Abstract
Transposable elements are major components of both prokaryotic and eukaryotic genomes. They are generally considered as “selfish DNA” sequences able to invade the chromosomes of a species in a parasitic way, leading to a plethora of mutations such as insertions, deletions, inversions, translocations and complex rearrangements. They are frequently deleterious, but sometimes provide a source of genetic diversity. Numerous population genetics models have been proposed to describe more precisely the dynamics of these complex genomic components, and despite a wide diversity among transposable elements and their hosts, the colonization process appears to be roughly predictable. In this paper, we aim to describe and comment on some of the theoretical studies, and attempt to define the “life cycle” of these genomic nomads. We further raise some new issues about the impact of moving sequences in the evolution and the structure of genomes.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Abrahamsen M, Templeton T, Enomoto S, Abrahante J, Zhu G, Lancto C, Deng M, Liu C, Widmer G, Tzipori S et al. (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304:441–445
Agrawal A, Eastman QM, Schatz DG (1998) Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394:744–751
Andrews JD, Gloor GB (1995) A role for the KP Leucine Zipper in regulating P element transposition in Drosophila melanogaster. Genetics 135:81–95
Anxolabéhère D, Benes H, Nouaud D, Périquet G (1987) Evolutionary steps and transposable elements in Drosophila melanogaster: the missing RP type obtained by genetic transformation. Evolution 4:846–853
Anxolabéhère D, Kidwell MG, Périquet G (1988) Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. Mol Biol Evol 5:252–269
Aravind L (2000) The BED finger, a novel DNA-binding domain in chromatin-boundary-element-binding proteins and transposases. Trends Biochem Sci 25:421–423
Arkhipova I, Meselson M (2000) Transposable elements in sexual and anciant asexual taxa. Proc Natl Acad Sci USA 97:14473–14477
Arkhipova I, Meselson M (2005) Deleterious transposable elements and the extinction of asexuals. Bioessays 27:76–85
Badge RM, Brookfield JFY (1997) The role of host factors in the population dynamics of selfish transposable elements. J Theor Biol 187:261–271
Bestor T (2003) Cytosine methylation mediates sexual conflict. Trends Genet 19:185–190
Bestor TH (1999) Sex brings transposons and genomes into conflict. Genetica 107:289–295
Biémont C (1994) Dynamic equilibrium between insertion and excision of P elements in highly inbred lines from an M′strain of Drosophila melanogaster. J Mol Evol 39:466–472
Biémont C, Nardon C, Deceliere G, Lepetit D, Loevenbruck C, Vieira C (2003) Worldwide distribution of transposable element copy number in natural populations of Drosophila simulans. Evolution 57:159–167
Birchler JA, Pal-Bhadra M, Bhadra U (1999) Less from more: cosuppression of transposable elements. Nature Genet 21:148–149
Bird AP (1997) Does DNA methylation control transposition of selfish elements in the germline? Trends Genet 13:469–470
Boissinot S, Chevret P, Furano A (2000) L1 (LINE-1) retrotransposon evolution and amplification in recent human history. Mol Biol Evol 17:915–928
Bonnivard E, Bazin C, Denis B, Higuet D (2000) A scenario for the hobo transposable element invasion, deduced from the structure of natural populations of Drosophila melanogaster using tandem TPE repeats. Genet Res 75:13–23
Bregliano JC, Kidwell MG (1983) Mobile Genetic Elements. chap. Hybrid Dysgenesis Determinants, p 363. Academic Press, inc.
