Transposable elements and viruses as factors in adaptation and evolution: an expansion and strengthening of the TE-Thrust hypothesis

In addition to the strong divergent evolution and significant and episodic evolutionary transitions and speciation we previously attributed to TE-Thrust, we have expanded the hypothesis to more fully account for the contribution of viruses to TE-Thrust and evolution. The concept of symbiosis and holobiontic genomes is acknowledged, with particular emphasis placed on the creativity potential of the union of retroviral genomes with vertebrate genomes. Further expansions of the TE-Thrust hypothesis are proposed regarding a fuller account of horizontal transfer of TEs, the life cycle of TEs, and also, in the case of a mammalian innovation, the contributions of retroviruses to the functions of the placenta. The possibility of drift by TE families within isolated demes or disjunct populations, is acknowledged, and in addition, we suggest the possibility of horizontal transposon transfer into such subpopulations. “Adaptive potential” and “evolutionary potential” are proposed as the extremes of a continuum of “intra-genomic potential” due to TE-Thrust. Specific data is given, indicating “adaptive potential” being realized with regard to insecticide resistance, and other insect adaptations. In this regard, there is agreement between TE-Thrust and the concept of adaptation by a change in allele frequencies. Evidence on the realization of “evolutionary potential” is also presented, which is compatible with the known differential survivals, and radiations of lineages. Collectively, these data further suggest the possibility, or likelihood, of punctuated episodes of speciation events and evolutionary transitions, coinciding with, and heavily underpinned by, intermittent bursts of TE activity.

[1]  D. Finnegan,et al.  Eukaryotic transposable elements and genome evolution. , 1989, Trends in genetics : TIG.

[2]  L. Villarreal,et al.  On viruses, sex, and motherhood , 1997, Journal of virology.

[3]  M. Nei The new mutation theory of phenotypic evolution , 2007, Proceedings of the National Academy of Sciences.

[4]  I. Sora,et al.  Intracisternal A-particle element in the 3′ noncoding region of the mu-opioid receptor gene in CXBK mice: a new genetic mechanism underlying differences in opioid sensitivity , 2006, Pharmacogenetics and genomics.

[5]  M. Wilkinson,et al.  A processed homeobox gene expressed in a stage-, tissue- and region-specific manner in epididymis. , 1997, Gene.

[6]  Masatoshi Nei,et al.  Selectionism and neutralism in molecular evolution. , 2005, Molecular biology and evolution.

[7]  G. Parris A hypothetical Master Development Program for multi-cellular organisms: Ontogeny and phylogeny , 2009 .

[8]  F. Hoffmann,et al.  Whole-genome duplications spurred the functional diversification of the globin gene superfamily in vertebrates. , 2012, Molecular biology and evolution.

[9]  Cédric Feschotte,et al.  Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. , 2010, Trends in ecology & evolution.

[10]  G. Khoury,et al.  Transcriptional "silencer" element in rat repetitive sequences associated with the rat insulin 1 gene locus. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[11]  H. Kazazian,et al.  High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes. , 2010, Genome research.

[12]  Guenther Witzany,et al.  Viruses are essential agents within the roots and stem of the tree of life. , 2010, Journal of theoretical biology.

[13]  D. Petrov,et al.  A recent adaptive transposable element insertion near highly conserved developmental loci in Drosophila melanogaster. , 2009, Molecular biology and evolution.

[14]  T. Flannery The Future Eaters , 1994 .

[15]  Keith R. Oliver,et al.  The Genomic Drive hypothesis and punctuated evolutionary taxonations, or radiations , 2009 .

[16]  Christian Biémont,et al.  Genetics: Junk DNA as an evolutionary force , 2006, Nature.

[17]  Keith R. Oliver,et al.  Transposable elements: powerful facilitators of evolution , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[18]  Miriam K. Konkel,et al.  Genome analysis of the platypus reveals unique signatures of evolution , 2008, Nature.

[19]  S. Boissinot,et al.  Different Rates of LINE-1 (L1) Retrotransposon Amplification and Evolution in New World Monkeys , 2003, Journal of Molecular Evolution.

[20]  L. Peshkin,et al.  Genome sequencing reveals insights into physiology and longevity of the naked mole rat , 2011, Nature.

