Dynamics of transposable elements: towards a community ecology of the genome.

Like ecological communities, which vary in species composition, eukaryote genomes differ in the amount and diversity of transposable elements (TEs) that they harbor. Given that TEs have a considerable impact on the biology of their host species, we need to better understand whether their dynamics reflects some form of organization or is primarily driven by stochastic processes. Here, we borrow ecological concepts on species diversity to explore how interactions between TEs can contribute to structure TE communities within their genomic ecosystem. Whereas the niche theory predicts a stable diversity of TEs because of their divergent characteristics, the neutral theory of biodiversity predicts the assembly of TE communities from stochastic processes acting at the level of the individual TE. Contrary to ecological communities, however, TE communities are shaped by selection at the level of their ecosystem (i.e. the host individual). Developing ecological models specific to the genome will thus be a prerequisite for modeling the dynamics of TEs.

[1]  F. Jiggins,et al.  The evolution of RNAi as a defence against viruses and transposable elements , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[2]  M. Pardue,et al.  Retrotransposons provide an evolutionarily robust non-telomerase mechanism to maintain telomeres. , 2003, Annual review of genetics.

[3]  C. Vieira,et al.  Wake up of transposable elements following Drosophila simulans worldwide colonization. , 1999, Molecular biology and evolution.

[4]  David Tilman,et al.  Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Arnaud Le Rouzic,et al.  Population Genetics Models of Competition Between Transposable Element Subfamilies , 2006, Genetics.

[6]  B. Potts,et al.  A framework for community and ecosystem genetics: from genes to ecosystems , 2006, Nature Reviews Genetics.

[7]  D. Lisch.  Epigenetic regulation of transposable elements in plants. , 2009, Annual review of plant biology.

[8]  Boris Jerchow,et al.  Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates , 2009, Nature Genetics.

[9]  S. Wessler,et al.  Dramatic amplification of a rice transposable element during recent domestication , 2006, Proceedings of the National Academy of Sciences.

[10]  T. Ohta.  Population genetics of transposable elements. , 1984, IMA journal of mathematics applied in medicine and biology.

[11]  D. Wilson,et al.  Artificial ecosystem selection. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[12]  L. Landweber,et al.  A Functional Role for Transposases in a Large Eukaryotic Genome , 2009, Science.

[13]  M. Batzer,et al.  Extensive individual variation in L1 retrotransposition capability contributes to human genetic diversity. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[14]  R. Dawkins.  The Extended Phenotype , 1982 .

[15]  Sergey V Nuzhdin,et al.  Intracellular battlegrounds: conflict and cooperation between transposable elements. , 2002, Genetical research.

[16]  Mathew A. Leibold,et al.  Metacommunities: Spatial Dynamics and Ecological Communities , 2005 .

[17]  B. Charlesworth,et al.  Transposable element distributions in Drosophila. , 1997, Genetics.

[18]  S. Boissinot,et al.  Adaptive evolution in LINE-1 retrotransposons. , 2001, Molecular biology and evolution.

[19]  S. Wright,et al.  Transposon dynamics and the breeding system , 2004, Genetica.

[20]  C. Feschotte.  Transposable elements and the evolution of regulatory networks , 2008, Nature Reviews Genetics.

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

[22]  H. L. Carson,et al.  The Genetics and Biology of Drosophila , 1976, Heredity.

[23]  S. DiFazio,et al.  Extending Genomics to Natural Communities and Ecosystems , 2008, Science.

[24]  J. Stinchcombe,et al.  An emerging synthesis between community ecology and evolutionary biology. , 2007, Trends in ecology & evolution.

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

[26]  C. Vieira,et al.  Infra- and Transspecific Clues to Understanding the Dynamics of Transposable Elements , 2009 .

[27]  H. Krambeck,et al.  Competition may determine the diversity of transposable elements. , 2006, Theoretical population biology.

[28]  C. Bergman,et al.  Recent LTR retrotransposon insertion contrasts with waves of non-LTR insertion since speciation in Drosophila melanogaster , 2007, Proceedings of the National Academy of Sciences.

[29]  P. Deininger,et al.  Mammalian non-LTR retrotransposons: for better or worse, in sickness and in health. , 2008, Genome research.

[30]  M. Batzer,et al.  Retrotransposable elements and human disease. , 2006, Genome dynamics.

[31]  Cédric Feschotte,et al.  Genome-wide analysis of mariner-like transposable elements in rice reveals complex relationships with stowaway miniature inverted repeat transposable elements (MITEs). , 2003, Genetics.

[32]  P. Capy,et al.  Abundance, distribution and dynamics of retrotransposable elements and transposons: similarities and differences , 2005, Cytogenetic and Genome Research.

[33]  J. Mekalanos,et al.  Hyperactive transposase mutants of the Himar1 mariner transposon. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[35]  D. Tilman.  Resource competition and community structure. , 1983, Monographs in population biology.

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

[37]  Daniel F Voytas,et al.  Chromodomains direct integration of retrotransposons to heterochromatin. , 2008, Genome research.

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

[39]  Jonathan M. Chase,et al.  Ecological Niches: Linking Classical and Contemporary Approaches , 2003 .

[40]  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.

[41]  M. Lynch,et al.  The Origins of Genome Complexity , 2003, Science.

