1932

Abstract

Studies of the population dynamics of transposable elements (TEs) in indicate that consistent forces are affecting TEs independently of their modes of transposition and regulation. New sequencing technologies enable biologists to sample genomes at an unprecedented scale in order to quantify genome-wide polymorphism for annotated and novel TE insertions. In this review, we first present new insights gleaned from high-throughput data for population genomics studies of . We then consider the latest population genomics models for TE evolution and present examples of functional evidence revealed by genome-wide studies of TE population dynamics in . Although most of the TE insertions are deleterious or neutral, some TE insertions increase the fitness of the individual that carries them and play a role in genome adaptation.

[Erratum, Closure]

An erratum has been published for this article:
Population Genomics of Transposable Elements in
Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120213-092359
2014-11-23
2024-06-25
Loading full text...

Full text loading...

/deliver/fulltext/genet/48/1/annurev-genet-120213-092359.html?itemId=/content/journals/10.1146/annurev-genet-120213-092359&mimeType=html&fmt=ahah

Literature Cited

  1. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD. 1.  et al. 2000. The genome sequence of Drosophila melanogaster. Science 287:2185–95 [Google Scholar]
  2. Akagi K, Li J, Symer DE. 2.  2013. How do mammalian transposons induce genetic variation? A conceptual framework: The age, structure, allele frequency, and genome context of transposable elements may define their wide-ranging biological impacts. BioEssays 35:397–407 [Google Scholar]
  3. Aminetzach YT, Macpherson JM, Petrov DA. 3.  2005. Pesticide resistance via transposition-mediated adaptive gene truncation in Drosophila. Science 309:764–67 [Google Scholar]
  4. Ashburner M, Bergman CM. 4.  2005. Drosophila melanogaster: a case study of a model genomic sequence and its consequences. Genome Res. 15:1661–67 [Google Scholar]
  5. Bartolome C, Maside X, Charlesworth B. 5.  2002. On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Mol. Biol. Evol. 19:926–37 [Google Scholar]
  6. Bellen HJ, Levis RW, He Y, Carlson JW, Evans-Holm M. 6.  et al. 2011. The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 188:731–43 [Google Scholar]
  7. Bergman CM, Bensasson D. 7.  2007. Recent LTR retrotransposon insertion contrasts with waves of non-LTR insertion since speciation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 104:11340–45 [Google Scholar]
  8. Betancourt AJ, Presgraves DC. 8.  2002. Linkage limits the power of natural selection in Drosophila. Proc. Natl. Acad. Sci. USA 99:13616–20 [Google Scholar]
  9. Biemont C. 9.  1992. Population genetics of transposable DNA elements. A Drosophila point of view. Genetica 86:67–84 [Google Scholar]
  10. Biemont C, Lemeunier F, Garcia Guerreiro MP, Brookfield JF, Gautier C. 10.  et al. 1994. Population dynamics of the copia, mdg1, mdg3, gypsy, and P transposable elements in a natural population of Drosophila melanogaster. Genet. Res. 63:197–212 [Google Scholar]
  11. Blumenstiel JP, Chen X, He M, Bergman CM. 11.  2014. An age-of-allele test of neutrality for transposable element insertions. Genetics 196:523–38 [Google Scholar]
  12. Blumenstiel JP, Noll AC, Griffiths JA, Perera AG, Walton KN. 12.  et al. 2009. Identification of EMS-induced mutations in Drosophila melanogaster by whole-genome sequencing. Genetics 182:25–32 [Google Scholar]
  13. Boutin TS, Le Rouzic A, Capy P. 13.  2012. How does selfing affect the dynamics of selfish transposable elements?. Mob. DNA 3:5 [Google Scholar]
  14. Bowen NJ, McDonald JF. 14.  2001. Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. Genome Res. 11:1527–40 [Google Scholar]
