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Evolutionary impact of transposable elements on genomic diversity and lineage-specific innovation in vertebrates

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Abstract

Since their discovery, a growing body of evidence has emerged demonstrating that transposable elements are important drivers of species diversity. These mobile elements exhibit a great variety in structure, size and mechanisms of transposition, making them important putative actors in organism evolution. The vertebrates represent a highly diverse and successful lineage that has adapted to a wide range of different environments. These animals also possess a rich repertoire of transposable elements, with highly diverse content between lineages and even between species. Here, we review how transposable elements are driving genomic diversity and lineage-specific innovation within vertebrates. We discuss the large differences in TE content between different vertebrate groups and then go on to look at how they affect organisms at a variety of levels: from the structure of chromosomes to their involvement in the regulation of gene expression, as well as in the formation and evolution of non-coding RNAs and protein-coding genes. In the process of doing this, we highlight how transposable elements have been involved in the evolution of some of the key innovations observed within the vertebrate lineage, driving the group’s diversity and success.

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Abbreviations

ChIP-Seq:

Chromatin immunoprecipitation sequencing

ERV:

Endogenous retrovirus

ESC:

Embryonic stem cell

HTT:

Horizontal transfer of TEs

LINE (or SINE):

Long (or short) interspersed nuclear element

lncRNA:

Long non-coding RNA

LTR:

Long terminal repeat

MYA:

Million years ago

Myr:

Million years

nt:

Nucleotides

TE:

Transposable element

References

  • Alzohairy AM, Gyulai G, Jansen RK, Bahieldin A (2013) Transposable elements domesticated and neofunctionalized by eukaryotic genomes. Plasmid 69:1–15

    Article  CAS  PubMed  Google Scholar 

  • Amaral PP, Dinger ME, Mattick JS (2013) Non-coding RNAs in homeostasis, disease and stress responses: an evolutionary perspective. Brief Funct Genomics 12:254–278

    Article  CAS  PubMed  Google Scholar 

  • Baack EJ, Rieseberg LH (2007) A genomic view of introgression and hybrid speciation. Curr Opin Genet Dev 17:513–518

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bae MI, Kim YJ, Lee JR, Jung YD, Kim HS (2013) A new exon derived from a mammalian apparent LTR retrotransposon of the SUPT16H gene. Int J Genomics 2013:387594

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Barker JN, Palmer CN, Zhao Y et al (2007) Null mutations in the filaggrin gene (FLG) determine major susceptibility to early-onset atopic dermatitis that persists into adulthood. J Invest Dermatol 127:564–567

    Article  CAS  PubMed  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  CAS  PubMed  Google Scholar 

  • Belancio VP, Roy-Engel AM, Deininger P (2008) The impact of multiple splice sites in human L1 elements. Gene 411:38–45

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bi S, Gavrilova O, Gong DW, Mason MM, Reitman M (1997) Identification of a placental enhancer for the human leptin gene. J Biol Chem 272:30583–30588

    Article  CAS  PubMed  Google Scholar 

  • Bièche I, Laurent A, Laurendeau I et al (2003) Placenta-specific INSL4 expression is mediated by a human endogenous retrovirus element. Biol Reprod 68:1422–1429

    Article  PubMed  CAS  Google Scholar 

  • Bingham PM, Kidwell MG, Rubin GM (1982) The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain-specific transposon family. Cell 29:995–1004

    Article  CAS  PubMed  Google Scholar 

  • Blaise S, de Parseval N, Bénit L, Heidmann T (2003) Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci U S A 100:13013–13018

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Blass E, Bell M, Boissinot S (2012) Accumulation and rapid decay of non-LTR retrotransposons in the genome of the three-spine stickleback. Genome Biol Evol 4:687–702

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Böhne A, Brunet F, Galiana-Arnoux D, Schultheis C, Volff JN (2008) Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res 16:203–215

    Article  PubMed  CAS  Google Scholar 

  • Borchert GM, Holton NW, Williams JD et al (2011) Comprehensive analysis of microRNA genomic loci identifies pervasive repetitive-element origins. Mob Genet Elem 1:8–17

    Article  Google Scholar 

  • Bourque G (2009) Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr Opin Genet Dev 19:607–612

    Article  CAS  PubMed  Google Scholar 

  • Bourque G, Leong B, Vega VB et al (2008) Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 18:1752–1762

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brandt J, Schrauth S, Veith AM et al (2005) Transposable elements as a source of genetic innovation: expression and evolution of a family of retrotransposon-derived neogenes in mammals. Gene 345:101–111

    Article  CAS  PubMed  Google Scholar 

  • Brawand D, Wagner CE, Li YI et al (2014) The genomic substrate for adaptive radiation in African cichlid fish. Nature 513:375–381

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Britten RJ, Davidson EH (1971) Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q Rev Biol 46:111–138

    Article  CAS  PubMed  Google Scholar 

  • Brow DA (2002) Allosteric cascade of spliceosome activation. Annu Rev Genet 36:333–360

    Article  CAS  PubMed  Google Scholar 

  • Campillos M, Doerks T, Shah PK, Bork P (2006) Computational characterization of multiple Gag-like human proteins. Trends Genet 22:585–589

    Article  CAS  PubMed  Google Scholar 

  • Cantrell MA, Scott L, Brown CJ, Martinez AR, Wichman HA (2008) Loss of LINE-1 activity in the megabats. Genetics 178:393–404

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cartault F, Munier P, Benko E et al (2012) Mutation in a primate-conserved retrotransposon reveals a noncoding RNA as a mediator of infantile encephalopathy. Proc Natl Acad Sci U S A 109:4980–4985