Brookfield J (1982) Interspersed repetitive DNA sequences are unlikely to be parasitic. J Theor Biol 94:281–299
Brookfield JFY (1995) Mobile genetics elements. chap. Transposable elements as selfish DNA. Oxford University Press, New York, p 131–153
Brookfield J (2003) Mobile DNAs: the poacher turned gamekeeper. Curr Biol 13:R846–R847
Brookfield JFY, Badge RM (1997) Population genetics models of transposable elements. Genetica 52:281–294
Brosius J (2005) Disparity, adaptation, exaptation, bookkeeping, and the contingency at the genome level. Paleobiology 31:1–16
Bucheton A (1990) I transposable elements and I-R hybrid dysgenesis in Drosophila. Trends Genet 6:16–21
Burke WB, Malik HS, Lathe WC, Eickbush TH (1998) Are retrotransposons long-term hitchhikers? Nature 392:141–142
Cambareri EB, Jensen BC, Schabtach E, Selker EU (1989) Repeat-induced G–C to A–T mutations in Neurospora crassa. Science 244:1571–1575
Capy P, Gasperi G, Biémont C, Bazin C (2000) Stress and transposable elements: co-evolution or useful parasites? Heredity 85:101–106
Carlton J, Angiuoli S, Suh B, Kooij T, Pertea M, Silva J, Ermolaeva M, Allen J, Selengut J, Koo H et al. (2002) Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 419:512–519
Charlesworth B (1991) Transposable elements in natural populations with a mixture of selected and neutral insertion sites. Genet Res 57:127–134
Charlesworth B (1996) Background selection and patterns of genetic diversity in Drosophila melanogaster. Genet Res 68:131–149
Charlesworth B, Charlesworth D (1983) The population dynamics of transposable elements. Genet Res 42:1–27
Charlesworth B, Langley CH (1986) The evolution of self-regulated transposition of transposable elements. Genetics 112:359–383
Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220
Coen D, Lemaitre B, Delattre M, Quesneville H, Ronsseray S, Simonelig M, Higuet D, Lehmann M, Montchamp C, Nouaud D (1994) Drosophila P element: transposition, regulation and evolution. Genetica 93:61–78
Corish P, Black D, Featherston D, Merriam J, Dover G (1996) Natural repressors of P-induced hybrid dysgenesis in Drosophila melanogaster: a model for repressor evolution. Genet Res 67:109–121
Davis C, Wurdack K (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305:676–678
Deceliere G, Charles S, Biémont C (2005) The dynamics of transposable elements in structured populations. Genetics 169:467–474
Doolittle W, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603
Doolittle WF, Kirkwood TBL, Dempster MAH (1984) Selfish DNA with self-restraint. Nature 307:501–502
Eanes WF, Wesley C, Hey J, Houle D (1988) The fitness consequences of P element insertion in Drosophila melanogaster. Genet Res 52:17–26
Eggleston W, Johnson-Schlitz D, Engels W (1988) P-M hybrid dysgenesis does not mobilize other transposable element families in Drosophila melanogaster. Nature 331:368–370
Engels WR (1989) Mobile DNA. chap. P elements in Drosophila melanogaster, p 437–484. American Society of Microbiology
Engels W (1997) Invasions of P elements. Genetics 145:11–15
Feschotte C, Mouchès C (2000) Evidence that a family of miniature inverted-repeat transposable elements (MITEs) from the Arabidopsis thaliana genome has arisen from a pogo-like DNA transposon. Mol Biol Evol 17:730–737
Ganko E, Bhattacharjee V, Schliekelman P, McDonald J (2003) Evidence for the contribution of LTR retrotransposons to C. elegans gene evolution. Mol Biol Evol 20:1925–1931
Ganko E, Fielman K, McDonald J (2001) Evolutionary history of Cer elements and their impact on the C. elegans genome. Genome Res 11:2066–2074
Gerasimova TI, Mizrokhi LJ, Georgiev GP (1984) Transposition bursts in genetically unstable Drosophila melanogaster. Nature 309:714–716
Gould SJ (2002) The structure of evolutionary theory. Belknap Press of Harvard University Press, Cambridge, Mass
Gloor et al. (1993) Type I repressors of P element mobility. Genetics 135:81–95
Hickey DA (1982) Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101:519–531
Hood M, Katawczik M, Giraud T (2005) Repeat-induced point mutation and the population structure of transposable elements in microbotryum violaceum. Genetics 170:1081–1089
Holt R, Subramanian G, Halpern A, Sutton G, Charlab R, Nusskern D, Wincker P, Clark A, Ribeiro J, Wides R et al. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149
Houle D, Nuzhdin SV (2004) Mutation accumulation and the effect of copia insertions in Drosophila melanogaster. Genet Res 83:7–18
Hua-Van A, Le Rouzic A, Maisonhaute C, Capy P (2005) Abundance, distribution and dynamics of retrotransposable elements and transposons: similarities and differences. Cytogenet Genome Res 110:426–440