  15. Braverman JM, Lazzaro BP, Aguade M, Langley CH. 15.  2005. DNA sequence polymorphism and divergence at the erect wing and suppressor of sable loci of Drosophila melanogaster and D. simulans. Genetics 170:1153–65 [Google Scholar]
  16. Burt A, Trivers R. 16.  2006. Genes in Conflict Cambridge, MA: Belknap Press [Google Scholar]
  17. Campos JL, Halligan DL, Haddrill PR, Charlesworth B. 17.  2014. The relation between recombination rate and patterns of molecular evolution and variation in Drosophila melanogaster. Mol. Biol. Evol. 31:1010–28 [Google Scholar]
  18. Carr M, Bensasson D, Bergman CM. 18.  2012. Evolutionary genomics of transposable elements in Saccharomyces cerevisiae. PLOS ONE 7:e50978 [Google Scholar]
  19. Casacuberta E, Gonzalez J. 19.  2013. The impact of transposable elements in environmental adaptation. Mol. Ecol. 22:1503–17 [Google Scholar]
  20. Charlesworth B, Coyne JA, Barton NH. 20.  1987. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130:113–46 [Google Scholar]
  21. Charlesworth B, Charlesworth D. 21.  1983. The population dynamics of transposable elements. Genet. Res. 42:1–27 [Google Scholar]
  22. Charlesworth B, Jarne P, Assimacopoulos S. 22.  1994. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. III. Element abundances in heterochromatin. Genet. Res. 64:183–97 [Google Scholar]
  23. Charlesworth B, Langley CH. 23.  1986. The evolution of self-regulated transposition of transposable elements. Genetics 112:359–83 [Google Scholar]
  24. Charlesworth B, Langley CH. 24.  1989. The population genetics of Drosophila transposable elements. Annu. Rev. Genet. 23:251–87 [Google Scholar]
  25. Charlesworth B, Lapid A, Canada D. 25.  1992. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genet. Res. 60:103–14 [Google Scholar]
  26. Chung H, Bogwitz MR, McCart C, Andrianopoulos A, Ffrench-Constant RH. 26.  et al. 2007. Cis-regulatory elements in the Accord retrotransposon result in tissue-specific expression of the Drosophila melanogaster insecticide resistance gene Cyp6g1. Genetics 175:1071–77 [Google Scholar]
  27. Comeron JM, Kreitman M. 27.  2000. The correlation between intron length and recombination in Drosophila. Dynamic equilibrium between mutational and selective forces. Genetics 156:1175–90 [Google Scholar]
  28. Comeron JM, Ratnappan R, Bailin S. 28.  2012. The many landscapes of recombination in Drosophila melanogaster. PLOS Genet. 8:e1002905 [Google Scholar]
  29. Cooley L, Kelley R, Spradling A. 29.  1988. Insertional mutagenesis of the Drosophila genome with single P elements. Science 239:1121–28 [Google Scholar]
  30. Cowley M, Oakey RJ. 30.  2013. Transposable elements re-wire and fine-tune the transcriptome. PLOS Genet. 9:e1003234 [Google Scholar]
  31. Cridland JM, Macdonald SJ, Long AD, Thornton KR. 31.  2013. Abundance and distribution of transposable elements in two Drosophila QTL mapping resources. Mol. Biol. Evol. 30:2311–27 [Google Scholar]
  32. Cuomo CA, Guldener U, Xu JR, Trail F, Turgeon BG. 32.  et al. 2007. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317:1400–2 [Google Scholar]
  33. Daborn PJ, Yen JL, Bogwitz MR, Le Goff G, Feil E. 33.  et al. 2002. A single p450 allele associated with insecticide resistance in Drosophila. Science 297:2253–56 [Google Scholar]
  34. Daniels SB, Chovnick A, Boussy IA. 34.  1990. Distribution of hobo transposable elements in the genus Drosophila. Mol. Biol. Evol. 7:589–606 [Google Scholar]
  35. de la Chaux N, Wagner A. 35.  2011. BEL/Pao retrotransposons in metazoan genomes. BMC Evol. Biol. 11:154 [Google Scholar]
  36. Deloger M, Cavalli FM, Lerat E, Biemont C, Sagot MF, Vieira C. 36.  2009. Identification of expressed transposable element insertions in the sequenced genome of Drosophila melanogaster. Gene 439:55–62 [Google Scholar]
