Mammalian transposable elements and their impacts on genome evolution

Roy N. Platt1, Michael W. Vandewege1, David A. Ray1
1Department of Biological Sciences, Texas Tech University, Lubbock, TX, USA

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Abrusán G, Krambeck HJ (2006) The distribution of L1 and Alu retroelements in relation to GC content on human sex chromosomes is consistent with the ectopic recombination model. J Mol Evol 63(4):484–492. https://doi.org/10.1007/s00239-005-0275-0

Alföldi J, di Palma F, Grabherr M, Williams C, Kong L, Mauceli E, Russell P, Lowe CB, Glor RE, Jaffe JD, Ray DA, Boissinot S, Shedlock AM, Botka C, Castoe TA, Colbourne JK, Fujita MK, Moreno RG, ten Hallers BF, Haussler D, Heger A, Heiman D, Janes DE, Johnson J, de Jong PJ, Koriabine MY, Lara M, Novick PA, Organ CL, Peach SE, Poe S, Pollock DD, de Queiroz K, Sanger T, Searle S, Smith JD, Smith Z, Swofford R, Turner-Maier J, Wade J, Young S, Zadissa A, Edwards SV, Glenn TC, Schneider CJ, Losos JB, Lander ES, Breen M, Ponting CP, Lindblad-Toh K (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477(7366):587–591. https://doi.org/10.1038/nature10390

Aravin A et al (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442:203

Aravin AA, Hannon GJ, Brennecke J (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318(5851):761–764. https://doi.org/10.1126/science.1146484

Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ (2008) A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31(6):785–799. https://doi.org/10.1016/j.molcel.2008.09.003

Baillie JK, Barnett MW, Upton KR, Gerhardt DJ, Richmond TA, de Sapio F, Brennan PM, Rizzu P, Smith S, Fell M, Talbot RT, Gustincich S, Freeman TC, Mattick JS, Hume DA, Heutink P, Carninci P, Jeddeloh JA, Faulkner GJ (2011) Somatic retrotransposition alters the genetic landscape of the human brain. Nature 479(7374):534–537. https://doi.org/10.1038/nature10531

Bennetzen JL, Kellogg EA (1997) Do plants have a one-way ticket to genomic obesity? Plant Cell 9(9):1509–1514. https://doi.org/10.1105/tpc.9.9.1509

Biémont C (2010) A brief history of the status of transposable elements: from junk DNA to major players in evolution. Genetics 186(4):1085–1093. https://doi.org/10.1534/genetics.110.124180

Bishop KN, Holmes RK, Sheehy AM, Davidson NO, Cho S-J, Malim MH (2004) Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr Biol 14(15):1392–1396. https://doi.org/10.1016/j.cub.2004.06.057

Bogerd HP, Wiegand HL, Doehle BP, Lueders KK, Cullen BR (2006) APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells. Nucleic Acids Res 34(1):89–95. https://doi.org/10.1093/nar/gkj416

Boissinot S, Roos C, Furano AV (2004) Different rates of LINE-1 (L1) retrotransposon amplification and evolution in New World monkeys. J Mol Evol 58(1):122–130. https://doi.org/10.1007/s00239-003-2539-x

Bourque G, Leong B, Vega VB, Chen X, Lee YL, Srinivasan KG, Chew JL, Ruan Y, Wei CL, Ng HH, Liu ET (2008) Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 18(11):1752–1762. https://doi.org/10.1101/gr.080663.108

Brandt J, Schrauth S, Veith AM, Froschauer A, Haneke T, Schultheis C, Gessler M, Leimeister C, Volff JN (2005) Transposable elements as a source of genetic innovation: expression and evolution of a family of retrotransposon-derived neogenes in mammals. Gene 345(1):101–111. https://doi.org/10.1016/j.gene.2004.11.022

Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV, Kazazian HH (2003) Hot L1s account for the bulk of retrotransposition in the human population. P Natl Acad Sci USA 100(9):5280–5285. https://doi.org/10.1073/pnas.0831042100

Burns KH, Boeke JD (2012) Human transposon tectonics. Cell 149(4):740–752. https://doi.org/10.1016/j.cell.2012.04.019

Cantrell MA, Scott L, Brown CJ, Martinez AR, Wichman HA (2008) Loss of LINE-1 activity in the megabats. Genetics 178(1):393–404. https://doi.org/10.1534/genetics.107.080275

Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, de Rooij DG, Hannon GJ (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12(4):503–514. https://doi.org/10.1016/j.devcel.2007.03.001

Casacuberta E, González J (2013) The impact of transposable elements in environmental adaptation. Mol Ecol 22(6):1503–1517. https://doi.org/10.1111/mec.12170

Chalopin D, Naville M, Plard F, Galiana D, Volff J-N (2015) Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates. Genome Biol Evol 7(2):567–580. https://doi.org/10.1093/gbe/evv005

Chen J, Greenblatt IM, Dellaporta SL (1992) Molecular analysis of Ac transposition and DNA replication. Genetics 130(3):665–676

Chénais B (2013) Transposable elements and human cancer: a causal relationship? Biochim Biophys Acta, Rev Cancer 1835(1):28–35. https://doi.org/10.1016/j.bbcan.2012.09.001

Cheng Z, Ventura M, She X, Khaitovich P, Graves T, Osoegawa K, Church D, DeJong P, Wilson RK, Pääbo S, Rocchi M, Eichler EE (2005) A genome-wide comparison of recent chimpanzee and human segmental duplications. Nature 437(7055):88–93. https://doi.org/10.1038/nature04000

Chuong EB, Elde NC, Feschotte C (2017) Regulatory activities of transposable elements: from conflicts to benefits. Nat Rev Genet 18:71

Churakov G, Sadasivuni MK, Rosenbloom KR, Huchon D, Brosius J, Schmitz J (2010) Rodent evolution: back to the root. Mol Biol Evol 27(6):1315–1326. https://doi.org/10.1093/molbev/msq019

