drosophilidae.Mém Soc Zool Fr39203247Google Scholar
  84. 84.
    Weisburg, WG, Giovannoni, SJ, Woese, CR 1989The Deinococcus-Thermus phylum and the effect of rRNA composition on phylogenetic tree construction.Syst Appl Microbiol11128134PubMedGoogle Scholar
  85. 85.
    Yang, Z 1994Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods.J Mol Evol39306314PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 2003

Authors and Affiliations

  1. 1.Institute of Molecular Evolutionary Genetics, Department of BiologyThe Pennsylvania State University, University Park, PA 16802USA

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