  37. de Souza FS, Franchini LF, Rubinstein M. 37.  2013. Exaptation of transposable elements into novel cis-regulatory elements: Is the evidence always strong?. Mol. Biol. Evol. 30:1239–51 [Google Scholar]
  38. Dolgin ES, Charlesworth B. 38.  2008. The effects of recombination rate on the distribution and abundance of transposable elements. Genetics 178:2169–77 [Google Scholar]
  39. Dray T, Gloor GB. 39.  1997. Homology requirements for targeting heterologous sequences during P-induced gap repair in Drosophila melanogaster. Genetics 147:689–99 [Google Scholar]
  40. Ellison CE, Bachtrog D. 40.  2013. Dosage compensation via transposable element mediated rewiring of a regulatory network. Science 342:846–50 [Google Scholar]
  41. Finnegan DJ. 41.  1992. Transposable elements. Curr. Opin. Genet. Dev. 2:861–67 [Google Scholar]
  42. Fiston-Lavier AS, Barrón M, Petrov DA, González J. 42.  2014. T-lex2: genotyping, frequency estimation and re-annotation of transposable elements using single or pooled next-generation sequencing data. BioRxiv doi: http://dx.doi.org/10.1101/002964 [Google Scholar]
  43. Fiston-Lavier AS, Carrigan M, Petrov DA, Gonzalez J. 43.  2011. T-lex: a program for fast and accurate assessment of transposable element presence using next-generation sequencing data. Nucleic Acids Res. 39:e36 [Google Scholar]
  44. Flutre T, Duprat E, Feuillet C, Quesneville H. 44.  2011. Considering transposable element diversification in de novo annotation approaches. PLOS ONE 6:e16526 [Google Scholar]
  45. Goldman AS, Lichten M. 45.  1996. The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics 144:43–55 [Google Scholar]
  46. Goldman AS, Lichten M. 46.  2000. Restriction of ectopic recombination by interhomolog interactions during Saccharomyces cerevisiae meiosis. Proc. Natl. Acad. Sci. USA 97:9537–42 [Google Scholar]
  47. González J, Karasov TL, Messer PW, Petrov DA. 47.  2010. Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila. PLOS Genet. 6:e1000905 [Google Scholar]
  48. González J, Lenkov K, Lipatov M, Macpherson JM, Petrov DA. 48.  2008. High rate of recent transposable element–induced adaptation in Drosophila melanogaster. PLOS Biol. 6:e251 [Google Scholar]
  49. González J, Macpherson JM, Petrov DA. 49.  2009. A recent adaptive transposable element insertion near highly conserved developmental loci in Drosophila melanogaster. Mol. Biol. Evol. 26:1949–61 [Google Scholar]
  50. Guio L, Barron MG, Gonzalez J. 50.  2014. The transposable element Bari-Jheh mediates oxidative stress response in Drosophila. Mol. Ecol. 23:2020–30 [Google Scholar]
  51. Guzzardo PM, Muerdter F, Hannon GJ. 51.  2013. The piRNA pathway in flies: highlights and future directions. Curr. Opin. Genet. Dev. 23:44–52 [Google Scholar]
  52. Haddrill PR, Charlesworth B, Halligan DL, Andolfatto P. 52.  2005. Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content. Genome Biol. 6:R67 [Google Scholar]
  53. Haddrill PR, Halligan DL, Tomaras D, Charlesworth B. 53.  2007. Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over. Genome Biol. 8:R18 [Google Scholar]
  54. Hartl DL, Lohe AR, Lozovskaya ER. 54.  1997. Regulation of the transposable element mariner. Genetica 100:177–84 [Google Scholar]
  55. Haynes KA, Caudy AA, Collins L, Elgin SC. 55.  2006. Element 1360 and RNAi components contribute to HP1-dependent silencing of a pericentric reporter. Curr. Biol. 16:2222–27 [Google Scholar]
  56. Hill WG, Robertson A. 56.  1966. The effect of linkage on limits to artificial selection. Genet. Res. 8:269–94 [Google Scholar]
  57. Hilton HR, Kliman M, Hey J. 57.  1994. Using hitchhiking genes to study adaptation and divergence during speciation within the Drosophila melanogaster species complex. Evolution 48:1900–13 [Google Scholar]