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Casola C, Hucks D, Feschotte C (2008) Convergent domestication of pogo-like transposases into centromere-binding proteins in fission yeast and mammals. Mol Biol Evol 25:29–41

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chalopin D, Galiana D, Volff JN (2012) Genetic innovation in vertebrates: gypsy integrase genes and other genes derived from transposable elements. Int J Evol Biol 2012:724519

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chalopin D, Naville M, Plard F, Galiana D, Volff JN (2015) Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates. Genome Biol Evol 7:567–580

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen Z, Cheng CH, Zhang J et al (2008) Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish. Proc Natl Acad Sci U S A 105:12944–12949

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen C, Ara T, Gautheret D (2009) Using Alu elements as polyadenylation sites: a case of retroposon exaptation. Mol Biol Evol 26:327–334

    Article  CAS  PubMed  Google Scholar 

  • Chinwalla AT, Cook LL, Delehaunty KD et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562

    Article  PubMed  CAS  Google Scholar 

  • Cho G, Bhat SS, Gao J et al (2008a) Evidence that SIZN1 is a candidate X-linked mental retardation gene. Am J Med Genet A 146A:2644–2650

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cho G, Lim Y, Zand D, Golden JA (2008b) Sizn1 is a novel protein that functions as a transcriptional coactivator of bone morphogenic protein signaling. Mol Cell Biol 28:1565–1572

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cho G, Lim Y, Golden JA (2011) XLMR candidate mouse gene, Zcchc12 (Sizn1) is a novel marker of Cajal-Retzius cells. Gene Expr Patterns 11:216–200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chuong EB, Rumi MAK, Soares MJ, Baker JC (2013) Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat Genet 45:325–329

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cordaux R, Udit S, Batzer MA, Feschotte C (2006) Birth of a chimeric primate gene by capture of the transposase gene from a mobile element. Proc Natl Acad Sci U S A 103:8101–8106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cornelis G, Heidmann O, Bernard-Stoecklin S et al (2012) Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. Proc Natl Acad Sci U S A 109:E432–E441

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cornelis G, Heidmann O, Degrelle SA et al (2013) Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants. Proc Natl Acad Sci U S A 110:E828–E837

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cornelis G, Vernochet C, Malicorne S et al (2014) Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs. Proc Natl Acad Sci 111:E4332–E4341

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cornelis G, Vernochet C, Carradec Q et al (2015) Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci U S A 112:E487–E496

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cotney J, Leng J, Yin J et al (2013) The evolution of lineage-specific regulatory activities in the human embryonic limb. Cell 154:185–196

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cowley M, Oakey RJ (2013) Transposable elements re-wire and fine-tune the transcriptome. PLoS Genet 9:e1003234

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Coyne JA, Orr HA (1998) The evolutionary genetics of speciation. Philos Trans R Soc Lond B Biol Sci 353:287–305

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cristofano AD, Strazzullo M, Longo L, Mantia GL (1995) Characterization and genomic mapping of the ZNF80 locus: expression of this zinc-finger gene is driven by a solitary LTR of ERV9 endogenous retrovrial family. Nucl Acids Res 23:2823–2830

    Article  PubMed Central  PubMed  Google Scholar 

  • Cui F, Sirotin MV, Zhurkin VB (2011) Impact of Alu repeats on the evolution of human p53 binding sites. Biol Direct 6:2

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cultrone A, Domínguez YR, Drevet C, Scazzocchio C, Fernández-Martín R (2007) The tightly regulated promoter of the xanA gene of Aspergillus nidulans is included in a helitron. Mol Microbiol 63:1577–1587

    Article  CAS  PubMed  Google Scholar 

  • de Boer JG, Yazawa R, Davidson WS, Koop BF (2007) Bursts and horizontal evolution of DNA transposons in the speciation of pseudotetraploid salmonids. BMC Genomics 8:422

    Article  PubMed Central  PubMed  Google Scholar 

  • de Souza FSJ, Franchini LF, Rubinstein M (2013) Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong? Mol Biol Evol 30:1239–1251

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Deininger P (2011a) Alu elements: know the SINEs. Genome Biol 12:236

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Deininger P (2011) Alu elements. Genomic disorders: the genomic basis of disease 12:236

  • Deininger PL, Batzer MA (1999) Alu repeats and human disease. Mol Genet Metab 67:183–193

    Article  CAS  PubMed  Google Scholar 

  • del Rosario RCH, Rayan NA, Prabhakar S (2014) Noncoding origins of anthropoid traits and a new null model of transposon functionalization. Genome Res 24:1469–1484

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Derrien T, Johnson R, Bussotti G et al (2012) The GENCODE v7 catalogue of human long non-coding RNAs: analysis of their structure, evolution and expression. Genome Res 22:1775–1789

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dion-Cote AM, Renaut S, Normandeau E, Bernatchez L (2014) RNA-seq reveals transcriptomic shock involving transposable elements reactivation in hybrids of young lake whitefish species. Mol Biol Evol 31:1188–1199

    Article  CAS  PubMed  Google Scholar 

  • Djebali S, Davis CA, Merkel A et al (2012) Landscape of transcription in human cells. Nature 489:101–108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dobigny G, Ozouf-Costaz C, Waters PD, Bonillo C, Coutanceau JP, Volobouev V (2004) LINE-1 amplification accompanies explosive genome repatterning in rodents. Chromosome Res 12:787–793

    Article  CAS  PubMed  Google Scholar 

  • Dotto BR, Carvalho EL, Silva AF et al (2015) HTT-DB: Horizontally transferred transposable elements database. Bioinformatics 31:2915–2917