Conticello SG (2008) The AID/APOBEC family of nucleic acid mutators. Genome Biol 9(6):229. https://doi.org/10.1186/gb-2008-9-6-229

Conticello SG, Thomas CJ, Petersen-Mahrt SK, Neuberger MS (2004) Evolution of the AID/APOBEC family of polynucleotide (deoxy) cytidine deaminases. Mol Biol Evol 22:367–377

Cowley M, Oakey RJ (2013) Transposable elements re-wire and fine-tune the transcriptome. PLoS Genet 9(1):e1003234. https://doi.org/10.1371/journal.pgen.1003234

de Koning AJ, Gu W, Castoe TA, Batzer MA, Pollock DD (2011) Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7(12):e1002384. https://doi.org/10.1371/journal.pgen.1002384

deHaro D, Kines KJ, Sokolowski M, Dauchy RT, Streva VA, Hill SM, Hanifin JP, Brainard GC, Blask DE, Belancio VP (2014) Regulation of L1 expression and retrotransposition by melatonin and its receptor: implications for cancer risk associated with light exposure at night. Nucleic Acids Res 42(12):7694–7707. https://doi.org/10.1093/nar/gku503

Denli AM, Narvaiza I, Kerman BE, Pena M, Benner C, Marchetto MCN, Diedrich JK, Aslanian A, Ma J, Moresco JJ, Moore L, Hunter T, Saghatelian A, Gage FH (2015) Primate-specific ORF0 contributes to retrotransposon-mediated diversity. Cell 163(3):583–593. https://doi.org/10.1016/j.cell.2015.09.025

Denne M, Sauter M, Armbruester V, Licht JD, Roemer K, Mueller-Lantzsch N (2007) Physical and functional interactions of human endogenous retrovirus proteins Np9 and rec with the promyelocytic leukemia zinc finger protein. J Virol 81(11):5607–5616. https://doi.org/10.1128/JVI.02771-06

Dupuy AJ, Akagi K, Largaespada DA, Copeland NG, Jenkins NA (2005) Mammalian mutagenesis using a highly mobile somatic Sleeping Beauty transposon system. Nature 436(7048):221–226. https://doi.org/10.1038/nature03691

Ecco G, Imbeault M, Trono D (2017) KRAB zinc finger proteins. Development 144(15):2719–2729. https://doi.org/10.1242/dev.132605

Eickbush T (1992) Transposing without ends: the non-LTR retrotransposable elements. New Biol 4(5):430–440

Eickbush TH, Jamburuthugoda VK (2008) The diversity of retrotransposons and the properties of their reverse transcriptases. Virus Res 134(1-2):221–234. https://doi.org/10.1016/j.virusres.2007.12.010

Eickbush TH, Malik HS (2002) Origins and evolution of retrotransposons. In: Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) Mobile DNA II. ASM Press, Washington D.C., pp. 1111–1144.

Elsik CG, Tellam RL, Worley KC (2009) The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324(5926):522–528. https://doi.org/10.1126/science.1169588

Emerson RO, Thomas JH (2009) Adaptive evolution in zinc finger transcription factors. PLoS Genet 5(1):e1000325. https://doi.org/10.1371/journal.pgen.1000325

Evrony GD, Lee E, Park PJ, Walsh CA (2016) Resolving rates of mutation in the brain using single-neuron genomics. Elife 5:e12966

Fanning TG (1983) Size and structure of the highly repetitive BAM HI element in mice. Nucleic Acids Res 11(15):5073–5091. https://doi.org/10.1093/nar/11.15.5073

Feschotte C, Gilbert C (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13(4):283–296. https://doi.org/10.1038/nrg3199

Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41(1):331–368. https://doi.org/10.1146/annurev.genet.40.110405.090448

Finnegan DJ (1989) Eukaryotic transposable elements and genome evolution. Trends Genet 5(4):103–107. https://doi.org/10.1016/0168-9525(89)90039-5

Flemr M, Malik R, Franke V, Nejepinska J, Sedlacek R, Vlahovicek K, Svoboda P (2013) A retrotransposon-driven dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell 155(4):807–816. https://doi.org/10.1016/j.cell.2013.10.001

Franke V, Ganesh S, Karlic R, Malik R, Pasulka J, Horvat F, Kuzman M, Fulka H, Cernohorska M, Urbanova J, Svobodova E, Ma J, Suzuki Y, Aoki F, Schultz RM, Vlahovicek K, Svoboda P (2017) Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes. Genome Res 27:1384–1394. https://doi.org/10.1101/gr.216150.116

Friedli M, Trono D (2015) The developmental control of transposable elements and the evolution of higher species. Annu Rev Cell Dev Bi 31(1):429–451. https://doi.org/10.1146/annurev-cellbio-100814-125514

Ge R-L, Cai Q, Shen YY, San A, Ma L, Zhang Y, Yi X, Chen Y, Yang L, Huang Y, He R, Hui Y, Hao M, Li Y, Wang B, Ou X, Xu J, Zhang Y, Wu K, Geng C, Zhou W, Zhou T, Irwin DM, Yang Y, Ying L, Bao H, Kim J, Larkin DM, Ma J, Lewin HA, Xing J, Platt RN, Ray DA, Auvil L, Capitanu B, Zhang X, Zhang G, Murphy RW, Wang J, Zhang YP, Wang J (2013) Draft genome sequence of the Tibetan antelope. Nat Commun 4:1858. https://doi.org/10.1038/ncomms2860

Gerdes P, Richardson SR, Mager DL, Faulkner GJ (2016) Transposable elements in the mammalian embryo: pioneers surviving through stealth and service. Genome Biol 17(1):100. https://doi.org/10.1186/s13059-016-0965-5

Gladyshev EA, Arkhipova IR (2011) A widespread class of reverse transcriptase-related cellular genes. P Natl Acad Sci USA 108(51):20311–20316. https://doi.org/10.1073/pnas.1100266108