  58. Huddleston J, Ranade S, Malig M, Antonacci F, Chaisson M. 58.  et al. 2014. Reconstructing complex regions of genomes using long-read sequencing technology. Genome Res. 24:688–96 [Google Scholar]
  59. Jaillet J, Genty M, Cambefort J, Rouault JD, Auge-Gouillou C. 59.  2012. Regulation of mariner transposition: the peculiar case of Mos1. PLOS ONE 7:e43365 [Google Scholar]
  60. Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R. 60.  et al. 2002. The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol. 3:research0084.1–0084.20 [Google Scholar]
  61. Kapitonov VV, Jurka J. 61.  2003. Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proc. Natl. Acad. Sci. USA 100:6569–74 [Google Scholar]
  62. Kapitonov VV, Jurka J. 62.  2008. A universal classification of eukaryotic transposable elements implemented in Repbase. Nat. Rev. Genet. 9:411–12; author reply 4 [Google Scholar]
  63. Keane TM, Wong K, Adams DJ. 63.  2013. RetroSeq: transposable element discovery from next-generation sequencing data. Bioinformatics 29:389–90 [Google Scholar]
  64. Kelley JL, Peyton JT, Fiston-Lavier A-S, Teets NM, Yee MC. 64.  2014. Compact genome of the Antarctic midge is likely an adaptation to an extreme environment. Nat. Commun. 54611 [Google Scholar]
  65. Khurana JS, Theurkauf W. 65.  2010. piRNAs, transposon silencing, and Drosophila germline development. J. Cell Biol. 191:905–13 [Google Scholar]
  66. Kidwell MG. 66.  1983. Hybrid dysgenesis in Drosophila melanogaster: factors affecting chromosomal contamination in the P-M system. Genetics 104:317–41 [Google Scholar]
  67. King EG, Macdonald SJ, Long AD. 67.  2012. Properties and power of the Drosophila synthetic population resource for the routine dissection of complex traits. Genetics 191:935–49 [Google Scholar]
  68. Kofler R, Betancourt AJ, Schlotterer C. 68.  2012. Sequencing of pooled DNA samples (Pool-Seq) uncovers complex dynamics of transposable element insertions in Drosophila melanogaster. PLOS Genet. 8:e1002487 [Google Scholar]
  69. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC. 69.  et al. 2001. Initial sequencing and analysis of the human genome. Nature 409:860–921 [Google Scholar]
  70. Langley CH, Montgomery E, Hudson R, Kaplan N, Charlesworth B. 70.  1988. On the role of unequal exchange in the containment of transposable element copy number. Genet. Res. 52:223–35 [Google Scholar]
  71. Langley CH, Stevens K, Cardeno C, Lee YC, Schrider DR. 71.  et al. 2012. Genomic variation in natural populations of Drosophila melanogaster. Genetics 192:533–98 [Google Scholar]
  72. Le Rouzic A, Boutin TS, Capy P. 72.  2007. Long-term evolution of transposable elements. Proc. Natl. Acad. Sci. USA 104:19375–80 [Google Scholar]
  73. Lee E, Iskow R, Yang L, Gokcumen O, Haseley P. 73.  et al. 2012. Landscape of somatic retrotransposition in human cancers. Science 337:967–71 [Google Scholar]
  74. Lee YC, Langley CH. 74.  2010. Transposable elements in natural populations of Drosophila melanogaster. Philos. Trans. R. Soc. Lond. Ser. B 365:1219–28 [Google Scholar]
  75. Lerat E. 75.  2010. Identifying repeats and transposable elements in sequenced genomes: how to find your way through the dense forest of programs. Heredity 104:520–33 [Google Scholar]
  76. Li W, Prazak L, Chatterjee N, Gruninger S, Krug L. 76.  et al. 2013. Activation of transposable elements during aging and neuronal decline in Drosophila. Nat. Neurosci. 16:529–31 [Google Scholar]
  77. Linheiro RS, Bergman CM. 77.  2012. Whole genome resequencing reveals natural target site preferences of transposable elements in Drosophila melanogaster. PLOS ONE 7:e30008 [Google Scholar]
  78. Lipatov M, Lenkov K, Petrov DA, Bergman CM. 78.  2005. Paucity of chimeric gene-transposable element transcripts in the Drosophila melanogaster genome. BMC Biol. 3:24 [Google Scholar]
