High rate of recent transposable element-induced adaptation in Drosophila melanogaster

PLoS Biology

Volumn 6, Issue 10, 2008, Pages 2109-2129

  González, Josefa ^a   Lenkov, Kapa ^a   Lipatov, Mikhail ^a   Macpherson, J Michael ^a   Petrov, Dmitri A ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; AFRICA; ARTICLE; CLIMATE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EVOLUTION; GENOME; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; TRANSPOSON; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; MOLECULAR EVOLUTION; POLYMERASE CHAIN REACTION;

DROSOPHILA MELANOGASTER;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; GENOME, INSECT; MUTAGENESIS, INSERTIONAL; MUTATION; POLYMERASE CHAIN REACTION;

EID: 54949129791     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0060251     Document Type: Article

References (110)

1. Glinka S, Ometto L, Mousset S, Stephan W, De Lorenzo D (2003) Demography and natural selection have shaped genetic variation in Drosophila melanogaster: a multi-locus approach. Genetics 165: 1269-1278.
2. Smith NG, Eyre-Walker A (2002) Adaptive protein evolution in Drosophila. Nature 415: 1022-1024.
3. Bierne N, Eyre-Walker A (2004) The genomic rate of adaptive amino acid substitution in Drosophila. Mol Biol Evol 21: 1350-1360.
4. Ometto L, Glinka S, De Lorenzo D, Stephan W (2005) Inferring the effects of demography and selection on Drosophila melanogaster populations from a chromosome-wide scan of DNA variation. Mol Biol Evol 22: 2119-2130.
5. Andolfatto P (2005) Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149-1152.
6. Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, et al. (2005) The effects of artificial selection on the maize genome. Science 308: 1310-1314.
7. Biswas S, Akey JM (2006) Genomic insights into positive selection. Trends Genet 22: 437-446.
8. Voight BF, Kudaravalli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biol 4: e72. doi:10.1371/journal. pbio.0040072
9. Shapiro JA, Huang W, Zhang C, Hubisz MJ, Lu J, et al. (2007) Adaptive genic evolution in the Drosophila genomes. Proc Natl Acad Sci U S A 104: 2271-2276.
10. Williamson SH, Hubisz MJ, Clark AG, Payseur BA, Bustamante CD, et al. (2007) Localizing recent adaptive evolution in the human genome. PLoS Genet 3: e90. doi:10.1371/journal.pgen.0030090
11. Andolfatto P (2007) Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome. Genome Res 17: 1755-1762.
12. Macpherson JM, Sella G, Davis JC, Petrov DA (2007) Genomewide spatial correspondence between nonsynonymous divergence and neutral polymorphism reveals extensive adaptation in Drosophila. Genetics 177: 2083-2099.
13. Kidwell MG, Lisch DR (2001) Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution Int J Org Evolution 55: 1-24.
14. Kazazian HH Jr (2004) Mobile elements: drivers of genome evolution. Science 303: 1626-1632.
15. Biemont C, Vieira C (2006) Genetics: junk DNA as an evolutionary force. Nature 443: 521-524.
16. Hughes JF, Coffin JM (2001) Evidence for genomic rearrangements mediated by human endogenous retroviruses during primate evolution. Nat Genet 29: 487-489.
17. van de Lagemaat LN, Landry JR, Mager DL, Medstrand P (2003) Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet 19: 530-536.
18. Jordan IK, Rogozin IB, Glazko GV, Koonin EV (2003) Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet 19: 68-72.
19. Marino-Ramirez L, Lewis KC, Landsman D, Jordan IK (2005) Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenet Genome Res 110: 333-341.
20. Lowe CB, Bejerano G, Haussler D (2007) Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. Proc Natl Acad Sci U S A 104: 8005-8010.
21. Nekrutenko A, Li WH (2001) Transposable elements are found in a large number of human protein-coding genes. Trends Genet 17: 619-621.
22. Lipatov M, Lenkov K, Petrov DA, Bergman CM (2005) Paucity of chimeric gene-transposable element transcripts in the Drosophila melanogaster genome. BMC Biol 3: 24.
23. Gotea V, Makalowski W (2006) Do transposable elements really contribute to proteomes? Trends Genet 22: 260-267.