    Article  PubMed  Google Scholar 

  • Dozmorov MG, Giles CB, Koelsch KA, Wren JD (2013) Systematic classification of non-coding RNAs by epigenomic similarity. BMC Bioinf 14:S2

    Article  Google Scholar 

  • Dupressoir A, Marceau G, Vernochet C et al (2005) Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc Natl Acad Sci U S A 102:725–730

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Edelstein LC, Collins T (2005) The SCAN domain family of zinc finger transcription factors. Gene 359:1–17

    Article  CAS  PubMed  Google Scholar 

  • Edwards CA, Mungall AJ, Matthews L et al (2008) The evolution of the DLK1-DIO3 imprinted domain in mammals. PLoS Biol 6:1292–1305

    CAS  Google Scholar 

  • Elisaphenko EA, Kolesnikov NN, Shevchenko AI et al (2008) A dual origin of the Xist gene from a protein-coding gene and a set of transposable elements. PLoS One 3:1–11

    Article  CAS  Google Scholar 

  • Emera D, Wagner GP (2012a) Transformation of a transposon into a derived prolactin promoter with function during human pregnancy. Proc Natl Acad Sci U S A 109:11246–11251

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Emera D, Wagner GP (2012b) Transposable element recruitments in the mammalian placenta: impacts and mechanisms. Brief Funct Genomics 11:267–276

    Article  CAS  PubMed  Google Scholar 

  • Emera D, Casola C, Lynch VJ, Wildman DE, Agnew D, Wagner GP (2012) Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol Biol Evol 29:239–247

    Article  CAS  PubMed  Google Scholar 

  • Emerson RO, Thomas JH (2009) Adaptive evolution in zinc finger transcription factors. PLoS Genet 5:e1000325

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Erickson IK, Cantrell MA, Scott L, Wichman HA (2011) Retrofitting the genome: L1 extinction follows endogenous retroviral expansion in a group of muroid rodents. J Virol 85:12315–12323

    Article  PubMed Central  PubMed  Google Scholar 

  • Feschotte C (2004) Merlin, a new superfamily of DNA transposons identified in diverse animal genomes and related to bacterial IS1016 insertion sequences. Mol Biol Evol 21:1769–1780

    Article  CAS  PubMed  Google Scholar 

  • Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397–405

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fort A, Hashimoto K, Yamada D et al (2014) Deep transcriptome profiling of mammalian stem cells supports a regulatory role for retrotransposons in pluripotency maintenance. Nat Genet 46:558–566

    Article  CAS  PubMed  Google Scholar 

  • Franchini LF, López-Leal R, Nasif S et al (2011) Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons. Proc Natl Acad Sci U S A 108:15270–15275

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Friedman RC, Farh KKH, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92–105

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fu B, Chen M, Zou M, Long M, He S (2010) The rapid generation of chimerical genes expanding protein diversity in zebrafish. BMC Genomics 11:657

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Furano AV, Duvernell DD, Boissinot S (2004) L1 (LINE-1) retrotransposon diversity differs dramatically between mammals and fish. Trends Genet 20:9–14

    Article  CAS  PubMed  Google Scholar 

  • Gentles AJ, Wakefield MJ, Kohany O et al (2007) Evolutionary dynamics of transposable elements in the short-tailed opossum Monodelphis domestica. Genome Res 17:992–1004

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gifford WD, Pfaff SL, Macfarlan TS (2013) Transposable elements as genetic regulatory substrates in early development. Trends Cell Biol 23:218–226

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gilbert C, Schaack S, Pace JK 2nd, Brindley PJ, Feschotte C (2010) A role for host-parasite interactions in the horizontal transfer of transposons across phyla. Nature 464:1347–1350

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gilbert C, Hernandez SS, Flores-Benabib J, Smith EN, Feschotte C (2012) Rampant horizontal transfer of SPIN transposons in squamate reptiles. Mol Biol Evol 29:503–515

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gim JA, Ha HS, Ahn K, Kim DS, Kim HS (2014) Genome-wide identification and classification of microRNAs derived from repetitive elements. Genomics Inform 12:261–267

    Article  PubMed Central  PubMed  Google Scholar 

  • Glinsky GV (2015) Transposable elements and DNA methylation create in embryonic stem cells human-specific regulatory sequences associated with distal enhancers and noncoding RNAs. Genome Biol Evol 7:1432–1454

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gombart AF, Saito T, Koeffler HP (2009) Exaptation of an ancient Alu short interspersed element provides a highly conserved vitamin D-mediated innate immune response in humans and primates. BMC Genomics 10:321

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Grahn RA, Rinehart TA, Cantrell MA, Wichman HA (2005) Extinction of LINE-1 activity coincident with a major mammalian radiation in rodents. Cytogenet Genome Res 110:407–415

    Article  CAS  PubMed  Google Scholar 

  • Ha M, Kim VN (2014) Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15:509–524

    Article  CAS  PubMed  Google Scholar 

  • Haas NB, Grabowski JM, Sivitz AB, Burch JBE (1997) Chicken repeat 1 (CR1) elements, which define an ancient family of vertebrate non-LTR retrotransposons, contain two closely spaced open reading frames. Gene 197:305–309

    Article  CAS  PubMed  Google Scholar 

  • Hambor JE, Mennone J, Coon ME, Hanke JH, Kavathas P (1993) Identification and characterization of an Alu-containing, T-cell-specific enhancer located in the last intron of the human CD8 alpha gene. Mol Cell Biol 13:7056–7070

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Han MJ, Shen YH, Xu MS, Liang HY, Zhang HH, Zhang Z (2013) Identification and evolution of the silkworm helitrons and their contribution to transcripts. DNA Res 20:471–484