  79. Loreto EL, Carareto CM, Capy P. 79.  2008. Revisiting horizontal transfer of transposable elements in Drosophila. Heredity 100:545–54 [Google Scholar]
  80. Lu C, Chen J, Zhang Y, Hu Q, Su W, Kuang H. 80.  2012. Miniature inverted-repeat transposable elements (MITEs) have been accumulated through amplification bursts and play important roles in gene expression and species diversity in Oryza sativa. Mol. Biol. Evol. 29:1005–17 [Google Scholar]
  81. Mackay TF, Richards S, Stone EA, Barbadilla A, Ayroles JF. 81.  et al. 2012. The Drosophila melanogaster Genetic Reference Panel. Nature 482:173–78 [Google Scholar]
  82. Magwire ML. 82.  2011. Addressing barriers to insulin therapy: the role of insulin pens. Am. J. Ther. 18:392–402 [Google Scholar]
  83. Magwire MM, Bayer F, Webster CL, Cao C, Jiggins FM. 83.  2011. Successive increases in the resistance of Drosophila to viral infection through a transposon insertion followed by a duplication. PLOS Genet. 7:e1002337 [Google Scholar]
  84. Makalowski W, Pande A, Gotea V, Makalowska I. 84.  2012. Transposable elements and their identification. Methods Mol. Biol. 855:337–59 [Google Scholar]
  85. Mateo L, Ullastres A, González JA. 85.  2014. A transposable element insertion confers xenobiotic resistance in Drosophila. PLOS Genet. 108e1004560 [Google Scholar]
  86. Maumus F, Quesneville H. 86.  2014. Deep investigation of Arabidopsis thaliana junk DNA reveals a continuum between repetitive elements and genomic dark matter. PLOS ONE 9:e94101 [Google Scholar]
  87. McCoy RC, Taylor RW, Blauwkamp TA, Kelley JL, Kertesz M. 87.  et al. 2014. Illumina TruSeq synthetic long-reads empower de novo assembly and resolve complex, highly repetitive transposable elements. PLOS ONE 99e106689 [Google Scholar]
  88. McDonald JF, Matyunina LV, Wilson S, Jordan IK, Bowen NJ, Miller WJ. 88.  1997. LTR retrotransposons and the evolution of eukaryotic enhancers. Genetica 100:3–13 [Google Scholar]
  89. Modolo L, Picard F, Lerat E. 89.  2014. A new genome-wide method to track horizontally transferred sequences: application to Drosophila. Genome Biol. Evol. 6:416–32 [Google Scholar]
  90. Montgomery E, Charlesworth B, Langley CH. 90.  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 [Google Scholar]
  91. Montgomery EA, Huang SM, Langley CH, Judd BH. 91.  1991. Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics 129:1085–98 [Google Scholar]
  92. Nuzhdin SV. 92.  1999. Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica 107:129–37 [Google Scholar]
  93. Nuzhdin SV, Pasyukova EG, Mackay TF. 93.  1997. Accumulation of transposable elements in laboratory lines of Drosophila melanogaster. Genetica 100:167–75 [Google Scholar]
  94. Permal E, Flutre T, Quesneville H. 94.  2012. Roadmap for annotating transposable elements in eukaryote genomes. Methods Mol. Biol. 859:53–68 [Google Scholar]
  95. Perrat PN, DasGupta S, Wang J, Theurkauf W, Weng Z. 95.  et al. 2013. Transposition-driven genomic heterogeneity in the Drosophila brain. Science 340:91–95 [Google Scholar]
  96. Petrov DA, Aminetzach YT, Davis JC, Bensasson D, Hirsh AE. 96.  2003. Size matters: non-LTR retrotransposable elements and ectopic recombination in Drosophila. Mol. Biol. Evol. 20:880–92 [Google Scholar]
  97. Petrov DA, Fiston-Lavier AS, Lipatov M, Lenkov K, Gonzalez J. 97.  2011. Population genomics of transposable elements in Drosophila melanogaster. Mol. Biol. Evol. 28:1633–44 [Google Scholar]
  98. Petrov DA, Hartl DL. 98.  1998. High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Mol. Biol. Evol. 15:293–302 [Google Scholar]
  99. Petrov DA, Lozovskaya ER, Hartl DL. 99.  1996. High intrinsic rate of DNA loss in Drosophila. Nature 384:346–49 [Google Scholar]