[21]  T. Mackay,et al.  Accumulation of transposable elements in the genome of Drosophila melanogaster is associated with a decrease in fitness. , 2004, The Journal of heredity.

[22]  D. Nouaud,et al.  Molecular domestication – more than a sporadic episode in evolution , 2004, Genetica.

[23]  A. Reymond,et al.  Emergence of Young Human Genes after a Burst of Retroposition in Primates , 2005, PLoS biology.

[24]  Active role of small non-coding RNAs derived from SINE/B1 retrotransposon during early mouse development , 2012, Molecular Biology Reports.

[25]  P. Capy,et al.  The First Steps of Transposable Elements Invasion , 2005, Genetics.

[26]  Alex Andrianopoulos,et al.  Cis-Regulatory Elements in the Accord Retrotransposon Result in Tissue-Specific Expression of the Drosophila melanogaster Insecticide Resistance Gene Cyp6g1 , 2007, Genetics.

[27]  Z. Izsvák,et al.  A novel active endogenous retrovirus family contributes to genome variability in rat inbred strains. , 2010, Genome research.

[28]  P. Opolon,et al.  Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene , 2009, Proceedings of the National Academy of Sciences.

[29]  S. O’Brien,et al.  A Molecular Phylogeny for Bats Illuminates Biogeography and the Fossil Record , 2005, Science.

[30]  H. Kazazian,et al.  Retrotransposons Revisited: The Restraint and Rehabilitation of Parasites , 2008, Cell.

[31]  S. Gould,et al.  Punctuated equilibria: an alternative to phyletic gradualism , 1972 .

[32]  T. Heidmann,et al.  Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[33]  M. Pagel,et al.  Large Punctuational Contribution of Speciation to Evolutionary Divergence at the Molecular Level , 2006, Science.

[34]  G. Georgiev Mobile genetic elements in animal cells and their biological significance. , 1984, European journal of biochemistry.

[35]  J. Jurka Evolutionary impact of human Alu repetitive elements. , 2004, Current opinion in genetics & development.

[36]  M. Batzer,et al.  Alu repeats and human disease. , 1999, Molecular genetics and metabolism.

[37]  Yoshiyuki Sakaki,et al.  Whole-genome screening indicates a possible burst of formation of processed pseudogenes and Alu repeats by particular L1 subfamilies in ancestral primates , 2003, Genome Biology.

[38]  C. Amemiya,et al.  Tuatara (Sphenodon) genomics: BAC library construction, sequence survey, and application to the DMRT gene family. , 2006, The Journal of heredity.

[39]  D. Ray,et al.  Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus. , 2008, Genome research.

[40]  I King Jordan,et al.  Transposable elements and the evolution of eukaryotic complexity. , 2002, Current issues in molecular biology.

[41]  Niles Eldredge Reinventing Darwin: The Great Evolution Debate , 1995 .

[42]  D. Hartl,et al.  Evidence for interspecific transfer of the transposable element mariner betweenDrosophila andZaprionus , 1991, Journal of Molecular Evolution.

[43]  C. Feschotte,et al.  Endogenous viruses: insights into viral evolution and impact on host biology , 2012, Nature Reviews Genetics.

[44]  N. Fedoroff,et al.  Transposable Elements As a Molecular Evolutionary Force , 1999, Annals of the New York Academy of Sciences.

[45]  F. Ryan An alternative approach to medical genetics based on modern evolutionary biology. Part 4: HERVs in cancer , 2009, Journal of the Royal Society of Medicine.

[46]  H. Robertson,et al.  Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. , 1995, Molecular biology and evolution.

[47]  C. Feschotte,et al.  DNA transposons and the evolution of eukaryotic genomes. , 2007, Annual review of genetics.

[48]  Evan L. Mulligan,et al.  The Mouse Gene Encoding the Testis-Specific Isoform of Poly(A) Binding Protein (Pabp2) Is an Expressed Retroposon: Intimations That Gene Expression in Spermatogenic Cells Facilitates the Creation of New Genes , 1998, Journal of Molecular Evolution.

[49]  S. Wright,et al.  Evolution in Mendelian Populations. , 1931, Genetics.