Gogolevsky KP, Vassetzky NS, Kramerov DA (2008) Bov-B-mobilized SINEs in vertebrate genomes. Gene 407(1-2):75–85. https://doi.org/10.1016/j.gene.2007.09.021

Gogolevsky KP, Vassetzky NS, Kramerov DA (2009) 5S rRNA-derived and tRNA-derived SINEs in fruit bats. Genomics 93(5):494–500. https://doi.org/10.1016/j.ygeno.2009.02.001

Goodier JL (2016) Restricting retrotransposons: a review. Mob DNA 7(1):16. https://doi.org/10.1186/s13100-016-0070-z

Grahn R, Rinehart T, Cantrell M, Wichman H (2005) Extinction of LINE-1 activity coincident with a major mammalian radiation in rodents. Cytogenet Genome Res 110(1-4):407–415. https://doi.org/10.1159/000084973

Green RE, Braun EL, Armstrong J, Earl D, Nguyen N, Hickey G, Vandewege MW, St. John JA, Capella-Gutierrez S, Castoe TA, Kern C, Fujita MK, Opazo JC, Jurka J, Kojima KK, Caballero J, Hubley RM, Smit AF, Platt RN, Lavoie CA, Ramakodi MP, Finger JW, Suh A, Isberg SR, Miles L, Chong AY, Jaratlerdsiri W, Gongora J, Moran C, Iriarte A, McCormack J, Burgess SC, Edwards SV, Lyons E, Williams C, Breen M, Howard JT, Gresham CR, Peterson DG, Schmitz J, Pollock DD, Haussler D, Triplett EW, Zhang G, Irie N, Jarvis ED, Brochu CA, Schmidt CJ, McCarthy FM, Faircloth BC, Hoffmann FG, Glenn TC, Gabaldon T, Paten B, Ray DA (2014) Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science 346(6215):1254449. https://doi.org/10.1126/science.1254449

Grimaldi G, Skowronski J, Singer MF (1984) Defining the beginning and end of KpnI family segments. EMBO J 3:1753

Hancks DC, Kazazian HH (2016) Roles for retrotransposon insertions in human disease. Mob DNA 7(1):9. https://doi.org/10.1186/s13100-016-0065-9

Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, Watt IN, Neuberger MS, Malim MH (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113(6):803–809. https://doi.org/10.1016/S0092-8674(03)00423-9

Herédia F, Loreto ELS, Valente VLS (2004) Complex evolution of gypsy in Drosophilid species. Mol Biol Evol 21(10):1831–1842. https://doi.org/10.1093/molbev/msh183

Hillier LW et al (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432(7018):695–716. https://doi.org/10.1038/nature03154

Ito H et al (2016) A stress-activated transposon in Arabidopsis induces transgenerational abscisic acid insensitivity. Sci Rep 6:srep23181

Jeffs AR, Benjes SM, Smith TL, Sowerby SJ, Morris CM (1998) The BCR gene recombines preferentially with Alu elements in complex BCR-ABL translocations of chronic myeloid leukaemia. Hum Mol Genet 7(5):767–776. https://doi.org/10.1093/hmg/7.5.767

Jurka J, Kohany O, Pavlicek A, Kapitonov VV, Jurka MV (2004) Duplication, coclustering, and selection of human Alu retrotransposons. P Natl Acad Sci USA 101(5):1268–1272. https://doi.org/10.1073/pnas.0308084100

Kale SP, Moore L, Deininger PL, Roy-Engel AM (2005) Heavy metals stimulate human LINE-1 retrotransposition. Int J Env Res Pub He 2(1):14–23. https://doi.org/10.3390/ijerph2005010014

Kapitonov VV, Jurka J (2001) Rolling-circle transposons in eukaryotes. P Natl Acad Sci USA 98(15):8714–8719. https://doi.org/10.1073/pnas.151269298

Kapitonov VV, Jurka J (2007) Helitrons on a roll: eukaryotic rolling-circle transposons. Trends Genet 23(10):521–529. https://doi.org/10.1016/j.tig.2007.08.004

Kinomoto M, Kanno T, Shimura M, Ishizaka Y, Kojima A, Kurata T, Sata T, Tokunaga K (2007) All APOBEC3 family proteins differentially inhibit LINE-1 retrotransposition. Nucleic Acids Res 35(9):2955–2964. https://doi.org/10.1093/nar/gkm181

Koonin EV, Mushegian AR, Ryabov EV, Dolja VV (1991) Diverse groups of plant RNA and DNA viruses share related movement proteins that may possess chaperone-like activity. J Gen Virol 72(12):2895–2903. https://doi.org/10.1099/0022-1317-72-12-2895

Kordis D, Gubensek F (1998) Unusual horizontal transfer of a long interspersed nuclear element between distant vertebrate classes. P Natl Acad Sci USA 95(18):10704–10709. https://doi.org/10.1073/pnas.95.18.10704

Kramerov D, Vassetzky N (2011) Origin and evolution of SINEs in eukaryotic genomes. Heredity 107(6):487–495. https://doi.org/10.1038/hdy.2011.43

Kriegs JO, Churakov G, Jurka J, Brosius J, Schmitz J (2007) Evolutionary history of 7SL RNA-derived SINEs in Supraprimates. Trends Genet 23(4):158–161. https://doi.org/10.1016/j.tig.2007.02.002

Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, Lin H, Matsuda Y, Nakano T (2004) Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131(4):839–849. https://doi.org/10.1242/dev.00973

Kvikstad EM, Makova KD (2010) The (r) evolution of SINE versus LINE distributions in primate genomes: sex chromosomes are important. Genome Res 20(5):600–613. https://doi.org/10.1101/gr.099044.109

Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, Stange-Thomann Y, Stojanovic N, Subramanian A, Wyman D, Rogers J, Sulston J, Ainscough R, Beck S, Bentley D, Burton J, Clee C, Carter N, Coulson A, Deadman R, Deloukas P, Dunham A, Dunham I, Durbin R, French L, Grafham D, Gregory S, Hubbard T, Humphray S, Hunt A, Jones M, Lloyd C, McMurray A, Matthews L, Mercer S, Milne S, Mullikin JC, Mungall A, Plumb R, Ross M, Shownkeen R, Sims S, Waterston RH, Wilson RK, Hillier LW, McPherson JD, Marra MA, Mardis ER, Fulton LA, Chinwalla AT, Pepin KH, Gish WR, Chissoe SL, Wendl MC, Delehaunty KD, Miner TL, Delehaunty A, Kramer JB, Cook LL, Fulton RS, Johnson DL, Minx PJ, Clifton SW, Hawkins T, Branscomb E, Predki P, Richardson P, Wenning S, Slezak T, Doggett N, Cheng JF, Olsen A, Lucas S, Elkin C, Uberbacher E, Frazier M, Gibbs RA, Muzny DM, Scherer SE, Bouck JB, Sodergren EJ, Worley KC, Rives CM, Gorrell JH, Metzker ML, Naylor SL, Kucherlapati RS, Nelson DL, Weinstock GM, Sakaki Y, Fujiyama A, Hattori M, Yada T, Toyoda A, Itoh T, Kawagoe C, Watanabe H, Totoki Y, Taylor T, Weissenbach J, Heilig R, Saurin W, Artiguenave F, Brottier P, Bruls T, Pelletier E, Robert C, Wincker P, Smith DR, Doucette-Stamm L, Rubenfield M, Weinstock K, Lee HM, Dubois J, Rosenthal A, Platzer M, Nyakatura G, Taudien S, Rump A, Yang H, Yu J, Wang J, Huang G, Gu J, Hood L, Rowen L, Madan A, Qin S, Davis RW, Federspiel NA, Abola AP, Proctor MJ, Myers RM, Schmutz J, Dickson M, Grimwood J, Cox DR, Olson MV, Kaul R, Raymond C, Shimizu N, Kawasaki K, Minoshima S, Evans GA, Athanasiou M, Schultz R, Roe BA, Chen F, Pan H, Ramser J, Lehrach H, Reinhardt R, McCombie WR, de la Bastide M, Dedhia N, Blöcker H, Hornischer K, Nordsiek G, Agarwala R, Aravind L, Bailey JA, Bateman A, Batzoglou S, Birney E, Bork P, Brown DG, Burge CB, Cerutti L, Chen HC, Church D, Clamp M, Copley RR, Doerks T, Eddy SR, Eichler EE, Furey TS, Galagan J, Gilbert JG, Harmon C, Hayashizaki Y, Haussler D, Hermjakob H, Hokamp K, Jang W, Johnson LS, Jones TA, Kasif S, Kaspryzk A, Kennedy S, Kent WJ, Kitts P, Koonin EV, Korf I, Kulp D, Lancet D, Lowe TM, McLysaght A, Mikkelsen T, Moran JV, Mulder N, Pollara VJ, Ponting CP, Schuler G, Schultz J, Slater G, Smit AF, Stupka E, Szustakowki J, Thierry-Mieg D, Thierry-Mieg J, Wagner L, Wallis J, Wheeler R, Williams A, Wolf YI, Wolfe KH, Yang SP, Yeh RF, Collins F, Guyer MS, Peterson J, Felsenfeld A, Wetterstrand KA, Patrinos A, Morgan MJ, de Jong P, Catanese JJ, Osoegawa K, Shizuya H, Choi S, Chen YJ, Szustakowki J (2001) Initial sequencing of the human genome. Nature 409:860–921. https://doi.org/10.1038/35057062

Larsen PA, Lutz MW, Hunnicutt KE, Mihovilovic M, Saunders AM, Yoder AD, Roses AD (2017) The Alu neurodegeneration hypothesis: a primate-specific mechanism for neuronal transcription noise, mitochondrial dysfunction, and manifestation of neurodegenerative disease. Alzheimers Dement 13(7):828–838. https://doi.org/10.1016/j.jalz.2017.01.017

Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, Kingston RE (2006) Characterization of the piRNA complex from rat testes. Science 313(5785):363–367. https://doi.org/10.1126/science.1130164

Leis J, Aiyar A, Cobrinik D (1993) Regulation of initiation of reverse transcription of retroviruses. Cold Spring Harbor M 23:33–33

Levin HL (1995) A novel mechanism of self-primed reverse transcription defines a new family of retroelements. Mol Cell Biol 15(6):3310–3317. https://doi.org/10.1128/MCB.15.6.3310

Li W, Jin Y, Prazak L, Hammell M, Dubnau J (2012) Transposable elements in TDP-43-mediated neurodegenerative disorders. PLoS One 7(9):e44099. https://doi.org/10.1371/journal.pone.0044099

Liu H, Chang L-H, Sun Y, Lu X, Stubbs L (2014) Deep vertebrate roots for mammalian zinc finger transcription factor subfamilies. Genome Biol Evol 6(3):510–525. https://doi.org/10.1093/gbe/evu030

Lowe CB, Haussler D (2012) 29 mammalian genomes reveal novel exaptations of mobile elements for likely regulatory functions in the human genome. PLoS One 7(8):e43128. https://doi.org/10.1371/journal.pone.0043128

Lupan I, Bulzu P, Popescu O, Damert A (2015) Lineage specific evolution of the VNTR composite retrotransposon central domain and its role in retrotransposition of gibbon LAVA elements. BMC Genomics 16(1):389. https://doi.org/10.1186/s12864-015-1543-z

Lynch M, Conery JS (2003) The origins of genome complexity. Science 302(5649):1401–1404. https://doi.org/10.1126/science.1089370

Lynch M, Conery J, Burger R (1995) Mutation accumulation and the extinction of small populations. Amer Nat 146(4):489–518. https://doi.org/10.1086/285812

Lynch VJ, Leclerc RD, May G, Wagner GP (2011) Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet 43(11):1154–1159. https://doi.org/10.1038/ng.917