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harris CR, Dewan A, Zupnick A et al (2009) p53 responsive elements in human retrotransposons. Oncogene 28:3857–3865

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hayakawa T, Satta Y, Gagneux P, Varki A, Takahata N (2001) Alu-mediated inactivation of the human CMP- N-acetylneuraminic acid hydroxylase gene. Proc Natl Acad Sci U S A 98:11399–11404

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hayward A, Cornwallis CK, Jern P (2015) Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. Proc Natl Acad Sci U S A 112:464–469

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • He S, Gu W, Li Y, Zhu H (2013) ANRIL/CDKN2B-AS shows two-stage clade-specific evolution and becomes conserved after transposon insertions in simians. BMC Evol Biol 13:247

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Heidmann O, Vernochet C, Dupressoir A, Heidmann T (2009) Identification of an endogenous retroviral envelope gene with fusogenic activity and placenta-specific expression in the rabbit: a new “syncytin” in a third order of mammals. Retrovirology 6:107

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hellsten U, Harland RM, Gilchrist MJ et al (2010) The genome of the Western clawed frog Xenopus tropicalis. Science 328:633–636

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Henke C, Strissel PL, Schubert MT et al (2015) Selective expression of sense and antisense transcripts of the sushi-ichi-related retrotransposon—derived family during mouse placentogenesis. Retrovirology 12:9

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Henrichsen CN, Vinckenbosch N, Zöllner S et al (2009) Segmental copy number variation shapes tissue transcriptomes. Nat Genet 41:424–429

    Article  CAS  PubMed  Google Scholar 

  • Herpin A, Braasch I, Kraeussling M et al (2010) Transcriptional rewiring of the sex determining dmrt1 gene duplicate by transposable elements. PLoS Genet 6:e1000844

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hezroni H, Koppstein D, Schwartz MG, Avrutin A, Bartel DP, Ulitsky I (2015) Principles of long noncoding RNA evolution derived from direct comparison of transcriptomes in 17 species. Cell Rep 11:1110–1122

    Article  CAS  PubMed  Google Scholar 

  • Hikosaka A, Kobayashi T, Saito Y, Kawahara A (2007) Evolution of the Xenopus piggyBac transposon family TxpB: domesticated and untamed strategies of transposon subfamilies. Mol Biol Evol 24:2648–2656

    Article  CAS  PubMed  Google Scholar 

  • Hillier L, Miller W, Birney E et al (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716

    Article  CAS  Google Scholar 

  • Holdt LM, Hoffmann S, Sass K et al (2013) Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLoS Genet 9:1–12

    Article  CAS  Google Scholar 

  • Hollister JD, Gaut BS (2007) Population and evolutionary dynamics of helitron transposable elements in Arabidopsis thaliana. Mol Biol Evol 24:2515–2524

    Article  CAS  PubMed  Google Scholar 

  • Howe K, Clark MD, Torroja CF et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hughes JF, Coffin JM (2001) Evidence for genomic rearrangements mediated by human endogenous retroviruses during primate evolution. Nat Genet 29:487–489

    Article  CAS  PubMed  Google Scholar 

  • Hughes JF, Coffin JM (2005) Human endogenous retroviral elements as indicators of ectopic recombination events in the primate genome. Genetics 171:1183–1194

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iida A, Takamatsu N, Hori H et al (2005) Reversion mutation of ib oculocutaneous albinism to wild-type pigmentation in medaka fish. Pigment Cell Res 18:382–384

    Article  CAS  PubMed  Google Scholar 

  • Ivancevic AM, Walsh AM, Kortschak RD, Adelson DL (2013) Jumping the fine LINE between species: horizontal transfer of transposable elements in animals catalyses genome evolution. BioEssays 35:1071–1082

    Article  CAS  PubMed  Google Scholar 

  • Jacques PÉ, Jeyakani J, Bourque G (2013) The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet 9:e1003504

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Johnson R, Guigó R (2014) The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs. RNA 20:959–976

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaessmann H (2010) Origins, evolution, and phenotypic impact of new genes. Genome Res 20:1313–1326

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaneko-Ishino T, Ishino F (2012) The role of genes domesticated from LTR retrotransposons and retroviruses in mammals. Front Microbiol 3:1–10

    Article  CAS  Google Scholar 

  • Kannan S, Chernikova D, Rogozin IB et al (2015) Transposable element insertions in long intergenic non-coding RNA genes. Front Bioeng Biotechnol 3:1–9

    Article  Google Scholar 

  • Kapitonov VV, Jurka J (2001) Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci U S A 98:8714–8719

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kapitonov VV, Jurka J (2004) Harbinger transposons and an ancient HARBI1 gene derived from a transposase. DNA Cell Biol 23:311–324

    Article  CAS  PubMed  Google Scholar 

  • Kapitonov VV, Jurka J (2006) Self-synthesizing DNA transposons in eukaryotes. Proc Natl Acad Sci U S A 103:4540–4545

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kapitonov VV, Koonin EV (2015) Evolution of the RAG1-RAG2 locus: both proteins came from the same transposon. Biol Direct 10:1–8

    Article  CAS  Google Scholar 

  • Kapusta A, Feschotte C (2014) Volatile evolution of long noncoding RNA repertoires: mechanisms and biological implications. Trends Genet 30:439–452

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kapusta A, Kronenberg Z, Lynch VJ et al (2013) Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet 9:e1003470

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kazazian HH Jr (2004) Mobile elements: drivers of genome evolution. Science 303:1626–1632