[50]  J. Jurka,et al.  Families of transposable elements, population structure and the origin of species , 2011, Biology Direct.

[51]  J. Mccoy,et al.  Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis , 2000, Nature.

[52]  J. Volff Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[53]  J. Ortonne,et al.  Transposable B2 SINE elements can provide mobile RNA polymerase II promoters , 2001, Nature Genetics.

[54]  T. Moore,et al.  An abundant placental transcript containing an IAP-LTR is allelic to mouse pregnancy-specific glycoprotein 23 (Psg23): cloning and genetic analysis. , 2004, Gene.

[55]  Mouse Genome Sequencing Consortium Initial sequencing and comparative analysis of the mouse genome , 2002, Nature.

[56]  R. Nowak Walker's bats of the world , 1994 .

[57]  H. Lodish,et al.  Transcriptional inhibition of the murine erythropoietin receptor gene by an upstream repetitive element , 1993, Molecular and cellular biology.

[58]  Keith R. Oliver,et al.  Mobile DNA and the TE-Thrust hypothesis: supporting evidence from the primates , 2011, Mobile DNA.

[59]  Andrew G Smith,et al.  B2 SINE retrotransposon causes polymorphic expression of mouse 5-aminolevulinic acid synthase 1 gene. , 2008, Biochemical and biophysical research communications.

[60]  T. Heidmann,et al.  Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[61]  J. Galagan,et al.  RIP: the evolutionary cost of genome defense. , 2004, Trends in genetics : TIG.

[62]  Stéphane Boissinot,et al.  Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. , 2005, Genome research.

[63]  Jonathan B. Clark,et al.  Factors that affect the horizontal transfer of transposable elements. , 2004, Current issues in molecular biology.

[64]  J. Grootegoed,et al.  Testis-specific expression of a functional retroposon encoding glucose-6-phosphate dehydrogenase in the mouse. , 1997, Genomics.

[65]  H. Kazazian,et al.  Mobile elements and disease. , 1998, Current opinion in genetics & development.

[66]  J. Cubo Evidence for speciational change in the evolution of ratites (Aves: Palaeognathae) , 2003 .

[67]  P. Stenson,et al.  A systematic analysis of LINE-1 endonuclease-dependent retrotranspositional events causing human genetic disease , 2005, Human Genetics.

[68]  E. Sverdlov,et al.  Perpetually mobile footprints of ancient infections in human genome , 1998, FEBS letters.

[69]  M. Batzer,et al.  From the margins of the genome: mobile elements shape primate evolution , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[70]  Dixie L Mager,et al.  Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. , 2003, Trends in genetics : TIG.

[71]  M. Yanagisawa,et al.  Reduced Expression of the Endothelin Receptor Type B Gene in Piebald Mice Caused by Insertion of a Retroposon-like Element in Intron 1* , 2006, Journal of Biological Chemistry.

[72]  E. Meese,et al.  Human endogenous retroviruses in the primate lineage and their influence on host genomes , 2005, Cytogenetic and Genome Research.

[73]  M. Kress,et al.  The gene encoding the MOK-2 zinc-finger protein: characterization of its promoter and negative regulation by mouse Alu type-2 repetitive elements. , 1994, Gene.

[74]  David J. Anderson,et al.  Atypical expansion in mice of the sensory neuron-specific Mrg G protein-coupled receptor family , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[75]  G. Fourel,et al.  Expression of the woodchuck N-myc2 retroposon in brain and in liver tumors is driven by a cryptic N-myc promoter , 1992, Molecular and cellular biology.

[76]  David I. K. Martin,et al.  Epigenetic inheritance at the agouti locus in the mouse , 1999, Nature Genetics.

[77]  Jennifer F Hughes,et al.  Human endogenous retrovirus K solo-LTR formation and insertional polymorphisms: implications for human and viral evolution. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[78]  T. Heidmann,et al.  ERV-L Elements: a Family of Endogenous Retrovirus-Like Elements Active throughout the Evolution of Mammals , 1999, Journal of Virology.

[79]  J. McDonald,et al.  Evolution and consequences of transposable elements. , 1993, Current opinion in genetics & development.