24. Piriyapongsa J, Rutledge MT, Patel S, Borodovsky M, Jordan IK (2007) Evaluating the protein coding potential of exonized transposable element sequences. Biol Direct 2: 31.
25. Volff JN (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28: 913-922.
26. Green MM (1988) Mobile DNA elements and spontaneous gene mutation. Banbury Rep: 41-50.
27. Sankaranarayanan K (1988) Mobile genetic elements, spontaneous mutations and the assessment of genetic radiation hazards in man. Banbury Rep: 319-336.
28. Ashburner M, Golic KG, Hawley RS (2005) Drosophila: a laboratory handbook.2nd ed. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press. 210 pp.
29. Charlesworth B, Langley CH (1989) The population genetics of Drosophila transposable elements. Annu Rev Genet 23: 251-287.
30. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371: 215-220.
31. Nuzhdin SV (1999) Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica 107: 129-137.
32. Maside X, Bartolome C, Charlesworth B (2002) S-element insertions are associated with the evolution of the Hsp70 genes in Drosophila melanogaster. Curr Biol 12: 1686-1691.
33. Daborn PJ, Yen JL, Bogwitz MR, Le Goff G, Feil E, et al. (2002) A single p450 allele associated with insecticide resistance in Drosophila. Science 297: 2253-2256.
34. McCollum AM, Ganko EW, Barrass PA, Rodriguez JM, McDonald JF (2002) Evidence for the adaptive significance of an LTR retrotransposon sequence in a Drosophila heterochromatic gene. BMC Evol Biol 2: 5.
35. Petrov DA, Aminetzach YT, Davis JC, Bensasson D, Hirsh AE (2003) Size matters: non-LTR retrotransposable elements and ectopic recombination in Drosophila. Mol Biol Evol 20: 880-892.
36. Franchini LF, Ganko EW, McDonald JF (2004) Retrotransposon-gene associations are widespread among D. melanogaster populations. Mol Biol Evol 21: 1323-1331.
37. Marsano RM, Caizzi R, Moschetti R, Junakovic N (2005) Evidence for a functional interaction between the Bari1 transposable element and the cytochrome P450 cyp12a4 gene in Drosophila melanogaster. Gene 357: 122-128.
38. Aminetzach YT, Macpherson JM, Petrov DA (2005) Pesticide resistance via transposition-mediated adaptive gene truncation in Drosophila. Science 309: 764-767.
39. Ganko EW, Greene CS, Lewis JA, Bhattacharjee V, McDonald JF (2006) LTR retrotransposon-gene associations in Drosophila melanogaster. J Mol Evol 62: 111-120.
40. Ashburner M, Bergman CM (2005) Drosophila melanogaster: a case study of a model genomic sequence and its consequences. Genome Res 15: 1661-1667.
41. Quesneville H, Bergman CM, Andrieu O, Autard D, Nouaud D, et al. (2005) Combined evidence annotation of transposable elements in genome sequences. PLoS Comput Biol 1: 166-175. doi:10.1371/journal.pcbi.0010022
42. David JR, Capy P (1988) Genetic variation of Drosophila melanogaster natural populations. Trends Genet 4: 106-111.
43. Lachaise D, Cariou M-L, David JR, Lemeunier F, Tsacas F, et al. (1988) Historical biogeography of the Drosophila melanogaster species subgroup. Evol Biol 22: 159-225.
44. Li H, Stephan W (2006) Inferring the demographic history and rate of adaptive substitution in Drosophila. PLoS Genet 2: e166. doi:10.1371/journal. pgen.0020166
45. Thornton K, Andolfatto P (2006) Approximate Bayesian inference reveals evidence for a recent, severe bottleneck in a Netherlands population of Drosophila melanogaster. Genetics 172: 1607-1619.
46. Orengo DJ, Aguade M (2004) Detecting the footprint of positive selection in a european population of Drosophila melanogaster: multilocus pattern of variation and distance to coding regions. Genetics 167: 1759-1766.
47. Przeworski M (2002) The signature of positive selection at randomly chosen loci. Genetics 160: 1179-1189.
48. Teshima KM, Coop G, Przeworski M (2006) How reliable are empirical genomic scans for selective sweeps? Genome Res 16: 702-712.
49. Thornton KR, Jensen JD, Becquet C, Andolfatto P (2007) Progress and prospects in mapping recent selection in the genome. Heredity 98: 340-348.
50. Macpherson JM, González J, Witten DM, Davis JC, Rosenberg NA, et al. (2008) Nonadaptive explanations for signatures of partial selective sweeps in Drosophila. Mol Biol Evol 25: 1025-1042.
51. Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, et al. (2002) The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3: RESEARCH0084.
52. Montgomery E, Charlesworth B, Langley CH (1987) A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet Res 49: 31-41.
53. Charlesworth B, Lapid A, Canada D (1992) The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements. Genet Res 60: 115-130.
54. Sniegowski PD, Charlesworth B (1994) Transposable element numbers in cosmopolitan inversions from a natural population of Drosophila melanogaster. Genetics 137: 815-827.
55. Hill WG, Robertson A (1966) The effect of linkage on limits to artificial selection. Genet Res 8: 269-294.
56. Smith JM, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23: 23-35.
57. Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289-1303.
58. Hudson RR, Kaplan NL (1995) Deleterious background selection with recombination. Genetics 141: 1605-1617.
59. Pool JE, Aquadro CF (2006) History and structure of sub-Saharan populations of Drosophila melanogaster. Genetics 174: 915-929.
60. Andolfatto P, Przeworski M (2001) Regions of lower crossing over harbor more rare variants in African populations of Drosophila melanogaster. Genetics 158: 657-665.
61. Sabeti PC, Reich DE, Higgins JM, Levine HZ, Richter DJ, et al. (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419: 832-837.
62. Innan H, Kim Y (2008) Detecting local adaptation using the joint sampling of polymorphism data in the parental and derived populations. Genetics 179: 1713-1720.
63. Slatkin M, Rannala B (2000) Estimating allele age. Annu Rev Genomics Hum Genet 1: 225-249.
64. Kidwell MG (1992) Horizontal transfer of P elements and other short inverted repeat transposons. Genetica 86: 275-286.
65. Hoffmann AA, Weeks AR (2007) Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 129: 133-147.
66. Papatsenko DA, Makeev VJ, Lifanov AP, Regnier M, Nazina AG, et al. (2002) Extraction of functional binding sites from unique regulatory regions: the Drosophila early developmental enhancers. Genome Res 12: 470-481.
67. Al-Shahrour F, Minguez P, Tarraga J, Montaner D, Alloza E, et al. (2006) BABELOMICS: a systems biology perspective in the functional annotation of genome-scale experiments. Nucleic Acids Res 34: W472-476.
68. Hubbard TJ, Aken BL, Beal K, Ballester B, Caccamo M, et al. (2007) Ensembl 2007. Nucleic Acids Res 35: D610-617.
69. Wittkopp PJ, Haerum BK, Clark AG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430: 85-88.
70. Schaart JG, Mehli L, Schouten HJ (2005) Quantification of allele-specific expression of a gene encoding strawberry polygalacturonase-inhibiting protein (PGIP) using Pyrosequencing. Plant J 41: 493-500.
71. Brizuela BJ, Elfring L, Ballard J, Tamkun JW, Kennison JA (1994) Genetic analysis of the brahma gene of Drosophila melanogaster and polytene chromosome subdivisions 72AB. Genetics 137: 803-813.
72. Przeworski M, Coop G, Wall JD (2005) The signature of positive selection on standing genetic variation. Evolution 59: 2312-2323.
73. Hermisson J, Pennings PS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169: 2335-2352.
74. Wray GA (2007) The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8: 206-216.
75. Hoekstra HE, Coyne JA (2007) The locus of evolution: evo devo and the genetics of adaptation. Evolution 61: 995-1016.
76. Wittkopp PJ, Haerum BK, Clark AG (2008) Regulatory changes underlying expression differences within and between Drosophila species. Nat Genet 40: 346-350.
77. Schlenke TA, Begun DJ (2004) Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proc Natl Acad Sci U S A 101: 1626-1631.
78. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, et al. (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218.
79. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh YP, et al. (2007) Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5: e310. doi:10.1371/journal.pbio.0050310
80. Vogel C, Teichmann SA, Chothia C (2003) The immunoglobulin superfamily in Drosophila melanogaster and Caenorhabditis elegans and the evolution of complexity. Development 130: 6317-6328.