    Article  CAS  PubMed  Google Scholar 

  • Kelley D, Rinn J (2012) Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol 13:R107

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Koga A, Iida A, Hori H, Shimada A, Shima A (2006) Vertebrate DNA transposon as a natural mutator: the medaka fish Tol2 element contributes to genetic variation without recognizable traces. Mol Biol Evol 23:1414–1419

    Article  CAS  PubMed  Google Scholar 

  • Kokošar J, Kordiš D (2013) Genesis and regulatory wiring of retroelement-derived domesticated genes: a phylogenomic perspective. Mol Biol Evol 30:1015–1031

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kordiš D, Gubensek F (1998) The Bov-B lines found in Vipera ammodytes toxic PLA2 genes are widespread in snake genomes. Toxicon 36:1585–1590

    Article  PubMed  Google Scholar 

  • Kordiš D, Gubensek F (1999) Molecular evolution of Bov-B LINEs in vertebrates. Gene 238:171–178

    Article  PubMed  Google Scholar 

  • Kraaijeveld K (2010) Genome size and species diversification. Evol Biol 37:227–233

    Article  PubMed Central  PubMed  Google Scholar 

  • Krull M, Brosius J, Schmitz J (2005) Alu-SINE exonization: en route to protein-coding function. Mol Biol Evol 22:1702–1711

    Article  CAS  PubMed  Google Scholar 

  • Krull M, Petrusma M, Makalowski W, Brosius J, Schmitz J (2007) Functional persistence of exonized mammalian-wide interspersed repeat elements (MIRs). Genome Res 17:1139–1145

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kunarso G, Chia NY, Jeyakani J et al (2010) Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 42:631–634

    Article  CAS  PubMed  Google Scholar 

  • Kutter C, Watt S, Stefflova K et al (2012) Rapid turnover of long noncoding RNAs and the evolution of gene expression. PLoS Genet 8:e1002841

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Landry JR, Mager DL (2003) Functional analysis of the endogenous retroviral promoter of the human endothelin B receptor gene. J Virol 77:7459–7466

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Landry JR, Rouhi A, Medstrand P, Mager DL (2002) The Opitz syndrome gene mid1 is transcribed from a human endogenous retroviral promoter. Mol Biol Evol 19:1934–1942

    Article  CAS  PubMed  Google Scholar 

  • Le Rouzic A, Capy P (2006) Population genetics models of competition between transposable element subfamilies. Genetics 174:785–793

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lee RC (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Oshige M, Durant ST et al (2005) The SET domain protein Metnase mediates foreign DNA integration and links integration to nonhomologous end-joining repair. Proc Natl Acad Sci U S A 102:18075–18080

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee JY, Ji Z, Tian B (2008) Phylogenetic analysis of mRNA polyadenylation sites reveals a role of transposable elements in evolution of the 3′-end of genes. Nucl Acids Res 36:5581–5590

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lev-Maor G, Sorek R, Shomron N, Ast G (2003) The birth of an alternatively spliced exon: 3ʹ splice-site selection in Alu exons. Science 300:1288–1291

    Article  CAS  PubMed  Google Scholar 

  • Li L, Keverne EB, Aparicio SA, Ishino F, Barton SC, Surani MA (1999) Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 284:330–333

    Article  CAS  PubMed  Google Scholar 

  • Lin L, Jiang P, Shen S, Sato S, Davidson BL, Xing Y (2009) Large-scale analysis of exonized mammalian-wide interspersed repeats in primate genomes. Hum Mol Genet 18:2204–2214

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu D, Bischerour J, Siddique A, Buisine N, Bigot Y, Chalmers R (2007) The human SETMAR protein preserves most of the activities of the ancestral Hsmar1 transposase. Mol Cell Biol 27:1125–1132

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Loewer S, Cabili MN, Guttman M et al (2010) Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 42:1113–1117

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Londin E, Loher P, Telonis AG et al (2015) Analysis of 13 cell types reveals evidence for the expression of numerous novel primate- and tissue-specific microRNAs. Proc Natl Acad Sci U S A 112:E1106–E1115

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lukic S, Chen K (2011) Human piRNAs are under selection in Africans and repress transposable elements. Mol Biol Evol 28:3061–3067

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 43:1154–1159

    Article  CAS  PubMed  Google Scholar 

  • Lynch VJ, Nnamani MC, Kapusta A et al (2015) Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep 10:551–561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Managadze D, Lobkovsky AE, Wolf YI, Shabalina SA, Rogozin IB, Koonin EV (2013) The vast, conserved mammalian lincRNome. PLoS Comput Biol 9:e1002917

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marques AC, Dupanloup I, Vinckenbosch N, Reymond A, Kaessmann H (2005) Emergence of young human genes after a burst of retroposition in primates. PLoS Biol 3:1970–1979

    Article  CAS  Google Scholar 

  • Marques AC, Vinckenbosch N, Brawand D, Kaessmann H (2008) Functional diversification of duplicate genes through subcellular adaptation of encoded proteins. Genome Biol 9:R54

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mason CE, Shu FJ, Wang C et al (2010) Location analysis for the estrogen receptor-α reveals binding to diverse ERE sequences and widespread binding within repetitive DNA elements. Nucl Acids Res 38:2355–2368

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Matsui T, Kinoshita-Ida Y, Hayashi-Kisumi F et al (2006) Mouse homologue of skin-specific retroviral-like aspartic protease involved in wrinkle formation. J Biol Chem 281:27512–27525

    Article  CAS  PubMed  Google Scholar 

  • Matsui T, Miyamoto K, Kubo A et al (2011) SASPase regulates stratum corneum hydration through profilaggrin-to-filaggrin processing. EMBO Mol Med 3:320–333