Inouye S, Furuichi T, Dhundale A, Inouye M (1987) Molecular biology of RNA: new perspectives. chap. Stable branched RNA covalently linked to the 5′end of a single-stranded DNA of Myxobacteria, p 271–284. Academic Press, San Diego/London
Izsvak Z, Ivics Z (2004) Sleeping beauty transposition: biology and applications for molecular therapy. Mol Ther 9:147–156
Jackson M, Black D, Dover G (1988) Amplification of KP elements associated with the repression of hybrid dysgenesis in Drosophila melanogaster. Genetics 120:1003–1013
Jordan I, Rogozin I, Glazko G, Koonin E (2003) Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet 19:68–72
Kaplan N, Darden T, Langley CH (1985) Evolution and extinction of transposable elements in mendelian populations. Genetics 109:459–480
Katinka M, Duprat S, Cornillot E, Metenier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P et al. (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450–453
Kazazian H (2000) L1 retrotransposons shape the mammalian genome. Science 289:1152–1153
Kidwell M (1983) Evolution of hybrid dysgenesis determinants in Drosophila melano- gaster. Proc Natl Acad Sci USA 80:1655–1659
Kidwell MG (1992) Horizontal transfer. Curr Opin Genet Dev 2:868–873
Kidwell MG, Lisch DR (2001) Transposable elements, parasitic DNA, and genome evolution. Evolution 55:1–24
Kurland C, Canback B, Berg O (2003) Horizontal gene transfer: a critical view. Proc Natl Acad Sci USA 100:9658–9662
Labrador M, Corces VG (1997) Transposable element-host interactions: regulation of insertion and excision. Annu Rev Genet 31:381–404
Lampe D, Witherspoon D, Soto-Adames F, Robertson H (2003) Recent horizontal transfer of mellifera subfamily mariner transposons into insect lineages representing four different orders shows that selection acts only during horizontal transfer. Mol Biol Evol 20:554–562
Langley CH, Montgomery E, Hudson R, Kaplan N, Charlesworth B (1988) On the role of unequal exchange in the containment of transposable element copy number. Genet Res 52:223–235
Lankenau S, Corces VG, Lankenau DH (1994) The Drosophila micropia retrotransposon encodes a testis-specific antisense RNA complementary to reverse transcriptase. Mol Cell Biol 14:1764–1775
Lankenau DH, Gloor GB (1998) In vivo gap repair in Drosophila: a one-way street with many destinations. BioEssays 20:317–327
Le Rouzic A, Capy P (2005) The first steps of transposable elements invasion: parasitic strategy vs. genetic drift. Genetics 169:1033–1043
Le Rouzic A, Deceliere G (2005) The models of population genetics of transposable elements. Genet Res 85:171–181
Leaver M (2001) A family of Tc1-like transposons from the genomes of fishes and frogs: evidence for horizontal transmission. Gene 271:203–214
Lemaitre B, Ronsseray S, Coen D (1993) Maternal repression of the P element promoter in the germline of Drosophila melanogaster: a model for the P cytotype. Genetics 135:149–160
Lippmann Z, May B, Yordan C, Singer T, Martienssen R (2003) Distinct mechanisms determine transposon inheritance and methylation via small interfering DNA and histone modification. PLoS Biol 1:420–428
Mackay TFC, Lyman R, Jackson M (1992) Effects of P element insertions on quantitative traits in Drosophila melanogaster. Genetics 130:315–332
Mackay TFC (1985) Transposable element-induced response to artificial selection in Drosophila melanogaster. Genetics 111:351–374
Marin L, Lehmann M, Nouaud D, Izaabel H, Anxolabehere D, Ronsseray S (2000) P-elem- ent repression in Drosophila melanogaster by a naturally occurring defective telomeric P copy. Genetics 155:1841–1854
Martienssen R (1998) Transposons, DNA methylation and gene control. Trends Genet 14:263–264
Maside X, Assimacopoulos S, Charlesworth B (2000) Rates of movement of transposable elements on the second chromosome of Drosophila melanogaster. Genet Res 75:275–284
Miller W, McDonald J, Nouaud D, Anxolabéhère D (1999) Molecular domestication – more than a sporadic episode in evolution. Genetica 107:197–207
Montchamp-Moreau C (1990) Dynamics of P-M hybrid dygenesis in P-transformed lines of Drosophila simulans. Evolution 44:194–203
Morgan MT (2001) Transposable element number in mixed mating populations. Genet Res 77:261–275
Nuzhdin SV (1999) Sure facts, speculations, and open questions about evolution of transposable elements. Genetica 107:129–137
Nuzhdin SV, Mackay TFC (1995) The genomic rate of transposable element movement in Drosophila melanogaster. Mol Biol Evol 12:180–181
Ohta T (1986) Population genetics of an expanding family of mobile genetic elements. Genetics 113:145–159
Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607