81. Bustamante CD, Fledel-Alon A, Williamson S, Nielsen R, Hubisz MT, et al. (2005) Natural selection on protein-coding genes in the human genome. Nature 437: 1153-1157.
82. Nielsen R, Hellmann I, Hubisz M, Bustamante C, Clark AG (2007) Recent and ongoing selection in the human genome. Nat Rev Genet 8: 857-868.
83. Khlebodarova TM, Gruntenko NE, Grenback LG, Sukhanova MZ, Mazurov MM, et al. (1996) A comparative analysis of juvenile hormone metabolyzing enzymes in two species of Drosophila during development. Insect Biochem Mol Biol 26: 829-835.
84. Flatt T, Tu MP, Tatar M (2005) Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. Bioessays 27: 999-1010.
85. Lai EC (2004) Notch signaling: control of cell communication and cell fate. Development 131: 965-973.
86. Kent D, Bush EW, Hooper JE (2006) Roadkill attenuates Hedgehog responses through degradation of Cubitus interruptus. Development 133: 2001-2010.
87. Jia J, Jiang J (2006) Decoding the Hedgehog signal in animal development. Cell Mol Life Sci 63: 1249-1265.
88. Maynard Smith JaH J. (1974) The hitch-hiking effect of a favorable gene. Genet Res 23: 23-25.
89. Kaplan NL, Darden T, Hudson RR (1988) The coalescent process in models with selection. Genetics 120: 819-829.
90. Kaplan NL, Hudson RR, Langley CH (1989) The "hitchhiking effect" revisited. Genetics 123: 887-899.
91. Berry AJ, Ajioka JW, Kreitman M (1991) Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics 129: 1111-1117.
92. Petrov DA (2002) DNA loss and evolution of genome size in Drosophila. Genetica 115: 81-91.
93. Kimura M, Ota T (1969) The average number of generations until extinction of an individual mutant gene in a finite population. Genetics 63: 701-709.
94. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
95. Lexa M, Horak J, Brzobohaty B (2001) Virtual PCR. Bioinformatics 17: 192-193.
96. Haring E, Hagemann S, Pinsker W (1995) Different evolutionary behaviour of P element subfamilies: M-type and O-type elements in Drosophila bifasciata and D. imaii. Gene 163: 197-202.
97. Wesley CS, Eanes WF (1994) Isolation and analysis of the breakpoint sequences of chromosome inversion In(3L)Payne in Drosophila melanogaster. Proc Natl Acad Sci U S A 91: 3132-3136.
98. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5: 150-163.
99. Ewens WJ (2004) Mathematical population genetics: theoretical introduction. 2nd edition. New York: Springer. 141 pp.
100. Kreitman M (1983) Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304: 412-417.
101. Schug MD, Hutter CM, Wetterstrand KA, Gaudette MS, Mackay TF, et al. (1998) The mutation rates of di-, tri- and tetranucleotide repeats in Drosophila melanogaster. Mol Biol Evol 15: 1751-1760.
102. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105: 437-460.
103. Hudson RR (2002) Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18: 337-338.
104. Tang H, Siegmund DO, Shen P, Oefner PJ, Feldman MW (2002) Frequentist estimation of coalescence times from nucleotide sequence data using a tree-based partition. Genetics 161: 447-459.
105. Wang H, Elbein SC (2007) Detection of allelic imbalance in gene expression using pyrosequencing. Methods Mol Biol 373: 157-176.
106. Peter A, Schottler P, Werner M, Beinert N, Dowe G, et al. (2002) Mapping and identification of essential gene functions on the X chromosome of Drosophila. EMBO Rep 3: 34-38.
107. Schultz J, Copley RR, Doerks T, Ponting CP, Bork P (2000) SMART: a webbased tool for the study of genetically mobile domains. Nucleic Acids Res 28: 231-234.
108. Augustin H, Grosjean Y, Chen K, Sheng Q, Featherstone DE (2007) Nonvesicular release of glutamate by glial xCT transporters suppresses glutamate receptor clustering in vivo. J Neurosci 27: 111-123.
109. Gonzalez-Aguero M, Zuniga A, Pottstock H, Del Pozo T, Gonzalez M, et al. (2005) Identification of genes expressed during Drosophila melanogaster gastrulation by using subtractive hybridization. Gene 345: 213-224.
110. Kamdar KP, Bachmann J, Broadus J, Stam L (2002) Nucleic acid sequences from Drosophila melanogaster that encode proteins essential for larval viability and uses thereof. World Patent 02057455.