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McClintock B (1956) Controlling elements and the gene. Cold Spring Harb Symp Quant Biol 21:197–216

    Article  CAS  PubMed  Google Scholar 

  • Metcalfe CJ, Bulazel KV, Ferreri GC et al (2007) Genomic instability within centromeres of interspecific marsupial hybrids. Genetics 177:2507–2517

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Metcalfe CJ, Filee J, Germon I, Joss J, Casane D (2012) Evolution of the Australian lungfish (Neoceratodus forsteri) genome: a major role for CR1 and L2 LINE elements. Mol Biol Evol 29:3529–3539

    Article  CAS  PubMed  Google Scholar 

  • Meunier J, Lemoine F, Soumillon M et al (2013) Birth and expression evolution of mammalian microRNA genes. Genome Res 23:34–45

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mi S, Lee X, Li X et al (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–789

    Article  CAS  PubMed  Google Scholar 

  • Micale L, Loviglio MN, Manzoni M et al (2012) A fish-specific transposable element shapes the repertoire of p53 target genes in zebrafish. PLoS One 7:e46642

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Minghetti PP, Dugaiczyk A (1993) The emergence of new DNA repeats and the divergence of primates. Proc Natl Acad Sci U S A 90:1872–1876

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mortazavi A, Leeper Thompson EC, Garcia ST, Myers RM, Wold B (2006) Comparative genomics modeling of the NRSF/REST repressor network: from single conserved sites to genome-wide repertoire. Genome Res 16:1208–1221

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nakanishi A, Kobayashi N, Suzuki-Hirano A et al (2012) A SINE-derived element constitutes a unique modular enhancer for mammalian diencephalic Fgf8. PLoS One 7:e43785

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Necsulea A, Soumillon M, Warnefors M et al (2014) The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505:635–640

    Article  CAS  PubMed  Google Scholar 

  • Notwell JH, Chung T, Heavner W, Bejerano G (2015) A family of transposable elements co-opted into developmental enhancers in the mouse neocortex. Nat Commun 6:6644

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 27:2606–2617

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • O’Neill RJ, O’Neill MJ, Graves JA (1998) Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393:68–72

    Article  PubMed  Google Scholar 

  • Ono R, Nakamura K, Inoue K et al (2006) Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat Genet 38:101–106

    Article  CAS  PubMed  Google Scholar 

  • Pan D, Zhang L (2009) Burst of young retrogenes and independent retrogene formation in mammals. PLoS One 4:e5040

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pang ALY, Peacock S, Johnson W, Bear DH, Rennert OM, Chan WY (2009) Cloning, characterization, and expression analysis of the novel acetyltransferase retrogene Ard1b in the mouse. Biol Reprod 81:302–309

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Perry GH, Dominy NJ, Claw KG et al (2007) Diet and the evolution of human amylase gene copy number variation. Nat Genet 39:1256–1260

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pi W, Yang Z, Wang J et al (2004) The LTR enhancer of ERV-9 human endogenous retrovirus is active in oocytes and progenitor cells in transgenic zebrafish and humans. Proc Natl Acad Sci U S A 101:805–810

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Piriyapongsa J, Jordan IK (2007) A family of human microRNA genes from miniature inverted-repeat transposable elements. PLoS One 2:e203

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Piriyapongsa J, Mariño-Ramírez L, Jordan IK (2007a) Origin and evolution of human microRNAs from transposable elements. Genetics 176:1323–1337

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Piriyapongsa J, Polavarapu N, Borodovsky M, McDonald J (2007b) Exonization of the LTR transposable elements in human genome. BMC Genomics 8:291

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Piskurek O, Jackson DJ (2011) Tracking the ancestry of a deeply conserved eumetazoan SINE domain. Mol Biol Evol 28:2727–2730

    Article  CAS  PubMed  Google Scholar 

  • Plath N, Ohana O, Dammermann B et al (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52:437–444

    Article  CAS  PubMed  Google Scholar 

  • Potrzebowski L, Vinckenbosch N, Marques AC, Chalmel F, Jégou B, Kaessmann H (2008) Chromosomal gene movements reflect the recent origin and biology of therian sex chromosomes. PLoS Biol 6:709–716

    Article  CAS  Google Scholar 

  • Potrzebowski L, Vinckenbosch N, Kaessmann H (2010) The emergence of new genes on the young therian X. Trends Genet 26:1–4

    Article  CAS  PubMed  Google Scholar 

  • Qin S, Jin P, Zhou X, Chen L, Ma F (2015) The role of transposable elements in the origin and evolution of microRNAs in human. Plos One 10:e0131365

    Article  PubMed Central  PubMed  Google Scholar 

  • Ray DA, Feschotte C, Pagan HJT et al (2008) Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus. Genome Res 18:717–728

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rebollo R, Romanish MT, Mager DL (2012) Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet 46:21–42

    Article  CAS  PubMed  Google Scholar 

  • Román AC, González-Rico FJ, Moltó E et al (2011) Dioxin receptor and SLUG transcription factors regulate the insulator activity of B1 SINE retrotransposons via an RNA polymerase switch. Genome Res 21:422–432

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ruiz-Orera J, Messeguer X, Subirana JA, Alba MM (2014) Long non-coding RNAs as a source of new peptides. Elife e03523

  • Samuelson LC, Wiebauer K, Snow CM, Meisler MH (1990) Retroviral and pseudogene insertion sites reveal the lineage of human salivary and pancreatic amylase genes from a single gene during primate evolution. Mol Cell Biol 10:2513–2520

