Genome‐wide patterns of transposon proliferation in an evolutionary young hybrid fish

Hybridization can induce transposons to jump into new genomic positions, which may result in their accumulation across the genome. Alternatively, transposon copy numbers may increase through nonallelic (ectopic) homologous recombination in highly repetitive regions of the genome. The relative contribution of transposition bursts versus recombination‐based mechanisms to evolutionary processes remains unclear because studies on transposon dynamics in natural systems are rare. We assessed the genomewide distribution of transposon insertions in a young hybrid lineage (“invasive Cottus”, n = 11) and its parental species Cottus rhenanus (n = 17) and Cottus perifretum(n = 9) using a reference genome assembled from long single molecule pacbio reads. An inventory of transposable elements was reconstructed from the same data and annotated. Transposon copy numbers in the hybrid lineage increased in 120 (15.9%) out of 757 transposons studied here. The copy number increased on average by 69% (range: 10%–197%). Given the age of the hybrid lineage, this suggests that they have proliferated within a few hundred generations since admixture began. However, frequency spectra of transposon insertions revealed no increase in novel and rare insertions across assembled parts of the genome. This implies that transposons were added to repetitive regions of the genome that remain difficult to assemble. Future studies will need to evaluate whether recombination‐based mechanisms rather than genomewide transposition may explain the majority of the recent transposon proliferation in the hybrid lineage. Irrespectively of the underlying mechanism, the observed overabundance in repetitive parts of the genome suggests that gene‐rich regions are unlikely to be directly affected.

[1]  David J. Miller,et al.  Finding Nemo’s Genes: A chromosome‐scale reference assembly of the genome of the orange clownfish Amphiprion percula , 2018, bioRxiv.

[2]  T. Bureau,et al.  Exaptation of transposable element coding sequences. , 2018, Current opinion in genetics & development.

[3]  B. Gaut,et al.  Modeling Interactions between Transposable Elements and the Plant Epigenetic Response: A Surprising Reliance on Element Retention , 2018, Genome biology and evolution.

[4]  J. de Meaux,et al.  Robustness of Transposable Element Regulation but No Genomic Shock Observed in Interspecific Arabidopsis Hybrids , 2018, bioRxiv.

[5]  Alexander Suh,et al.  Abundant recent activity of retrovirus‐like retrotransposons within and among flycatcher species implies a rich source of structural variation in songbird genomes , 2018, Molecular ecology.

[6]  D. Barbash,et al.  Beyond speciation genes: an overview of genome stability in evolution and speciation. , 2017, Current opinion in genetics & development.

[7]  Neva C. Durand,et al.  Hybrid de novo genome assembly and centromere characterization of the gray mouse lemur (Microcebus murinus) , 2017, BMC Biology.

[8]  E. Betrán,et al.  Transposable Element Domestication As an Adaptation to Evolutionary Conflicts. , 2017, Trends in genetics : TIG.

[9]  D. Barbash,et al.  Double insertion of transposable elements provides a substrate for the evolution of satellite DNA , 2017, bioRxiv.

[10]  Cesar Martins,et al.  Centromeric enrichment of LINE-1 retrotransposons and its significance for the chromosome evolution of Phyllostomid bats , 2017, Chromosome Research.

[11]  C. Vieira,et al.  High-Throughput Sequencing of Transposable Element Insertions Suggests Adaptive Evolution of the Invasive Asian Tiger Mosquito Towards Temperate Environments , 2016, bioRxiv.

[12]  R. B. Azevedo,et al.  The Evolution of Small RNA-Mediated Silencing of an Invading Transposable Element , 2017, bioRxiv.

[13]  C. Vieira,et al.  Transposable Element Misregulation Is Linked to the Divergence between Parental piRNA Pathways in Drosophila Hybrids , 2017, Genome biology and evolution.

[14]  F. Sedlazeck,et al.  Copy number increases of transposable elements and protein‐coding genes in an invasive fish of hybrid origin , 2017, Molecular ecology.

