Different regulatory mechanisms underlie similar transposable element profiles in pufferfish and fruitflies.

Comparative analysis of recently sequenced eukaryotic genomes has uncovered extensive variation in transposable element (TE) abundance, diversity, and distribution. The TE profile in the sequenced pufferfish genomes is more similar to that of Drosophila melanogaster than to human or mouse, in that pufferfish TEs exhibit low overall abundance, high family diversity, and localization in the heterochromatin. It has been suggested that selection against the deleterious effects of ectopic recombination between TEs has structured the TE profile in Drosophila and pufferfish but not in humans. We test this hypothesis by measuring the sample frequency of 48 euchromatic TE insertions in the genome of the green spotted pufferfish (Tetraodon nigroviridis). We estimate the strength of selection acting on recent insertions by analyzing the site frequency spectrum using a maximum-likelihood approach. We show that in contrast to Drosophila, euchromatic TE insertions in Tetraodon are selectively neutral and that the low copy number and compartmentalized distribution of TEs in the Tetraodon genome must be caused by regulation by means other than purifying selection acting on recent insertions. Inference of regulatory processes governing TE profiles should take into account factors such as effective population size, incidence of inbreeding/outcrossing, and other species-specific traits.

[1]  X. Maside,et al.  The lack of recombination drives the fixation of transposable elements on the fourth chromosome of Drosophila melanogaster. , 2004, Genetical research.

[2]  A. Pélisson,et al.  Evidence for rapid limitation of the I element copy number in a genome submitted to several generations of I-R hybrid dysgenesis in Drosophila melanogaster , 1987, Molecular and General Genetics MGG.

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

[4]  S. Nuzhdin Sure facts, speculations, and open questions about the evolution of transposable element copy number , 2004, Genetica.

[5]  D. Hartl,et al.  Regulation of the transposable element mariner , 2004, Genetica.

[6]  J. Brookfield,et al.  Population genetics models of transposable elements , 2004, Genetica.

[7]  J. Volff,et al.  Diversity of retrotransposable elements in compact pufferfish genomes. , 2003, Trends in genetics : TIG.

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

[9]  Ronald H. A. Plasterk,et al.  Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi , 2003, Nature.

[10]  D. Garfinkel,et al.  Post-transcriptional cosuppression of Ty1 retrotransposition. , 2003, Genetics.

[11]  S. Wright,et al.  Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. , 2003, Genome research.

[12]  J. Weissenbach,et al.  An active non-LTR retrotransposon with tandem structure in the compact genome of the pufferfish Tetraodon nigroviridis. , 2003, Genome research.

[13]  A. E. Hirsh,et al.  Size matters: non-LTR retrotransposable elements and ectopic recombination in Drosophila. , 2003, Molecular biology and evolution.

[14]  T. Bestor,et al.  Cytosine methylation mediates sexual conflict. , 2003, Trends in genetics : TIG.

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

[16]  J. Weissenbach,et al.  Remarkable compartmentalization of transposable elements and pseudogenes in the heterochromatin of the Tetraodon nigroviridis genome , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Brian Charlesworth,et al.  On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. , 2002, Molecular biology and evolution.

[18]  M. Batzer,et al.  Alu repeats and human genomic diversity , 2002, Nature Reviews Genetics.

[19]  Y. Jiang Transcriptional cosuppression of yeast Ty1 retrotransposons. , 2002, Genes & development.

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

[21]  R. Poulter,et al.  The DIRS1 group of retrotransposons. , 2001, Molecular biology and evolution.

[22]  S. Wright,et al.  Population dynamics of an Ac-like transposable element in self- and cross-pollinating arabidopsis. , 2001, Genetics.

[23]  M. Morgan Transposable element number in mixed mating populations. , 2001, Genetical research.

[24]  S. Boissinot,et al.  Selection against deleterious LINE-1-containing loci in the human lineage. , 2001, Molecular biology and evolution.

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

[26]  International Human Genome Sequencing Consortium Initial sequencing and analysis of the human genome , 2001, Nature.

[27]  S Wright,et al.  Transposon diversity in Arabidopsis thaliana. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Klein,et al.  Ancient allelism at the cytosolic chaperonin-alpha-encoding gene of the zebrafish. , 2000, Genetics.

[29]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[30]  T. Heidmann,et al.  Cosuppression of I transposon activity in Drosophila by I-containing sense and antisense transgenes. , 1999, Genetics.

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

[32]  W. Belknap,et al.  Characterization of Repetitive DNA Elements in Arabidopsis , 1999, Journal of Molecular Evolution.