[42]  C. Hoogland,et al.  Transposable element distribution in Drosophila. , 1997, Genetics.

[43]  G. van der Velde,et al.  Ecological niches. Linking classical and contemporary approaches , 2008 .

[44]  D. Hickey.  Selfish DNA: a sexually-transmitted nuclear parasite. , 1982, Genetics.

[45]  James P. Grover,et al.  Simple Rules for Interspecific Dominance in Systems with Exploitative and Apparent Competition , 1994, The American Naturalist.

[46]  B. Charlesworth,et al.  The population genetics of Drosophila transposable elements. , 1989, Annual review of genetics.

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

[48]  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.

[49]  G. Bell.  Neutral macroecology. , 2001, Science.

[50]  D. Hartl,et al.  Modern thoughts on an ancyent marinere: function, evolution, regulation. , 1997, Annual review of genetics.

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

[52]  T. Mackay,et al.  The genomic rate of transposable element movement in Drosophila melanogaster. , 1995, Molecular biology and evolution.

[53]  A. Furano,et al.  Fruit flies and humans respond differently to retrotransposons. , 2002, Current opinion in genetics & development.

[54]  C. Vieira,et al.  What transposable elements tell us about genome organization and evolution: the case of Drosophila , 2005, Cytogenetic and Genome Research.

[55]  A. Le Rouzic,et al.  Models of the population genetics of transposable elements. , 2005, Genetical research.

[56]  Eörs Szathmáry,et al.  The Major Transitions in Evolution , 1997 .

[57]  R. Holt.  Emergent neutrality. , 2006, Trends in ecology & evolution.

[58]  Population Genetics Models 3.1 Introduction , 2022 .

[59]  D. Rio,et al.  Identification and analysis of a hyperactive mutant form of Drosophila P-element transposase. , 2002, Genetics.

[60]  Arnaud Le Rouzic,et al.  Long-term evolution of transposable elements , 2007, Proceedings of the National Academy of Sciences.

[61]  Gregory J. Hannon,et al.  Small RNAs as Guardians of the Genome , 2009, Cell.

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

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

[64]  N. Saitou,et al.  Possible involvement of SINEs in mammalian-specific brain formation , 2008, Proceedings of the National Academy of Sciences.

[65]  C. Biémont,et al.  The Dynamics of Transposable Elements in Structured Populations , 2005, Genetics.

[66]  S. Hubbell,et al.  The unified neutral theory of biodiversity and biogeography at age ten. , 2011, Trends in ecology & evolution.

[67]  Cédric Feschotte,et al.  Mariner-like transposases are widespread and diverse in flowering plants , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[68]  C. Vieira,et al.  Transposition rate of the 412 retrotransposable element is independent of copy number in natural populations of Drosophila simulans. , 1997, Molecular biology and evolution.

[69]  P. Chesson.  Mechanisms of Maintenance of Species Diversity , 2000 .

[70]  Jef D. Boeke,et al.  A highly active synthetic mammalian retrotransposon , 2004, Nature.

[71]  Michael Lynch,et al.  The Origins of Genome Architecture , 2007 .

[72]  M. Boerlijst,et al.  Selection at the level of the community: the importance of spatial structure , 2002 .

[73]  E. Richards,et al.  Differential Epigenetic Regulation Within an Arabidopsis Retroposon Family , 2007, Genetics.

[74]  C. Vieira,et al.  The heterochromatic copies of the LTR retrotransposons as a record of the genomic events that have shaped the Drosophila melanogaster genome. , 2008, Gene.

[75]  J. Jurka,et al.  RAG1 Core and V(D)J Recombination Signal Sequences Were Derived from Transib Transposons , 2005, PLoS biology.

[76]  S. Dupas,et al.  Genome ecosystem and transposable elements species. , 2007, Gene.

[77]  R. Martienssen,et al.  Transposable elements and the epigenetic regulation of the genome , 2007, Nature Reviews Genetics.

[78]  Rongcheng Lin,et al.  Transposase-Derived Transcription Factors Regulate Light Signaling in Arabidopsis , 2007, Science.

[79]  Colin N. Dewey,et al.  Initial sequencing and comparative analysis of the mouse genome. , 2002 .

[80]  J. V. Moran,et al.  Initial sequencing and analysis of the human genome. , 2001, Nature.

[81]  J. V. Moran,et al.  Hot L1s account for the bulk of retrotransposition in the human population , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[82]  H. Robertson,et al.  Loss of transposase-DNA interaction may underlie the divergence of mariner family transposable elements and the ability of more than one mariner to occupy the same genome. , 2001, Molecular biology and evolution.

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

[84]  R. Mauricio.  Can ecology help genomics: the genome as ecosystem? , 2005, Genetica.

[85]  John F. Y. Brookfield,et al.  The ecology of the genome — mobile DNA elements and their hosts , 2005, Nature Reviews Genetics.

[86]  C. Biémont.  Population genetics of transposable DNA elements , 2004, Genetica.

[87]  Hywel T. P. Williams,et al.  Artificial selection of simulated microbial ecosystems , 2007, Proceedings of the National Academy of Sciences.

[88]  J. Jurka,et al.  Molecular paleontology of transposable elements in the Drosophila melanogaster genome , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[89]  M. G. Kidwell,et al.  Transposable elements and host genome evolution. , 2000, Trends in ecology & evolution.