[15]  Steven G. Schroeder,et al.  Single-molecule sequencing and chromatin conformation capture enable de novo reference assembly of the domestic goat genome , 2017, Nature Genetics.

[16]  S. Koren,et al.  Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation , 2016, bioRxiv.

[17]  B. Mellone,et al.  Centromeres Drive a Hard Bargain. , 2017, Trends in genetics : TIG.

[18]  Evan A. Clayton,et al.  Population and clinical genetics of human transposable elements in the (post) genomic era , 2017, Mobile genetic elements.

[19]  L. Hurst,et al.  Mutation rate analysis via parent–progeny sequencing of the perennial peach. I. A low rate in woody perennials and a higher mutagenicity in hybrids , 2016, Proceedings of the Royal Society B: Biological Sciences.

[20]  M. Quail,et al.  The industrial melanism mutation in British peppered moths is a transposable element , 2016, Nature.

[21]  C. Parisod,et al.  Differential introgression and reorganization of retrotransposons in hybrid zones between wild wheats , 2016, Molecular ecology.

[22]  C. Vieira,et al.  Genomic evidence for adaptive evolution of the invasive Asian tiger mosquito towards temperate environment , 2016 .

[23]  F. Han,et al.  De Novo Centromere Formation and Centromeric Sequence Expansion in Wheat and its Wide Hybrids , 2016, PLoS genetics.

[24]  C. Feschotte,et al.  Regulatory evolution of innate immunity through co-option of endogenous retroviruses , 2016, Science.

[25]  Robert D. Finn,et al.  The Pfam protein families database: towards a more sustainable future , 2015, Nucleic Acids Res..

[26]  Elizabeth Hénaff,et al.  Jitterbug: somatic and germline transposon insertion detection at single-nucleotide resolution , 2015, BMC Genomics.

[27]  Xiayun Jiang,et al.  Tc1-like Transposase Thm3 of Silver Carp (Hypophthalmichthys molitrix) Can Mediate Gene Transposition in the Genome of Blunt Snout Bream (Megalobrama amblycephala) , 2015, G3: Genes, Genomes, Genetics.

[28]  Evgeny M. Zdobnov,et al.  BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs , 2015, Bioinform..

[29]  T. Wicker,et al.  Genome-wide comparison of Asian and African rice reveals high recent activity of DNA transposons , 2015, Mobile DNA.

[30]  C. Parisod,et al.  Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation , 2015, Proceedings of the Royal Society B: Biological Sciences.

[31]  L. Bernatchez,et al.  Reproductive isolation in a nascent species pair is associated with aneuploidy in hybrid offspring , 2015, Proceedings of the Royal Society B: Biological Sciences.

[32]  Floriane Plard,et al.  Comparative Analysis of Transposable Elements Highlights Mobilome Diversity and Evolution in Vertebrates , 2015, Genome biology and evolution.

[33]  A. Belyayev Bursts of transposable elements as an evolutionary driving force , 2014, Journal of evolutionary biology.

[34]  Maite G. Barrón,et al.  Population genomics of transposable elements in Drosophila. , 2014, Annual review of genetics.

[35]  Matthias Zytnicki,et al.  Tedna: a transposable element de novo assembler , 2014, Bioinform..

[36]  A. Quinlan BEDTools: The Swiss‐Army Tool for Genome Feature Analysis , 2014, Current protocols in bioinformatics.

[37]  L. Rieseberg,et al.  Genomics of homoploid hybrid speciation: diversity and transcriptional activity of long terminal repeat retrotransposons in hybrid sunflowers , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[38]  C. Vieira,et al.  Specific Activation of an I-Like Element in Drosophila Interspecific Hybrids , 2014, Genome biology and evolution.

[39]  H. Quesneville,et al.  PASTEC: An Automatic Transposable Element Classification Tool , 2014, PloS one.