Lynch VJ, Nnamani MC, Kapusta A, Brayer K, Plaza SL, Mazur EC, Emera D, Sheikh SZ, Grützner F, Bauersachs S, Graf A, Young SL, Lieb JD, DeMayo FJ, Feschotte C, Wagner GP (2015) Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep 10(4):551–561. https://doi.org/10.1016/j.celrep.2014.12.052

Maksakova IA, Romanish MT, Gagnier L, Dunn CA, Van de Lagemaat LN, Mager DL (2006) Retroviral elements and their hosts: insertional mutagenesis in the mouse germ line. PLoS Genet 2(1):e2. https://doi.org/10.1371/journal.pgen.0020002

Mangeat B, Turelli P, Caron G, Friedli M (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424(6944):99–103. https://doi.org/10.1038/nature01709

Marques-Bonet T, Girirajan S, Eichler EE (2009) The origins and impact of primate segmental duplications. Trends Genet 25(10):443–454. https://doi.org/10.1016/j.tig.2009.08.002

Martinez G, Choudury SG, Slotkin RK (2017) tRNA-derived small RNAs target transposable element transcripts. Nucleic Acids Res 45(9):5142–5152. https://doi.org/10.1093/nar/gkx103

McClintock B (1984) The significance of responses of the genome to challenge. Science 226(4676):792–801. https://doi.org/10.1126/science.15739260

Medstrand P, Van De Lagemaat LN, Mager DL (2002) Retroelement distributions in the human genome: variations associated with age and proximity to genes. Genome Res 12(10):1483–1495. https://doi.org/10.1101/gr.388902

Meredith RW, Janecka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simao TLL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ (2011) Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334(6055):521–524. https://doi.org/10.1126/science.1211028

Mi S, Lee X, Xiang-ping L, Veldman GM (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403(6771):785–789. https://doi.org/10.1038/35001608

Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, Garber M, Gentles AJ, Goodstadt L, Heger A, Jurka J, Kamal M, Mauceli E, Searle SMJ, Sharpe T, Baker ML, Batzer MA, Benos PV, Belov K, Clamp M, Cook A, Cuff J, Das R, Davidow L, Deakin JE, Fazzari MJ, Glass JL, Grabherr M, Greally JM, Gu W, Hore TA, Huttley GA, Kleber M, Jirtle RL, Koina E, Lee JT, Mahony S, Marra MA, Miller RD, Nicholls RD, Oda M, Papenfuss AT, Parra ZE, Pollock DD, Ray DA, Schein JE, Speed TP, Thompson K, VandeBerg JL, Wade CM, Walker JA, Waters PD, Webber C, Weidman JR, Xie X, Zody MC, Baldwin J, Abdouelleil A, Abdulkadir J, Abebe A, Abera B, Abreu J, Acer SC, Aftuck L, Alexander A, An P, Anderson E, Anderson S, Arachi H, Azer M, Bachantsang P, Barry A, Bayul T, Berlin A, Bessette D, Bloom T, Blye J, Boguslavskiy L, Bonnet C, Boukhgalter B, Bourzgui I, Brown A, Cahill P, Channer S, Cheshatsang Y, Chuda L, Citroen M, Collymore A, Cooke P, Costello M, D'Aco K, Daza R, de Haan G, DeGray S, DeMaso C, Dhargay N, Dooley K, Dooley E, Doricent M, Dorje P, Dorjee K, Dupes A, Elong R, Falk J, Farina A, Faro S, Ferguson D, Fisher S, Foley CD, Franke A, Friedrich D, Gadbois L, Gearin G, Gearin CR, Giannoukos G, Goode T, Graham J, Grandbois E, Grewal S, Gyaltsen K, Hafez N, Hagos B, Hall J, Henson C, Hollinger A, Honan T, Huard MD, Hughes L, Hurhula B, Husby ME, Kamat A, Kanga B, Kashin S, Khazanovich D, Kisner P, Lance K, Lara M, Lee W, Lennon N, Letendre F, LeVine R, Lipovsky A, Liu X, Liu J, Liu S, Lokyitsang T, Lokyitsang Y, Lubonja R, Lui A, MacDonald P, Magnisalis V, Maru K, Matthews C, McCusker W, McDonough S, Mehta T, Meldrim J, Meneus L, Mihai O, Mihalev A, Mihova T, Mittelman R, Mlenga V, Montmayeur A, Mulrain L, Navidi A, Naylor J, Negash T, Nguyen T, Nguyen N, Nicol R, Norbu C, Norbu N, Novod N, O'Neill B, Osman S, Markiewicz E, Oyono OL, Patti C, Phunkhang P, Pierre F, Priest M, Raghuraman S, Rege F, Reyes R, Rise C, Rogov P, Ross K, Ryan E, Settipalli S, Shea T, Sherpa N, Shi L, Shih D, Sparrow T, Spaulding J, Stalker J, Stange-Thomann N, Stavropoulos S, Stone C, Strader C, Tesfaye S, Thomson T, Thoulutsang Y, Thoulutsang D, Topham K, Topping I, Tsamla T, Vassiliev H, Vo A, Wangchuk T, Wangdi T, Weiand M, Wilkinson J, Wilson A, Yadav S, Young G, Yu Q, Zembek L, Zhong D, Zimmer A, Zwirko Z, Jaffe DB, Alvarez P, Brockman W, Butler J, Chin CW, Gnerre S, MacCallum I, Graves JAM, Ponting CP, Breen M, Samollow PB, Lander ES, Lindblad-Toh K (2007) Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447(7141):167–177. https://doi.org/10.1038/nature05805

Miller W, Drautz DI, Ratan A, Pusey B, Qi J, Lesk AM, Tomsho LP, Packard MD, Zhao F, Sher A, Tikhonov A, Raney B, Patterson N, Lindblad-Toh K, Lander ES, Knight JR, Irzyk GP, Fredrikson KM, Harkins TT, Sheridan S, Pringle T, Schuster SC (2008) Sequencing the nuclear genome of the extinct woolly mammoth. Nature 456(7220):387–390. https://doi.org/10.1038/nature07446