Pardue ML, DeBaryshe P (2003) Retrotransposons provide an evolutionnary robust non-telomerase mechanism to maintain telomeres. Annu Rev Genet 37:485–511
Petrov DA (2001) Evolution of genome size: new approches to an old problem. Trends Genet 17:23–28
Petrov D, Hartl D (1998) High rate of DNA loss in the Drosophila melanogaster and Drosophila viridis species group. Mol Biol Evol 15:293–302
Petrov D, Schutzman J, Hartl D, Lozovskaya E (1995) Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis. Proc Natl Acad Sci USA 92:8050–8054
Quesneville H, Anxolabéhère D (1998) Dynamics of transposable elements in metapopulations: a model of P elements invasion in Drosophila. Theor Pop Biol 54:175–193
Quesneville H, Anxolabéhère D (2001) Genetic algorithm-based model of evolutionnary dynamics of class II transposable elements. J Theor Biol 213:21–30
Quesneville H, Nouaud D, Anxolabéhère D (2003) Detection of new transposable element families in Drosophila melanogaster and Anopheles gambiae genomes. J Mol Evol 57 Suppl 1:S50–S59
Rio DC (1991) Regulation of Drosophila P element transposition. Trends Genet 7:282–287
Roussigne M, Kossida S, Lavigne A, Clouaire T, Ecochard V, Glories A, Amalric F, Girard J (2003) The THAP domain: a novel protein motif with similarity to the DNA-binding domain of P element transposase. Trends Biochem Sci 28:66–69
San Miguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z et al. (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768
Sanchez-Gracia A, Maside X, Charlesworth B (2005) High rate of horizontal transfer of transposable elements in Drosophila. Trends Genet 21:200–203
Silva J, Loreto E, Clark J (2004) Factors that affect the horizontal transfer of transposable elements. Curr Issues Mol Biol 6:57–71
Simmons M, Raymond J, Rasmusson K, Miller L, McLarnon C, Zunt J (1990) Repression of P element-mediated hybrid dysgenesis in Drosophila melanogaster. Genetics 124:663–676
Snyder M, Doolittle W (1988) P elements in Drosophila: selection at many levels. Trends Genet 4:147–149
Suh D, Choi E, Yamazaki T, Harada K (1995) Studies on the transposition rates of mobile genetic elements in a natural population of Drosophila melanogaster. Mol Biol Evol 12:748–758
Tsitrone A, Charles S, Biémont C (1999) Dynamics of transposable elements under the selection model. Genet Res 74:159–164
Vieira C, Biémont C (2004) Transposable element dynamics in two sibling species: Drosophila melanogaster and Drosophila simulans. Genetica 120:115–123
Vieira C, Lepetit D, Dumont S, Biemont C (1999) Wake up of transposable elements following Drosophila simulans worldwide colonization. Mol Biol Evol 16:1251–1255
Vieira J, Vieira C, Hartl D, Lozovskaya E (1998) Factors contributing to the hybrid dysgenesis syndrome in Drosophila virilis. Genet Res 71:109–117
Vitte C, Panaud O (2003) Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotransposons in rice Oryza sativa L. Mol Biol Evol 20:528–540
Weiner A (2002) SINEs and LINEs: the art of biting the hand that feeds you. Curr Opin Cell Biol 14:343–350
Witherspoon D (1999) Selective constraints on P-element evolution. Mol Biol Evol 16:472–478
Woodruff R, Thompson J Jr, Gu S (2004) Premeiotic clusters of mutation and the cost of natural selection. J Hered 95:277–283
Wright SI, Schoen DJ (1999) Transposon dynamics and the breeding system. Genetica 107:139–148
Xu P, Widmer G, Wang Y, Ozaki L, Alves J, Serrano M, Puiu D, Manque P, Akiyoshi D, Mackey A et al. (2004) The genome of Cryptosporidium hominis. Nature 431:1107–1112
Xu T, Deng K (2002) Sex and retrotransposons: a new approach to the problem. J Theor Biol 218:259–260
Yoder JA, Walsh CP, Bestor TH (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13:335–340
Zeyl C, Bell G, Green DM (1996) Sex and spread of retrotransposon ty3 in experimental populations of Saccharomyces cerevisiae. Genetics 143:1567–1577
Acknowledgments
We would like to thank D. Lankenau and two anonymous referees for their useful comments. The English text was reviewed by M. Eden.
Author information
Authors and Affiliations
Corresponding author
Editor information
Rights and permissions
Copyright information
© 2006 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Le Rouzic, A., Capy, P. (2006). Theoretical Approaches to the Dynamics of Transposable Elements in Genomes, Populations, and Species. In: Lankenau, DH., Volff, JN. (eds) Transposons and the Dynamic Genome. Genome Dynamics and Stability, vol 4. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7050_017
Download citation
DOI: https://doi.org/10.1007/7050_017
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-02004-9
Online ISBN: 978-3-642-02005-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)