[80]  U. Kämmerer,et al.  Human endogenous retrovirus K (HERV-K) is expressed in villous and extravillous cytotrophoblast cells of the human placenta. , 2011, Journal of reproductive immunology.

[81]  D. Kordis,et al.  Unusual horizontal transfer of a long interspersed nuclear element between distant vertebrate classes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[82]  Arnold J. Levine,et al.  Unexpected Inheritance: Multiple Integrations of Ancient Bornavirus and Ebolavirus/Marburgvirus Sequences in Vertebrate Genomes , 2010, PLoS pathogens.

[83]  J. Chamberlain,et al.  A B2 repeat insertion generates alternate structures of the mouse muscle gamma-phosphorylase kinase gene. , 1993, Genomics.

[84]  J. Cross,et al.  The evolution, regulation, and function of placenta-specific genes. , 2008, Annual review of cell and developmental biology.

[85]  D. Mager,et al.  Creation of the two isoforms of rodent NKG2D was driven by a B1 retrotransposon insertion , 2009, Nucleic acids research.

[86]  R. Baker,et al.  Natural hybridization generates mammalian lineage with species characteristics , 2010, Proceedings of the National Academy of Sciences.

[87]  Jennifer F. Hughes,et al.  Evidence for genomic rearrangements mediated by human endogenous retroviruses during primate evolution , 2001, Nature Genetics.

[88]  S. Gilbert,et al.  Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[89]  Jacob D. Jaffe,et al.  The genome of the green anole lizard and a comparative analysis with birds and mammals , 2011, Nature.

[90]  L. Tarantino,et al.  Comt1 genotype and expression predicts anxiety and nociceptive sensitivity in inbred strains of mice , 2010, Genes, brain, and behavior.

[91]  M. Pagel,et al.  Phylogenies reveal new interpretation of speciation and the Red Queen , 2010, Nature.

[92]  N. Okada,et al.  Poxviruses as possible vectors for horizontal transfer of retroposons from reptiles to mammals , 2007, Proceedings of the National Academy of Sciences.

[93]  M. A. McClure,et al.  The evolutionary dynamics of autonomous non-LTR retrotransposons in the lizard Anolis carolinensis shows more similarity to fish than mammals. , 2009, Molecular biology and evolution.

[94]  Y. Boie,et al.  Retroviral long terminal repeat is the promoter of the gene encoding the tumor-associated calcium-binding protein oncomodulin in the rat. , 1989, Journal of molecular biology.

[95]  Robert W. Williams,et al.  A Transposon in Comt Generates mRNA Variants and Causes Widespread Expression and Behavioral Differences among Mice , 2010, PloS one.

[96]  B. Koop,et al.  Bursts and horizontal evolution of DNA transposons in the speciation of pseudotetraploid salmonids , 2007, BMC Genomics.

[97]  J. Lingrel,et al.  Polymorphism in an androgen-regulated mouse gene is the result of the insertion of a B1 repetitive element into the transcription unit , 1986, Molecular and cellular biology.

[98]  Ellen J. Pritham Transposable elements and factors influencing their success in eukaryotes. , 2009, The Journal of heredity.

[99]  B. Spear,et al.  Hereditary persistence of alpha-fetoprotein and H19 expression in liver of BALB/cJ mice is due to a retrovirus insertion in the Zhx2 gene. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[100]  C. Ufer,et al.  Discovery of a functional retrotransposon of the murine phospholipid hydroperoxide glutathione peroxidase: chromosomal localization and tissue-specific expression pattern. , 2002, Genomics.

[101]  James A. Shapiro Transposable elements as the key to a 21st century view of evolution , 2000 .

[102]  R. ffrench-Constant,et al.  A Single P450 Allele Associated with Insecticide Resistance in Drosophila , 2002, Science.

[103]  J. Cubo,et al.  Testing gradual and speciational models of evolution in extant taxa: the example of ratites , 2012, Journal of evolutionary biology.

[104]  P. Michalak An eruption of mobile elements in genomes of hybrid sunflowers , 2010, Heredity.