Molaro A, Falciatori I, Hodges E, Aravin AA, Marran K, Rafii S, McCombie WR, Smith AD, Hannon GJ (2014) Two waves of de novo methylation during mouse germ cell development. Genes Dev 28(14):1544–1549. https://doi.org/10.1101/gad.244350.114

Morse B, Rotherg PG, South VJ, Spandorfer JM, Astrin SM (1988) Insertional mutagenesis of the myc locus by a LINE-1 sequence in a human breast carcinoma. Nature 333(6168):87–90. https://doi.org/10.1038/333087a0

Muotri AR, Zhao C, Marchetto MC, Gage FH (2009) Environmental influence on L1 retrotransposons in the adult hippocampus. Hippocampus 19(10):1002–1007. https://doi.org/10.1002/hipo.20564

Nekrutenko A, Li W-H (2001) Transposable elements are found in a large number of human protein-coding genes. Trends Genet 17(11):619–621. https://doi.org/10.1016/S0168-9525(01)02445-3

Nikaido M, Nishihara H, Hukumoto Y, Okada N (2003) Ancient SINEs from African endemic mammals. Mol Biol Evol 20(4):522–527. https://doi.org/10.1093/molbev/msg052

Nilsson MA (2016) The devil is in the details: transposable element analysis of the Tasmanian devil genome. Mobile Genet Elem 6(1):e1119926. https://doi.org/10.1080/2159256X.2015.1119926

Nishihara H, Kobayashi N, Kimura-Yoshida C, Yan K, Bormuth O, Ding Q, Nakanishi A, Sasaki T, Hirakawa M, Sumiyama K, Furuta Y, Tarabykin V, Matsuo I, Okada N (2016) Coordinately co-opted multiple transposable elements constitute an enhancer for wnt5a expression in the mammalian secondary palate. PLoS Genet 12(10):e1006380. https://doi.org/10.1371/journal.pgen.1006380

Novick P, Smith J, Ray D, Boissinot S (2010) Independent and parallel lateral transfer of DNA transposons in tetrapod genomes. Gene 449(1-2):85–94. https://doi.org/10.1016/j.gene.2009.08.017

Nowick K, Hamilton AT, Zhang H, Stubbs L (2010) Rapid sequence and expression divergence suggest selection for novel function in primate-specific KRAB-ZNF genes. Mol Biol Evol 27(11):2606–2617. https://doi.org/10.1093/molbev/msq157

Nozawa K, Kawagishi Y, Kawabe A, Sato M, Masuta Y, Kato A, Ito H (2017) Epigenetic regulation of a heat-activated retrotransposon in cruciferous vegetables. Epigenomes 1(1):7. https://doi.org/10.3390/epigenomes1010007

Ohno S (1970) Evolution by gene duplication. Springer, New York. https://doi.org/10.1007/978-3-642-86659-3

Oliver KR, Greene WK (2011) Mobile DNA and the TE-Thrust hypothesis: supporting evidence from the primates. Mob DNA 2(1):8. https://doi.org/10.1186/1759-8753-2-8

O'Neil J, Tchinda J, Gutierrez A, Moreau L, Maser RS, Wong KK, Li W, McKenna K, Liu XS, Feng B, Neuberg D, Silverman L, DeAngelo DJ, Kutok JL, Rothstein R, DePinho RA, Chin L, Lee C, Look AT (2007) Alu elements mediate MYB gene tandem duplication in human T-ALL. J Exp Med 204(13):3059–3066. https://doi.org/10.1084/jem.20071637

Ostertag EM, Kazazian HH Jr (2001) Biology of mammalian L1 retrotransposons. Annu Rev Genet 35(1):501–538. https://doi.org/10.1146/annurev.genet.35.102401.091032

Pace JK, Feschotte C (2007) The evolutionary history of human DNA transposons: evidence for intense activity in the primate lineage. Genome Res 17(4):422–432. https://doi.org/10.1101/gr.5826307

Pace JK, Gilbert C, Clark MS, Feschotte C (2008) Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods. P Natl Acad Sci USA 105(44):17023–17028. https://doi.org/10.1073/pnas.0806548105

Pagan HJ, Smith JD, Hubley RM, Ray DA (2010) PiggyBac-ing on a primate genome: novel elements, recent activity and horizontal transfer. Genome Biol Evol 2(0):293–303. https://doi.org/10.1093/gbe/evq021

Pagán HJ, Macas J, Novák P, McCulloch ES, Stevens RD, Ray DA (2012) Survey sequencing reveals elevated DNA transposon activity, novel elements, and variation in repetitive landscapes among vesper bats. Genome Biol Evol 4(4):575–585. https://doi.org/10.1093/gbe/evs038

Peccoud J, Loiseau V, Cordaux R, Gilbert C (2017) Massive horizontal transfer of transposable elements in insects. P Natl Acad Sci USA 114(18):4721–4726. https://doi.org/10.1073/pnas.1621178114

Platt RN II, Ray DA (2012) A non-LTR retroelement extinction in Spermophilus tridecemlineatus. Gene 500(1):47–53. https://doi.org/10.1016/j.gene.2012.03.051

Platt RN II, Vandewege MW, Kern C, Schmidt CJ, Hoffmann FG, Ray DA (2014) Large numbers of novel miRNAs originate from DNA transposons and are coincident with a large species radiation in bats. Mol Biol Evol 31(6):1536–1545. https://doi.org/10.1093/molbev/msu112

Platt RN II, Blanco-Berdugo L, Ray DA (2016a) Accurate transposable element annotation is vital when analyzing new genome assemblies. Genome Biol Evol 8(2):403–410. https://doi.org/10.1093/gbe/evw009

Platt RN II, Mangum SF, Ray DA (2016b) Pinpointing the vesper bat transposon revolution using the Miniopterus natalensis genome. Mob DNA 7(1):12. https://doi.org/10.1186/s13100-016-0071-y