[33]  D. Duvernell,et al.  VARIATION AND DIVERGENCE OF DEATH VALLEY PUPFISH POPULATIONS AT RETROTRANSPOSON-DEFINED LOCI , 1999 .

[34]  Julio Rozas,et al.  DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis , 1999, Bioinform..

[35]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[36]  A. Ballabio,et al.  LINE-1 elements at the sites of molecular rearrangements in Alport syndrome-diffuse leiomyomatosis. , 1999, American journal of human genetics.

[37]  G. B. Petersen,et al.  Is gene deletion in eukaryotes sequence-dependent? A study of nine deletion junctions and nineteen other deletion breakpoints in intron 7 of the human dystrophin gene. , 1998, Gene.

[38]  C. Walsh,et al.  Transcription of IAP endogenous retroviruses is constrained by cytosine methylation , 1998, Nature Genetics.

[39]  R. O’Neill,et al.  Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid , 1998, Nature.

[40]  B. Burwinkel,et al.  Unequal homologous recombination between LINE-1 elements as a mutational mechanism in human genetic disease. , 1998, Journal of molecular biology.

[41]  J. Drake,et al.  Rates of spontaneous mutation. , 1998, Genetics.

[42]  S. Sherry,et al.  Alu evolution in human populations: using the coalescent to estimate effective population size. , 1997, Genetics.

[43]  G. Gloor,et al.  Homology requirements for targeting heterologous sequences during P-induced gap repair in Drosophila melanogaster. , 1997, Genetics.

[44]  N. Okada,et al.  The salmon SmaI family of short interspersed repetitive elements (SINEs): interspecific and intraspecific variation of the insertion of SINEs in the genomes of chum and pink salmon. , 1997, Genetics.

[45]  S. Nuzhdin,et al.  Positive association between copia transposition rate and copy number in Drosophila melanogaster , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[46]  B. Charlesworth,et al.  Transposable elements in inbreeding and outbreeding populations. , 1995, Genetics.

[47]  J. Wallenburg,et al.  Integration of a vector containing a repetitive LINE-1 element in the human genome. , 1994, Molecular and cellular biology.

[48]  J. Felsenstein,et al.  Estimating effective population size from samples of sequences: inefficiency of pairwise and segregating sites as compared to phylogenetic estimates. , 1992, Genetical research.

[49]  D. Lindsley,et al.  The Genome of Drosophila Melanogaster , 1992 .

[50]  C. Langley,et al.  Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. , 1991, Genetics.

[51]  N E Morton,et al.  Parameters of the human genome. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[52]  O. Smithies,et al.  Homology requirements for unequal crossing over in humans. , 1991, Genetics.

[53]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[54]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[55]  B. Charlesworth,et al.  A study of ten families of transposable elements on X chromosomes from a population of Drosophila melanogaster. , 1989, Genetical research.

[56]  J. Hey The transposable portion of the genome of Drosophila algonquin is very different from that in D. melanogaster. , 1989, Molecular biology and evolution.

[57]  R. Hudson,et al.  On the role of unequal exchange in the containment of transposable element copy number. , 1988, Genetical research.

[58]  B. Charlesworth,et al.  A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. , 1987, Genetical research.

[59]  B. Charlesworth,et al.  The evolution of self-regulated transposition of transposable elements. , 1986, Genetics.

[60]  S. Tavaré,et al.  Line-of-descent and genealogical processes, and their applications in population genetics models. , 1984, Theoretical population biology.

[61]  Simon Tavaré,et al.  Lines-of-descent and genealogical processes, and their applications in population genetics models , 1984, Advances in Applied Probability.

[62]  S. W. Rasmussen,et al.  The synaptonemal complex in genetic segregation. , 1984, Annual review of genetics.

[63]  D. von Wettstein The synaptonemal complex and genetic segregation. , 1984, Symposia of the Society for Experimental Biology.

[64]  W. Gehring,et al.  Unequal crossing-over associated with asymmetrical synapsis between nomadic elements in the Drosophila melanogaster genome. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[65]  C. Langley,et al.  Transposable Elements in Mendelian Populations. II. Distribution of Three COPIA-like Elements in a Natural Population of DROSOPHILA MELANOGASTER. , 1983, Genetics.

[66]  W. Ewens Mathematical Population Genetics , 1980 .

[67]  A. Bucheton,et al.  Non-mendelian female sterility in Drosophila melanogaster: Quantitative variations in the efficiency of inducer and reactive strains , 1976, Heredity.

[68]  G. A. Watterson On the number of segregating sites in genetical models without recombination. , 1975, Theoretical population biology.

[69]  T. Nagylaki The moments of stochastic integrals and the distribution of sojourn times. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[70]  W. Feller An Introduction to Probability Theory and Its Applications , 1959 .