[105]  Yoichi Ishida,et al.  Transposable elements and an epigenetic basis for punctuated equilibria , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[106]  Shigeyuki Esumi,et al.  Negative and positive effects of an IAP-LTR on nearby Pcdaα gene expression in the central nervous system and neuroblastoma cell lines , 2004 .

[107]  S. Pandalai,et al.  Mutation breeding, evolution, and the law of recurrent variation. , 2005 .

[108]  Vincent J. Lynch,et al.  Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals , 2011, Nature Genetics.

[109]  F. Tashiro,et al.  Molecular cloning and chromosomal mapping of mouse intronless myc gene acting as a potent apoptosis inducer. , 1999, Gene.

[110]  J.R. Harris The evolution of placental mammals , 1991, FEBS letters.

[111]  T. Kunz,et al.  Molecular phylogeny of New World Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. , 2007, Molecular phylogenetics and evolution.

[112]  Woo-Yeon Kim,et al.  Molecular Evolution of the Periphilin Gene in Relation to Human Endogenous Retrovirus M Element , 2006, Journal of Molecular Evolution.

[113]  Ariel Fernández,et al.  Nonadaptive origins of interactome complexity , 2011, Nature.

[114]  G. Barsh,et al.  Neomorphic agouti mutations in obese yellow mice , 1994, Nature Genetics.

[115]  N. C. Casavant,et al.  The end of the LINE?: lack of recent L1 activity in a group of South American rodents. , 2000, Genetics.

[116]  D. Witherspoon,et al.  Recent horizontal transfer of mellifera subfamily mariner transposons into insect lineages representing four different orders shows that selection acts only during horizontal transfer. , 2003, Molecular biology and evolution.

[117]  F. Ryan An alternative approach to medical genetics based on modern evolutionary biology. Part 1: mutation and symbiogenesis , 2009, Journal of the Royal Society of Medicine.

[118]  M. Benahmed,et al.  Recent evolutionary acquisition of alternative pre-mRNA splicing and 3' processing regulations induced by intronic B2 SINE insertion. , 1997, Nucleic acids research.

[119]  S. Gould The Structure of Evolutionary Theory , 2002 .

[120]  I. Darboux,et al.  Transposon‐mediated resistance to Bacillus sphaericus in a field‐evolved population of Culex pipiens (Diptera: Culicidae) , 2007, Cellular microbiology.

[121]  H. Wichman,et al.  Extinction of LINE-1 activity coincident with a major mammalian radiation in rodents , 2005, Cytogenetic and Genome Research.

[122]  I. Holm,et al.  Cloning and Sequencing of an Intronless Mouse S-Adenosylmethionine Decarboxylase Gene Coding for a Functional Enzyme Strongly Expressed in the Liver (*) , 1995, The Journal of Biological Chemistry.

[123]  Jerilyn A. Walker,et al.  SVA elements: a hominid-specific retroposon family. , 2005, Journal of molecular biology.

[124]  Frank Eisenhaber,et al.  Arxes: retrotransposed genes required for adipogenesis , 2010, Nucleic acids research.

[125]  Marc Vidal,et al.  Ten years of genetics and genomics: what have we achieved and where are we heading? , 2010, Nature Reviews Genetics.

[126]  A. Nekrutenko,et al.  Transposable elements are found in a large number of human protein-coding genes. , 2001, Trends in genetics : TIG.

[127]  Putting together the pieces: evolutionary mechanisms at work within genomes , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[128]  H. Wichman,et al.  Loss of LINE-1 Activity in the Megabats , 2008, Genetics.

[129]  Liane Gagnier,et al.  Retroviral Elements and Their Hosts: Insertional Mutagenesis in the Mouse Germ Line , 2006, PLoS genetics.

[130]  James L. Kitchen,et al.  Archaeogenomic evidence of punctuated genome evolution in Gossypium. , 2012, Molecular biology and evolution.

[131]  L. Villarreal Can Viruses Make Us Human? 1 , 2004 .

[132]  M. Brilliant,et al.  The mouse intracisternal A particle-promoted placental gene retrotransposition is mouse-strain-specific. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[133]  C. Vieira,et al.  Vertical inheritance and bursts of transposition have shaped the evolution of the BS non-LTR retrotransposon in Drosophila , 2011, Molecular Genetics and Genomics.