[40]  L. Bernatchez,et al.  RNA-seq reveals transcriptomic shock involving transposable elements reactivation in hybrids of young lake whitefish species. , 2014, Molecular biology and evolution.

[41]  Andrew C. Adey,et al.  Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions , 2013, Nature Biotechnology.

[42]  Arndt von Haeseler,et al.  NextGenMap: fast and accurate read mapping in highly polymorphic genomes , 2013, Bioinform..

[43]  S. Boissinot,et al.  Lizards and LINEs: Selection and Demography Affect the Fate of L1 Retrotransposons in the Genome of the Green Anole (Anolis carolinensis) , 2013, Genome biology and evolution.

[44]  Aaron A. Klammer,et al.  Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data , 2013, Nature Methods.

[45]  A. Wong,et al.  RECURRENT AND RECENT SELECTIVE SWEEPS IN THE piRNA PATHWAY , 2013, Evolution; international journal of organic evolution.

[46]  Josefa González,et al.  The impact of transposable elements in environmental adaptation , 2013, Molecular ecology.

[47]  Thomas M. Keane,et al.  RetroSeq: transposable element discovery from next-generation sequencing data , 2013, Bioinform..

[48]  Robert A. Martienssen,et al.  RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond , 2013, Nature Reviews Genetics.

[49]  U. Dieckmann,et al.  Hybridization and speciation , 2013, Journal of evolutionary biology.

[50]  C. Bergman,et al.  An Age-of-Allele Test of Neutrality for Transposable Element Insertions , 2012, Genetics.

[51]  D. Mager,et al.  Transposable elements: an abundant and natural source of regulatory sequences for host genes. , 2012, Annual review of genetics.

[52]  J. Boeke,et al.  Active transposition in genomes. , 2012, Annual review of genetics.

[53]  D. Barbash,et al.  Drosophila Interspecific Hybrids Phenocopy piRNA-Pathway Mutants , 2012, PLoS biology.

[54]  Ira M. Hall,et al.  YAHA: fast and flexible long-read alignment with optimal breakpoint detection , 2012, Bioinform..

[55]  Miriam K. Konkel,et al.  Centromere Remodeling in Hoolock leuconedys (Hylobatidae) by a New Transposable Element Unique to the Gibbons , 2012, Genome biology and evolution.

[56]  A. Fujiyama,et al.  Centromere-targeted de novo integrations of an LTR retrotransposon of Arabidopsis lyrata. , 2012, Genes & development.

[57]  S. Maheshwari,et al.  The genetics of hybrid incompatibilities. , 2011, Annual review of genetics.

[58]  D. Petrov,et al.  Population genomics of transposable elements in Drosophila melanogaster. , 2011, Molecular biology and evolution.

[59]  D. Tautz,et al.  Rapid formation of distinct hybrid lineages after secondary contact of two fish species (Cottus sp.) , 2011, Molecular ecology.

[60]  A. Futschik,et al.  PoPoolation: A Toolbox for Population Genetic Analysis of Next Generation Sequencing Data from Pooled Individuals , 2011, PloS one.

[61]  D. Tautz,et al.  Copy number changes of CNV regions in intersubspecific crosses of the house mouse. , 2010, Molecular biology and evolution.

[62]  Diethard Tautz,et al.  Understanding the onset of hybrid speciation. , 2010, Trends in genetics : TIG.

[63]  Y. Wakamatsu,et al.  Distribution of complete and defective copies of the Tol1 transposable element in natural populations of the medaka fish Oryzias latipes. , 2009, Genes & genetic systems.

[64]  I. Amit,et al.  Comprehensive mapping of long range interactions reveals folding principles of the human genome , 2011 .

[65]  Richard C. Moore,et al.  The genomic organization of Ty3/gypsy-like retrotransposons in Helianthus (Asteraceae) homoploid hybrid species. , 2009, American journal of botany.