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Santangelo AM, de Souza FSJ, Franchini LF, Bumaschny VF, Low MJ, Rubinstein M (2007) Ancient exaptation of a CORE-SINE retroposon into a highly conserved mammalian neuronal enhancer of the proopiomelanocortin gene. PLoS Genet 3:1813–1826

    Article  CAS  PubMed  Google Scholar 

  • Santoni FA, Guerra J, Luban J (2012) HERV-H RNA is abundant in human embryonic stem cells and a precise marker for pluripotency. Retrovirology 9:111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Santos ME, Braasch I, Boileau N et al (2014) The evolution of cichlid fish egg-spots is linked with a cis-regulatory change. Nat Commun 5:5149

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sasaki T, Nishihara H, Hirakawa M et al (2008) Possible involvement of SINEs in mammalian-specific brain formation. Proc Natl Acad Sci U S A 105:4220–4225

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saunders MA, Liang H, Li WH (2007) Human polymorphism at microRNAs and microRNA target sites. Proc Natl Acad Sci U S A 104:3300–3305

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schaack S, Gilbert C, Feschotte C (2010) Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol 25:537–546

    Article  PubMed Central  PubMed  Google Scholar 

  • Schartl M, Hornung U, Gutbrod H, Volff JN, Wittbrodt J (1999) Melanoma loss-of-function mutants in Xiphophorus caused by Xmrk-oncogene deletion and gene disruption by a transposable element. Genetics 153:1385–1394

    PubMed Central  CAS  PubMed  Google Scholar 

  • Schatz DG, Swanson PC (2011) V(D)J recombination: mechanisms of initiation. Annu Rev Genet 45:167–202

    Article  CAS  PubMed  Google Scholar 

  • Schmidt D, Schwalie PC, Wilson MD et al (2012) Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148:335–348

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schmitz J, Brosius J (2011) Exonization of transposed elements: a challenge and opportunity for evolution. Biochimie 93:1928–1934

    Article  CAS  PubMed  Google Scholar 

  • Schüller M, Jenne D, Voltz R (2005) The human PNMA family: novel neuronal proteins implicated in paraneoplastic neurological disease. J Neuroimmunol 169:172–176

    Article  PubMed  CAS  Google Scholar 

  • Schulte AM, Wellstein A (1998) Structure and phylogenetic analysis of an endogenous retrovirus inserted into the human growth factor gene pleiotrophin. J Virol 72:6065–6072

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sekita Y, Wagatsuma H, Nakamura K et al (2008) Role of retrotransposon-derived imprinted gene, Rtl1, in the feto-maternal interface of mouse placenta. Nat Genet 40:243–248

    Article  CAS  PubMed  Google Scholar 

  • Sela N, Mersch B, Gal-Mark N, Lev-Maor G, Hotz-Wagenblatt A, Ast G (2007) Comparative analysis of transposed element insertion within human and mouse genomes reveals Alu’s unique role in shaping the human transcriptome. Genome Biol 8:R127

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sela N, Mersch B, Hotz-Wagenblatt A, Ast G (2010) Characteristics of transposable element exonization within human and mouse. PLoS One 5:e10907

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Shen S, Lin L, Cai JJ et al (2011) Widespread establishment and regulatory impact of Alu exons in human genes. Proc Natl Acad Sci U S A 108:2837–2842

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Singer SS, Männel DN, Hehlgans T, Brosius J, Schmitz J (2004) From “junk” to gene: curriculum vitae of a primate receptor isoform gene. J Mol Biol 341:883–886

    Article  CAS  PubMed  Google Scholar 

  • Sinzelle L, Izsvák Z, Ivics Z (2009) Molecular domestication of transposable elements: from detrimental parasites to useful host genes. Cell Mol Life Sci 66:1073–1093

    Article  CAS  PubMed  Google Scholar 

  • Smalheiser NR, Torvik VI (2005) Mammalian microRNAs derived from genomic repeats. Trends Genet 21:322–326

    Article  CAS  PubMed  Google Scholar 

  • Spengler RM, Oakley CK, Davidson BL (2014) Functional microRNAs and target sites are created by lineage-specific transposition. Hum Mol Genet 23:1783–1793

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • St. Laurent G, Wahlestedt C, Kapranov P (2015) The landscape of long noncoding RNA classification. Trends Genet 31:239–251

    Article  CAS  PubMed  Google Scholar 

  • Steinemann S, Steinemann M (2005) Y chromosomes: born to be destroyed. BioEssays 27:1076–1083

    Article  CAS  PubMed  Google Scholar 

  • Sun C, Shepard DB, Chong RA et al (2012) LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders. Genome Biol Evol 4:168–183

    Article  PubMed Central  PubMed  Google Scholar 

  • Sundaram V, Cheng Y, Ma Z et al (2014) Widespread contribution of transposable elements to the innovation of gene regulatory networks. Genome Res 24:1963–1976

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tang Z, Zhang HH, Huang K, Zhang XG, Han MJ, Zhang Z (2015) Repeated horizontal transfers of four DNA transposons in invertebrates and bats. Mob DNA 6:3

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tashiro K, Teissier A, Kobayashi N et al (2011) A mammalian conserved element derived from SINE displays enhancer properties recapitulating satb2 expression in early-born callosal projection neurons. PLoS One 6:e28497

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thomas J, Schaack S, Pritham EJ (2010) Pervasive horizontal transfer of rolling-circle transposons among animals. Genome Biol Evol 2:656–664

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Thomas J, Phillips CD, Baker RJ, Pritham EJ (2014) Rolling-circle transposons catalyze genomic innovation in a mammalian lineage. Genome Biol Evol 6:2595–2610