[134]  H. Kazazian Mobile Elements: Drivers of Genome Evolution , 2004, Science.

[135]  F. Ryan Genomic creativity and natural selection: a modern synthesis , 2006 .

[136]  L. Villarreal Can Viruses Make Us Human ? , 2004 .

[137]  F. Bokma,et al.  Extant mammal body masses suggest punctuated equilibrium , 2008, Proceedings of the Royal Society B: Biological Sciences.

[138]  P. Kloetzel,et al.  A second gene encoding the mouse proteasome activator PA28beta subunit is part of a LINE1 element and is driven by a LINE1 promoter. , 1999, Journal of molecular biology.

[139]  J. Bennetzen,et al.  A unified classification system for eukaryotic transposable elements , 2007, Nature Reviews Genetics.

[140]  H. Toju,et al.  Do arms races punctuate evolutionary stasis? Unified insights from phylogeny, phylogeography and microevolutionary processes , 2009, Molecular ecology.

[141]  M. G. Kidwell,et al.  Transposable elements as sources of variation in animals and plants. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[142]  M. Belfort,et al.  The take and give between retrotransposable elements and their hosts. , 2008, Annual review of genetics.

[143]  M. G. Kidwell,et al.  PERSPECTIVE: TRANSPOSABLE ELEMENTS, PARASITIC DNA, AND GENOME EVOLUTION , 2001, Evolution; international journal of organic evolution.

[144]  C. Feschotte,et al.  The evolutionary history of human DNA transposons: evidence for intense activity in the primate lineage. , 2007, Genome research.

[145]  R. Aitken,et al.  Identification and characterization of a novel Mt-retrotransposon highly represented in the female mouse germline. , 2006, Genomics.

[146]  Ellen J. Pritham,et al.  Pervasive Horizontal Transfer of Rolling-Circle Transposons among Animals , 2010, Genome biology and evolution.

[147]  James A. Shapiro,et al.  Transposable elements as the key to a 21st century view of evolution , 2004, Genetica.

[148]  J. Wienberg,et al.  Reciprocal chromosome painting shows that genomic rearrangement between rat and mouse proceeds ten times faster than between humans and cats , 1999, Cytogenetic and Genome Research.

[149]  T. Gojobori,et al.  Endogenous non-retroviral RNA virus elements in mammalian genomes , 2010, Nature.

[150]  Jürgen Brosius,et al.  Genomes were forged by massive bombardments with retroelements and retrosequences , 2004, Genetica.

[151]  T. Heidmann,et al.  Cloning of a new murine endogenous retrovirus, MuERV-L, with strong similarity to the human HERV-L element and with a gag coding sequence closely related to the Fv1 restriction gene , 1997, Journal of virology.

[152]  David J. Earl,et al.  Evolvability is a selectable trait. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[153]  E. Schon,et al.  RNA-mediated gene duplication: the rat preproinsulin I gene is a functional retroposon , 1985, Molecular and cellular biology.

[154]  J. Seidman,et al.  Functional insertion of an Alu type 2 (B2 SINE) repetitive sequence in murine class I genes. , 1984, Science.

[155]  M. Syvanen The evolutionary implications of mobile genetic elements. , 1984, Annual review of genetics.

[156]  J. Brosius,et al.  Retroposons--seeds of evolution. , 1991, Science.

[157]  D M Raup,et al.  The role of extinction in evolution. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[158]  S. Boissinot,et al.  The Evolution and Diversity of DNA Transposons in the Genome of the Lizard Anolis carolinensis , 2010, Genome biology and evolution.

[159]  N. Talbot,et al.  Evolution of Filamentous Plant Pathogens: Gene Exchange across Eukaryotic Kingdoms , 2006, Current Biology.

[160]  G. Petersen,et al.  A unified classification system for eukaryotic transposable elements should reflect their phylogeny , 2009, Nature Reviews Genetics.

[161]  J. Jurka,et al.  Self-synthesizing DNA transposons in eukaryotes. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[162]  R. Baker,et al.  MysTR: an Endogenous Retrovirus Family in Mammals That Is Undergoing Recent Amplifications to Unprecedented Copy Numbers , 2005, Journal of Virology.