[66]  Josefa González,et al.  High Rate of Recent Transposable Element–Induced Adaptation in Drosophila melanogaster , 2008, PLoS biology.

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

[68]  R. O’Neill,et al.  Genomic Instability Within Centromeres of Interspecific Marsupial Hybrids , 2007, Genetics.

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

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

[71]  M. A. McClure,et al.  Identification of Novel Retroid Agents in Danio rerio, Oryzias latipes, Gasterosteus aculeatus and Tetraodon nigroviridis , 2007, Evolutionary bioinformatics online.

[72]  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.

[73]  P. Deininger,et al.  Inviting instability: Transposable elements, double-strand breaks, and the maintenance of genome integrity. , 2007, Mutation research.

[74]  J. Mallet Hybrid speciation , 2007, Nature.

[75]  Jerzy Jurka,et al.  Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor , 2006, BMC Bioinformatics.

[76]  J. Hancock,et al.  Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. , 2006, The Plant journal : for cell and molecular biology.

[77]  A. Iida,et al.  Vertebrate DNA transposon as a natural mutator: the medaka fish Tol2 element contributes to genetic variation without recognizable traces. , 2006, Molecular biology and evolution.

[78]  D. Tautz,et al.  When invaders meet locally adapted types: rapid moulding of hybrid zones between sculpins (Cottus, Pisces) in the Rhine system , 2006, Molecular ecology.

[79]  S. Jackson,et al.  Retrotransposon accumulation and satellite amplification mediated by segmental duplication facilitate centromere expansion in rice. , 2005, Genome research.

[80]  D. Tautz,et al.  An invasive lineage of sculpins, Cottus sp. (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogeographic groups , 2005, Proceedings of the Royal Society B: Biological Sciences.

[81]  A. Fontdevila Hybrid genome evolution by transposition , 2005, Cytogenetic and Genome Research.

[82]  J. Jurka,et al.  Repbase Update, a database of eukaryotic repetitive elements , 2005, Cytogenetic and Genome Research.

[83]  E. Eichler,et al.  Punctuated duplication seeding events during the evolution of human chromosome 2p11. , 2005, Genome research.

[84]  Stefan R. Henz,et al.  A gene expression map of Arabidopsis thaliana development , 2005, Nature Genetics.

[85]  D. Hartl,et al.  Different regulatory mechanisms underlie similar transposable element profiles in pufferfish and fruitflies. , 2004, Molecular biology and evolution.

[86]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

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

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

[89]  G. Carvalho,et al.  Timing of the population dynamics of bullhead Cottus gobio (Teleostei: Cottidae) during the Pleistocene , 2002 .

[90]  S. Henikoff,et al.  The Centromere Paradox: Stable Inheritance with Rapidly Evolving DNA , 2001, Science.

[91]  R. O’Neill,et al.  Chromosome heterozygosity and de novo chromosome rearrangements in mammalian interspecies hybrids , 2001, Mammalian Genome.

[92]  J. Volff,et al.  Multiple lineages of the non-LTR retrotransposon Rex1 with varying success in invading fish genomes. , 2000, Molecular biology and evolution.

[93]  D. Tautz,et al.  Phylogeography of the bullhead Cottus gobio (Pisces: Teleostei: Cottidae) suggests a pre‐Pleistocene origin of the major central European populations , 2000, Molecular ecology.

[94]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[95]  M. Plohl,et al.  Evolution of satellite DNAs from the genus Palorus--experimental evidence for the "library" hypothesis. , 1998, Molecular biology and evolution.

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

[97]  B. Charlesworth,et al.  The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. III. Element abundances in heterochromatin. , 1994, Genetical research.

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

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

[100]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[101]  B. Charlesworth,et al.  The population dynamics of transposable elements , 1983 .

[102]  N. Fedoroff,et al.  Investigation of the organization of mammalian chromosomes at the DNA sequence level. , 1976, Federation proceedings.