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thomson SJP, Goh FG, Banks H et al (2009) The role of transposable elements in the regulation of IFN-λ1 gene expression. Proc Natl Acad Sci U S A 106:11564–11569

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ting CN, Rosenberg MP, Snow CM, Samuelson LC, Meisler MH (1992) Endogenous retroviral sequences are required for tissue-specific expression of a human salivary amylase gene. Genes Dev 6:1457–1465

    Article  CAS  PubMed  Google Scholar 

  • Tipney HJ, Hinsley TA, Brass A, Metcalfe K, Donnai D, Tassabehji M (2004) Isolation and characterisation of GTF2IRD2, a novel fusion gene and member of the TFII-I family of transcription factors, deleted in Williams-Beuren syndrome. Eur J Hum Genet 12:551–560

    Article  CAS  PubMed  Google Scholar 

  • Tomascik-Cheeseman L, Marchetti F, Lowe X et al (2002) CENP-B is not critical for meiotic chromosome segregation in male mice. Mutat Res 513:197–203

    Article  CAS  PubMed  Google Scholar 

  • Ullu E, Tschudi C (1984) Alu sequences are processed 7SL RNA genes. Nature 312:171–172

    Article  CAS  PubMed  Google Scholar 

  • Vance KW, Ponting CP (2014) Transcriptional regulatory functions of nuclear long noncoding RNAs. Trends Genet 30:348–355

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Varki A (2001) Loss of N-glycolylneuraminic acid in humans: mechanisms, consequences, and implications for hominid evolution. Am J Phys Anthropol Suppl 33:54–69

    Article  Google Scholar 

  • Varki A (2010) Colloquium paper: uniquely human evolution of sialic acid genetics and biology. Proc Natl Acad Sci U S A 107(Suppl):8939–8946

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Verneau O, Catzeflis F, Furano AV (1998) Determining and dating recent rodent speciation events by using L1 (LINE-1) retrotransposons. Proc Natl Acad Sci U S A 95:11284–11289

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vernochet C, Redelsperger F, Harper F et al (2014) The captured retroviral envelope syncytin-A and syncytin-B genes are conserved in the Spalacidae together with hemotrichorial placentation. Biol Reprod 91:148–148

    Article  PubMed  CAS  Google Scholar 

  • Villar D, Berthelot C, Aldridge S et al (2015) Enhancer evolution across 20 mammalian species. Cell 160:554–566

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vinckenbosch N, Dupanloup I, Kaessmann H (2006) Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci U S A 103:3220–3225

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Volff JN (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. BioEssays 28:913–922

    Article  CAS  PubMed  Google Scholar 

  • Volff JN, Bouneau L, Ozouf-Costaz C, Fischer C (2003) Diversity of retrotransposable elements in compact pufferfish genomes. Trends Genet 19:674–678

    Article  CAS  PubMed  Google Scholar 

  • Volff JN, Nanda I, Schmid M, Schartl M (2007) Governing sex determination in fish: regulatory putsches and ephemeral dictators. Sex Dev 1:85–99

    Article  PubMed  Google Scholar 

  • Wallau GL, Ortiz MF, Loreto EL (2012) Horizontal transposon transfer in eukarya: detection, bias, and perspectives. Genome Biol Evol 4:689–699

    Article  PubMed  CAS  Google Scholar 

  • Wang T, Zeng J, Lowe CB et al (2007) Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc Natl Acad Sci U S A 104:18613–18618

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang J, Xie G, Singh M et al (2014) Primate-specific endogenous retrovirus-driven transcription defines naive-like stem cells. Nature 516:405–409

    Article  CAS  PubMed  Google Scholar 

  • Washietl S, Kellis M, Garber M (2014) Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals. Genome Res 24:616–628

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Watson CT, Lubieniecki KP, Loew E, Davidson WS, Breden F (2010) Genomic organization of duplicated short wave-sensitive and long wave-sensitive opsin genes in the green swordtail, Xiphophorus helleri. BMC Evol Biol 10:87

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wicker T, Robertson JS, Schulze SR et al (2005) The repetitive landscape of the chicken genome. Genome Res 15:126–136

    Article  PubMed Central  PubMed  Google Scholar 

  • Wu LT, Hui JHL, Chu KH (2013) Origin and evolution of yolk proteins: expansion and functional diversification of large lipid transfer protein superfamily. Biol Reprod 88:102

    Article  PubMed  CAS  Google Scholar 

  • Xing J, Wang H, Belancio VP, Cordaux R, Deininger PL, Batzer MA (2006) Emergence of primate genes by retrotransposon-mediated sequence transduction. Proc Natl Acad Sci U S A 103:17608–17613

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yuan Z, Sun X, Jiang D et al (2010) Origin and evolution of a placental-specific microRNA family in the human genome. BMC Evol Biol 10:346

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang H, Liu Y, Su D et al (2011) A single nucleotide polymorphism in a miR-1302 binding site in CGA increases the risk of idiopathic male infertility. Fertil Steril 96:34–39

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Edwards A, Fan W, Fang Z, Deininger P, Zhang K (2013) Inferring the expression variability of human transposable element-derived exons by linear model analysis of deep RNA sequencing data. BMC Genomics 14:584

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Ian Warren, Magali Naville and Domitille Chalopin contributed equally to this work.

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Warren, I.A., Naville, M., Chalopin, D. et al. Evolutionary impact of transposable elements on genomic diversity and lineage-specific innovation in vertebrates. Chromosome Res 23, 505–531 (2015). https://doi.org/10.1007/s10577-015-9493-5

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