[163]  P. Capy,et al.  The struggle for life of the genome's selfish architects , 2011, Biology Direct.

[164]  J. Shapiro,et al.  Why repetitive DNA is essential to genome function , 2005, Biological reviews of the Cambridge Philosophical Society.

[165]  O. R. Borodulina,et al.  Wide distribution of short interspersed elements among eukaryotic genomes , 1999, FEBS letters.

[166]  V. Valente,et al.  Complex evolution of gypsy in Drosophilid species. , 2004, Molecular biology and evolution.

[167]  Marlen S. Clark,et al.  Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods , 2008, Proceedings of the National Academy of Sciences.

[168]  Jean-Nicolas Volff,et al.  Transposable elements as drivers of genomic and biological diversity in vertebrates , 2008, Chromosome Research.

[169]  Haig H. Kazazian,et al.  An estimated frequency of endogenous insertional mutations in humans , 1999, Nature Genetics.

[170]  Douglas E. Soltis,et al.  Advances in the study of polyploidy since Plant speciation , 2003 .

[171]  G. Glazko,et al.  Origin of a substantial fraction of human regulatory sequences from transposable elements. , 2003, Trends in genetics : TIG.

[172]  T. Heidmann,et al.  Placental syncytins: Genetic disjunction between the fusogenic and immunosuppressive activity of retroviral envelope proteins , 2007, Proceedings of the National Academy of Sciences.

[173]  S. Boissinot,et al.  L1 (LINE-1) retrotransposon diversity differs dramatically between mammals and fish. , 2004, Trends in genetics : TIG.

[174]  J. Stavenhagen,et al.  An ancient provirus has imposed androgen regulation on the adjacent mouse sex-limited protein gene , 1988, Cell.

[175]  C. A. Dunn,et al.  Repeated Recruitment of LTR Retrotransposons as Promoters by the Anti-Apoptotic Locus NAIP during Mammalian Evolution , 2006, PLoS genetics.

[176]  J. Shapiro,et al.  Mobile DNA and evolution in the 21st century , 2010, Mobile DNA.

[177]  J. Drezen,et al.  Transfer of a chromosomal Maverick to endogenous bracovirus in a parasitoid wasp , 2011, Genetica.

[178]  F. Ryan Darwin's Blind Spot: Evolution Beyond Natural Selection , 2002 .

[179]  D. Ray,et al.  A non-LTR retroelement extinction in Spermophilus tridecemlineatus. , 2012, Gene.

[180]  F. Ryan Viruses as symbionts. , 2007 .

[181]  A. Burt,et al.  Long-term reinfection of the human genome by endogenous retroviruses. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[182]  F. Gage,et al.  The necessary junk: new functions for transposable elements. , 2007, Human molecular genetics.

[183]  D. Mager,et al.  Endogenous retroviral LTRs as promoters for human genes: a critical assessment. , 2009, Gene.

[184]  Eugene Rosenberg,et al.  The role of microorganisms in coral health, disease and evolution , 2007, Nature Reviews Microbiology.

[185]  Philipp W. Messer,et al.  Genome-Wide Patterns of Adaptation to Temperate Environments Associated with Transposable Elements in Drosophila , 2010, PLoS genetics.

[186]  M. Lynch The frailty of adaptive hypotheses for the origins of organismal complexity , 2007, Proceedings of the National Academy of Sciences.

[187]  J. Jurka,et al.  A universal classification of eukaryotic transposable elements implemented in Repbase , 2008, Nature Reviews Genetics.

[188]  D A Kramerov,et al.  Origin and evolution of SINEs in eukaryotic genomes , 2011, Heredity.

[189]  E. Steele Lamarck and Immunity : Somatic and Germline Evolution of Antibody Genes , 2009 .

[190]  B. Mcclintock,et al.  The significance of responses of the genome to challenge. , 1984, Science.

[191]  J. Werren Selfish genetic elements, genetic conflict, and evolutionary innovation , 2011, Proceedings of the National Academy of Sciences.

[192]  M. Goddard,et al.  Copy Number Variation and Transposable Elements Feature in Recent, Ongoing Adaptation at the Cyp6g1 Locus , 2010, PLoS genetics.