  100. Platzer A, Nizhynska V, Long Q. 100.  2012. TE-locate: a tool to locate and group transposable element occurrences using paired-end next-generation sequencing data. Biology 1:2395–410 [Google Scholar]
  101. Puig M, Caceres M, Ruiz A. 101.  2004. Silencing of a gene adjacent to the breakpoint of a widespread Drosophila inversion by a transposon-induced antisense RNA. Proc. Natl. Acad. Sci. USA 101:9013–18 [Google Scholar]
  102. Quesneville H, Bergman CM, Andrieu O, Autard D, Nouaud D. 102.  et al. 2005. Combined evidence annotation of transposable elements in genome sequences. PLOS Comput. Biol. 1:166–75 [Google Scholar]
  103. Robb SM, Lu L, Valencia E, Burnette JM 3rd, Okumoto Y. 103.  et al. 2013. The use of RelocaTE and unassembled short reads to produce high-resolution snapshots of transposable element generated diversity in rice. G3 3:949–57 [Google Scholar]
  104. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL. 104.  1998. The paleontology of intergene retrotransposons of maize. Nat. Genet. 20:43–45 [Google Scholar]
  105. Schmidt JM, Good RT, Appleton B, Sherrard J, Raymant GC. 105.  et al. 2010. Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLOS Genet. 6:e1000998 [Google Scholar]
  106. Sentmanat MF, Elgin SC. 106.  2012. Ectopic assembly of heterochromatin in Drosophila melanogaster triggered by transposable elements. Proc. Natl. Acad. Sci. USA 109:14104–9 [Google Scholar]
  107. Shapiro JA, Huang W, Zhang C, Hubisz MJ, Lu J. 107.  et al. 2007. Adaptive genic evolution in the Drosophila genomes. Proc. Natl. Acad. Sci. USA 104:2271–76 [Google Scholar]
  108. Singh ND, Petrov DA. 108.  2004. Rapid sequence turnover at an intergenic locus in Drosophila. Mol. Biol. Evol. 21:670–80 [Google Scholar]
  109. Sniegowski PD, Charlesworth B. 109.  1994. Transposable element numbers in cosmopolitan inversions from a natural population of Drosophila melanogaster. Genetics 137:815–27 [Google Scholar]
  110. Tajima F. 110.  1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–95 [Google Scholar]
  111. Tenaillon MI, Hufford MB, Gaut BS, Ross-Ibarra J. 111.  2011. Genome size and transposable element content as determined by high-throughput sequencing in maize and Zea luxurians.. Genome Biol. Evol. 3:219–29 [Google Scholar]
  112. Touchon M, Rocha EP. 112.  2007. Causes of insertion sequences abundance in prokaryotic genomes. Mol. Biol. Evol. 24:969–81 [Google Scholar]
  113. Vázquez JF, Albornoz J, Dominguez A. 113.  2007. Direct determination of the effects of genotype and extreme temperature on the transposition of roo in long-term mutation accumulation lines of Drosophila melanogaster. Mol. Genet. Genomics 278:653–64 [Google Scholar]
  114. Venner S, Feschotte C, Biemont C. 114.  2009. Dynamics of transposable elements: towards a community ecology of the genome. Trends Genet. 25:317–23 [Google Scholar]
  115. Voskoboynik A, Neff NF, Sahoo D, Newman AM, Pushkarev D. 115.  et al. 2013. The genome sequence of the colonial chordate, Botryllus schlosseri. Elife 2:e00569 [Google Scholar]
  116. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P. 116.  et al. 2007. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8:973–82 [Google Scholar]
  117. Yang HP, Nuzhdin SV. 117.  2003. Fitness costs of Doc expression are insufficient to stabilize its copy number in Drosophila melanogaster. Mol. Biol. Evol. 20:800–4 [Google Scholar]
  118. Zhang Z, Parsch J. 118.  2005. Positive correlation between evolutionary rate and recombination rate in Drosophila genes with male-biased expression. Mol. Biol. Evol. 22:1945–47 [Google Scholar]
/content/journals/10.1146/annurev-genet-120213-092359
Loading
/content/journals/10.1146/annurev-genet-120213-092359
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error