Pritham EJ, Feschotte C (2007) Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus. P Natl Acad Sci USA 104(6):1895–1900. https://doi.org/10.1073/pnas.0609601104

Ray DA, Pagan HJ, Thompson ML, Stevens RD (2006) Bats with hAT s: evidence for recent DNA transposon activity in genus Myotis. Mol Biol Evol 24(3):632–639. https://doi.org/10.1093/molbev/msl192

Ray DA, Feschotte C, Pagan HJ, Smith JD, Pritham EJ, Arensburger P, Atkinson PW, Craig NL (2008) Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus. Genome Res 18:717–728. https://doi.org/10.1101/gr.071886.107

Ray DA, Pagan HJ, Platt RN II, Kroll AR, Schaack S, Stevens RD (2015) Differential SINE evolution in vesper and non-vesper bats. Mob DNA 6(1):10. https://doi.org/10.1186/s13100-015-0038-4

Reilly MT, Faulkner GJ, Dubnau J, Ponomarev I, Gage FH (2013) The role of transposable elements in health and diseases of the central nervous system. J Neurosci 33(45):17577–17586. https://doi.org/10.1523/JNEUROSCI.3369-13.2013

Richardson SR, Narvaiza I, Planegger RA, Weitzman MD, Moran JV (2014) APOBEC3A deaminates transiently exposed single-strand DNA during LINE-1 retrotransposition. Elife 3:e02008

Rinehart T, Grahn R, Wichman H (2005) SINE extinction preceded LINE extinction in sigmodontine rodents: implications for retrotranspositional dynamics and mechanisms. Cytogenet Genome Res 110(1-4):416–425. https://doi.org/10.1159/000084974

Rogers RL, Slatkin M (2017) Excess of genomic defects in a woolly mammoth on Wrangel island. PLoS Genet 13(3):e1006601. https://doi.org/10.1371/journal.pgen.1006601

Rogozin IB, Iyer LM, Liang L, Glazko GV, Liston VG, Pavlov YI, Aravind L, Pancer Z (2007) Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nat Immunol 8(6):647–656. https://doi.org/10.1038/ni1463

Rowe G, Beebee TJ (2003) Population on the verge of a mutational meltdown? Fitness costs of genetic load for an amphibian in the wild. Evolution 57(1):177–181. https://doi.org/10.1111/j.0014-3820.2003.tb00228.x

Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, Maillard PV, Layard-Liesching H, Verp S, Marquis J, Spitz F, Constam DB, Trono D (2010) KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463(7278):237–240. https://doi.org/10.1038/nature08674

Sawyer SL, Emerman M, Malik HS (2004) Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2(9):e275. https://doi.org/10.1371/journal.pbio.0020275

Schorn AJ, Gutbrod MJ, LeBlanc C, Martienssen R (2017) LTR-retrotransposon control by tRNA-derived small RNAs. Cell 170(1):61–71.e11. https://doi.org/10.1016/j.cell.2017.06.013

Schrader L, Kim JW, Ence D, Zimin A, Klein A, Wyschetzki K, Weichselgartner T, Kemena C, Stökl J, Schultner E, Wurm Y, Smith CD, Yandell M, Heinze J, Gadau J, Oettler J (2014) Transposable element islands facilitate adaptation to novel environments in an invasive species. Nat Commun 5:5495. https://doi.org/10.1038/ncomms6495

Schumann G (2007) APOBEC3 proteins: major players in intracellular defence against LINE-1 mediated retrotransposition. Biochem Soc Trans. 35:637–642. https://doi.org/10.1042/BST0350637

Scott EC, Gardner EJ, Masood A, Chuang NT, Vertino PM, Devine SE (2016) A hot L1 retrotransposon evades somatic repression and initiates human colorectal cancer. Genome Res 26(6):745–755. https://doi.org/10.1101/gr.201814.115

Shimamura M, Abe H, Nikaido M, Ohshima K, Okada N (1999) Genealogy of families of SINEs in cetaceans and artiodactyls: the presence of a huge superfamily of tRNA (Glu)-derived families of SINEs. Mol Biol Evol 16(8):1046–1060. https://doi.org/10.1093/oxfordjournals.molbev.a026194

Smit AF (1993) Identification of a new, abundant superfamily of mammalian LTR-transposons. Nucleic Acids Res 21(8):1863–1872. https://doi.org/10.1093/nar/21.8.1863

Smit AF, Tóth G, Riggs AD, Jurka J (1995) Ancestral, mammalian-wide subfamilies of LINE-1 repetitive sequences. J Mol Biol 246(3):401–417. https://doi.org/10.1006/jmbi.1994.0095

Sotero-Caio CG, Platt RN II, Suh A, Ray DA (2017) Evolution and diversity of transposable elements in vertebrate genomes. Genome Biol Evol 9(1):161–177. https://doi.org/10.1093/gbe/evw264

Stapley J, Santure AW, Dennis SR (2015) Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species. Mol Ecol 24(9):2241–2252. https://doi.org/10.1111/mec.13089

Stoebel DM, Dorman CJ (2010) The effect of mobile element IS 10 on experimental regulatory evolution in Escherichia coli. Mol Biol Evol 27(9):2105–2112. https://doi.org/10.1093/molbev/msq101

Stribinskis V, Ramos KS (2006) Activation of human long interspersed nuclear element 1 retrotransposition by benzo (a) pyrene, an ubiquitous environmental carcinogen. Cancer Res 66(5):2616–2620. https://doi.org/10.1158/0008-5472.CAN-05-3478

Strout MP, Marcucci G, Bloomfield CD, Caligiuri MA (1998) The partial tandem duplication of ALL1 (MLL) is consistently generated by Alu-mediated homologous recombination in acute myeloid leukemia. P Natl Acad Sci USA 95(5):2390–2395. https://doi.org/10.1073/pnas.95.5.2390