[193]  Philip C. J. Donoghue,et al.  MicroRNAs and the advent of vertebrate morphological complexity , 2008, Proceedings of the National Academy of Sciences.

[194]  D. Ray,et al.  The limited distribution of Helitrons to vesper bats supports horizontal transfer. , 2011, Gene.

[195]  M. Nonaka,et al.  Insertion of the B2 sequence into intron 13 is the only defect of the H-2k C4 gene which causes low C4 production. , 1992, Nucleic acids research.

[196]  D. Ray,et al.  Bats with hATs: evidence for recent DNA transposon activity in genus Myotis. , 2006, Molecular biology and evolution.

[197]  S. Wessler Eukaryotic Transposable Elements : Teaching Old Genomes New Tricks , 2006 .

[198]  J. Honacki,et al.  Mammal species of the world : a taxonomic and geographic reference , 1982 .

[199]  L. Villarreal Origin of Group Identity: Viruses, Addiction and Cooperation , 2008 .

[200]  Gratien G. Prefontaine,et al.  Developmentally Regulated Activation of a SINE B2 Repeat as a Domain Boundary in Organogenesis , 2007, Science.

[201]  L. Johnson,et al.  Polyadenylylation signal of the mouse thymidylate synthase gene was created by insertion of an L1 repetitive element downstream of the open reading frame. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[202]  E. Lutz,et al.  Characterisation of the Mouse Vasoactive Intestinal Peptide Receptor Type 2 Gene, Vipr2, and Identification of a Polymorphic LINE-1-like Sequence That Confers Altered Promoter Activity , 2007, Journal of neuroendocrinology.

[203]  Cédric Feschotte,et al.  Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus , 2007, Proceedings of the National Academy of Sciences.

[204]  L. Schalkwyk,et al.  A B2 SINE insertion in the Comt1 gene (Comt1B2i) results in an overexpressing, behavior modifying allele present in classical inbred mouse strains , 2010, Genes, brain, and behavior.

[205]  A. Ashworth,et al.  Zfa is an expressed retroposon derived from an alternative transcript of the Zfx gene. , 1990, The EMBO journal.

[206]  K. Schwartz,et al.  Characterization of a novel transcript of retroviral origin expressed in rat heart and liver. , 1995, Journal of molecular and cellular cardiology.

[207]  D. Anxolabéhère,et al.  Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. , 1988, Molecular biology and evolution.

[208]  Luca Comai,et al.  Genetic and epigenetic interactions in allopolyploid plants , 2000, Plant Molecular Biology.

[209]  J. Mattick The central role of RNA in human development and cognition , 2011, FEBS letters.

[210]  M. G. Kidwell,et al.  Evidence for horizontal transmission of the P transposable element between Drosophila species. , 1990, Genetics.

[211]  J. Bennetzen,et al.  Transposable element contributions to plant gene and genome evolution , 2004, Plant Molecular Biology.

[212]  Lisa M. D'Souza,et al.  Genome sequence of the Brown Norway rat yields insights into mammalian evolution , 2004, Nature.

[213]  D. A. Kramerov,et al.  Bov-B-mobilized SINEs in vertebrate genomes. , 2008, Gene.

[214]  B. Mcclintock,et al.  Controlling elements and the gene. , 1956, Cold Spring Harbor symposia on quantitative biology.

[215]  T. Mackay,et al.  The Genetic Architecture of Odor-Guided Behavior in Drosophila melanogaster , 2001, Behavior genetics.

[216]  H. Wichman,et al.  Retrofitting the Genome: L1 Extinction Follows Endogenous Retroviral Expansion in a Group of Muroid Rodents , 2011, Journal of Virology.

[217]  D. Mager,et al.  Insertional polymorphisms of ETn retrotransposons include a disruption of the wiz gene in C57BL/6 mice , 2002, Mammalian Genome.

[218]  Jeffrey E. Barrick,et al.  Second-Order Selection for Evolvability in a Large Escherichia coli Population , 2011, Science.

[219]  N. Okada,et al.  Unique mammalian tRNA-derived repetitive elements in dermopterans: the t-SINE family and its retrotransposition through multiple sources. , 2003, Molecular biology and evolution.