Suh A, Churakov G, Ramakodi MP, Platt RN 2nd, Jurka J, Kojima KK, Caballero J, Smit AF, Vliet KA, Hoffmann FG, Brosius J, Green RE, Braun EL, Ray DA, Schmitz J (2014) Multiple lineages of ancient CR1 retroposons shaped the early genome evolution of amniotes. Genome Biol Evol 7(1):205–217. https://doi.org/10.1093/gbe/evu256

Swerdlow RH, Khan SM (2004) A “mitochondrial cascade hypothesis” for sporadic Alzheimer's disease. Med Hypotheses 63(1):8–20. https://doi.org/10.1016/j.mehy.2003.12.045

Thomas JH, Schneider S (2011) Coevolution of retroelements and tandem zinc finger genes. Genome Res 21(11):1800–1812. https://doi.org/10.1101/gr.121749.111

Thomas J, Sorourian M, Ray D, Baker RJ, Pritham EJ (2011) The limited distribution of Helitrons to vesper bats supports horizontal transfer. Gene 474(1-2):52–58. https://doi.org/10.1016/j.gene.2010.12.007

Urrutia R (2003) KRAB-containing zinc-finger repressor proteins. Genome Biol 4(10):231. https://doi.org/10.1186/gb-2003-4-10-231

van de Lagemaat LN, Landry J-R, Mager DL, Medstrand P (2003) Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet 19(10):530–536. https://doi.org/10.1016/j.tig.2003.08.004

Vandewege MW, Platt RN II, Ray DA, Hoffmann FG (2016) Transposable element targeting by piRNAs in Laurasiatherians with distinct transposable element histories. Genome Biol Evol 8(5):1327–1337. https://doi.org/10.1093/gbe/evw078

Vassetzky NS, Kramerov DA (2002) CAN—a pan-carnivore SINE family. Mamm Genome 13(1):50–57. https://doi.org/10.1007/s00335-001-2111-1

Walsh AM, Kortschak RD, Gardner MG, Bertozzi T, Adelson DL (2013) Widespread horizontal transfer of retrotransposons. P Natl Acad Sci USA 110(3):1012–1016. https://doi.org/10.1073/pnas.1205856110

Wang W, Kirkness EF (2005) Short interspersed elements (SINEs) are a major source of canine genomic diversity. Genome Res 15(12):1798–1808. https://doi.org/10.1101/gr.3765505

Wang H, Xing J, Grover D, Hedges DJ, Han K, Walker JA, Batzer MA (2005) SVA elements: a hominid-specific retroposon family. J Mol Biol 354(4):994–1007. https://doi.org/10.1016/j.jmb.2005.09.085

Warren WC, Hillier LW, Marshall Graves JA, Birney E, Ponting CP, Grützner F, Belov K, Miller W, Clarke L, Chinwalla AT, Yang SP, Heger A, Locke DP, Miethke P, Waters PD, Veyrunes F, Fulton L, Fulton B, Graves T, Wallis J, Puente XS, López-Otín C, Ordóñez GR, Eichler EE, Chen L, Cheng Z, Deakin JE, Alsop A, Thompson K, Kirby P, Papenfuss AT, Wakefield MJ, Olender T, Lancet D, Huttley GA, Smit AF, Pask A, Temple-Smith P, Batzer MA, Walker JA, Konkel MK, Harris RS, Whittington CM, Wong ES, Gemmell NJ, Buschiazzo E, Vargas Jentzsch IM, Merkel A, Schmitz J, Zemann A, Churakov G, Kriegs JO, Brosius J, Murchison EP, Sachidanandam R, Smith C, Hannon GJ, Tsend-Ayush E, McMillan D, Attenborough R, Rens W, Ferguson-Smith M, Lefèvre CM, Sharp JA, Nicholas KR, Ray DA, Kube M, Reinhardt R, Pringle TH, Taylor J, Jones RC, Nixon B, Dacheux JL, Niwa H, Sekita Y, Huang X, Stark A, Kheradpour P, Kellis M, Flicek P, Chen Y, Webber C, Hardison R, Nelson J, Hallsworth-Pepin K, Delehaunty K, Markovic C, Minx P, Feng Y, Kremitzki C, Mitreva M, Glasscock J, Wylie T, Wohldmann P, Thiru P, Nhan MN, Pohl CS, Smith SM, Hou S, Nefedov M, de Jong PJ, Renfree MB, Mardis ER, Wilson RK (2008) Genome analysis of the platypus reveals unique signatures of evolution. Nature 453(7192):175–183. https://doi.org/10.1038/nature06936

Warren IA, Naville M, Chalopin D, Levin P, Berger CS, Galiana D, Volff J-N (2015) Evolutionary impact of transposable elements on genomic diversity and lineage-specific innovation in vertebrates. Chromosom Res 23(3):505–531. https://doi.org/10.1007/s10577-015-9493-5

Waterston RH, Pachter L (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420(6915):520–562. https://doi.org/10.1038/nature01262

Werren JH (2011) Selfish genetic elements, genetic conflict, and evolutionary innovation. P Natl Acad Sci USA 108(Supplement_2):10863–10870. https://doi.org/10.1073/pnas.1102343108

Wicker T, Sabot F, Hua-van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8(12):973–982. https://doi.org/10.1038/nrg2165

Zeh DW, Zeh JA, Ishida Y (2009) Transposable elements and an epigenetic basis for punctuated equilibria. BioEssays 31(7):715–726. https://doi.org/10.1002/bies.200900026

Zemojtel T, Penzkofer T, Schultz J, Dandekar T, Badge R, Vingron M (2007) Exonization of active mouse L1s: a driver of transcriptome evolution? BMC Genomics 8(1):392. https://doi.org/10.1186/1471-2164-8-392

Zeyl C, Mizesko M, Visser JAGM (2001) Mutational meltdown in laboratory yeast populations. Evolution 55(5):909–917.

Zhang Y, Romanish MT, Mager DL (2011) Distributions of transposable elements reveal hazardous zones in mammalian introns. PLoS Comput Biol 7(5):e1002046. https://doi.org/10.1371/journal.pcbi.1002046