Copy number increases of transposable elements and protein‐coding genes in an invasive fish of hybrid origin

Evolutionary dynamics of structural genetic variation in lineages of hybrid origin is not well explored, although structural mutations may increase in controlled hybrid crosses. We therefore tested whether structural variants accumulate in a fish of recent hybrid origin, invasive Cottus, relative to both parental species Cottus rhenanus and Cottus perifretum. Copy‐number variation in exons of 10,979 genes was assessed using comparative genome hybridization arrays. Twelve genes showed significantly higher copy numbers in invasive Cottus compared to both parents. This coincided with increased expression for three genes related to vision, detoxification and muscle development, suggesting possible gene dosage effects. Copy number increases of putative transposons were assessed by comparative mapping of genomic DNA reads against a de novo assembly of 1,005 repetitive elements. In contrast to exons, copy number increases of repetitive elements were common (20.7%) in invasive Cottus, whereas decrease was very rare (0.01%). Among the increased repetitive elements, 53.8% occurred at higher numbers in C. perifretum compared to C. rhenanus, while only 1.4% were more abundant in C. rhenanus. This implies a biased mutational process that amplifies genetic material from one ancestor. To assess the frequency of de novo mutations through hybridization, we screened 64 laboratory‐bred F2 offspring between the parental species for copy‐number changes at five candidate loci. We found no evidence for new structural variants, indicating that they are too rare to be detected given our sampling scheme. Instead, they must have accumulated over more generations than we observed in a controlled cross.

[1]  C. Pigott Genetics and the Origin of Species , 1959, Nature.

[2]  Dr. Susumu Ohno Evolution by Gene Duplication , 1970, Springer Berlin Heidelberg.

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

[4]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[5]  Loren H. Rieseberg,et al.  Hybrid Origins of Plant Species , 1997 .

[6]  C. Miranda,et al.  Expression of a constitutive cytochrome P450 (CYP2K1) in livers of rainbow trout (Oncorhynchus mykiss) embryo and sac-fry , 1997 .

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

[8]  L. Rieseberg,et al.  Transgressive segregation, adaptation and speciation , 1999, Heredity.

[9]  Roger Bivand,et al.  Implementing functions for spatial statistical analysis using the language , 2000, J. Geogr. Syst..

[10]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

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

[12]  W. J. Kent,et al.  BLAT--the BLAST-like alignment tool. , 2002, Genome research.

[13]  Giovanni Parmigiani,et al.  Human L1 Retrotransposition Is Associated with Genetic Instability In Vivo , 2002, Cell.

[14]  P. Danielson,et al.  The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans. , 2002, Current drug metabolism.

[15]  Danielson Pb,et al.  The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans. , 2002 .

[16]  C. Pál,et al.  Dosage sensitivity and the evolution of gene families in yeast , 2003, Nature.

[17]  M. Cáceres,et al.  The foldback-like transposon Galileo is involved in the generation of two different natural chromosomal inversions of Drosophila buzzatii. , 2003, Molecular biology and evolution.

[18]  M. Labrador,et al.  High transposition rates of Osvaldo, a new Drosophila buzzatii retrotransposon , 1994, Molecular and General Genetics MGG.

[19]  L. Rieseberg,et al.  Candidate gene polymorphisms associated with salt tolerance in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. , 2003, The New phytologist.

[20]  N. Iizuka,et al.  Altered Levels of Cytochrome P450 Genes in Hepatitis B or C Virus-infected Liver Identified by Oligonucleotide Microarray. , 2004, Cancer genomics & proteomics.

[21]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

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

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

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

[25]  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.

[26]  R. Andrews,et al.  Exon array CGH: detection of copy-number changes at the resolution of individual exons in the human genome. , 2005, American journal of human genetics.

[27]  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.

[28]  M. Batzer,et al.  Emergence of primate genes by retrotransposon-mediated sequence transduction , 2006, Proceedings of the National Academy of Sciences.

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

[30]  Giovanni Parmigiani,et al.  Pre-processing Agilent microarray data , 2007, BMC Bioinformatics.

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

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

[33]  D. Hartl,et al.  Genome clashes in hybrids: insights from gene expression , 2007, Heredity.

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

[35]  Sven Becker,et al.  Housekeeping genes for quantitative expression studies in the three-spined stickleback Gasterosteus aculeatus , 2008, BMC Molecular Biology.

[36]  M. Ungerer,et al.  Proliferation of Ty3/gypsy-like retrotransposons in hybrid sunflower taxa inferred from phylogenetic data , 2009, BMC Biology.

[37]  Z. Gompert,et al.  Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations , 2009, Molecular ecology.

[38]  Beatrice Bateson,et al.  William Bateson, Naturalist: Heredity and Variation in Modern Lights , 2009 .

[39]  J. Hemingway,et al.  Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. , 2008, Genome research.

[40]  P. Michalak Epigenetic, transposon and small RNA determinants of hybrid dysfunctions , 2009, Heredity.

[41]  M. Pellegrini,et al.  Copy number variation influences gene expression and metabolic traits in mice. , 2009, Human molecular genetics.

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

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

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

[45]  Sébastien Renaut,et al.  Mining transcriptome sequences towards identifying adaptive single nucleotide polymorphisms in lake whitefish species pairs (Coregonus spp. Salmonidae) , 2010, Molecular ecology.

[46]  F. Kondrashov,et al.  The evolution of gene duplications: classifying and distinguishing between models , 2010, Nature Reviews Genetics.

[47]  C. Parisod,et al.  Impact of transposable elements on the organization and function of allopolyploid genomes. , 2010, The New phytologist.

[48]  W. Amos Heterozygosity and mutation rate: evidence for an interaction and its implications , 2010, BioEssays : news and reviews in molecular, cellular and developmental biology.

[49]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

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

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

[52]  M. Ungerer,et al.  Transposable Element Proliferation and Genome Expansion Are Rare in Contemporary Sunflower Hybrid Populations Despite Widespread Transcriptional Activity of LTR Retrotransposons , 2011, Genome biology and evolution.

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

[54]  Surong Hasi,et al.  Genome sequences of wild and domestic bactrian camels , 2012, Nature Communications.

[55]  F. Kondrashov Gene duplication as a mechanism of genomic adaptation to a changing environment , 2012, Proceedings of the Royal Society B: Biological Sciences.

[56]  T. Itakura,et al.  Cytochrome P450 (CYP) in fish. , 2012, Environmental toxicology and pharmacology.

[57]  A. Pozhitkov,et al.  Transcriptome changes after genome‐wide admixture in invasive sculpins (Cottus) , 2012, Molecular ecology.

[58]  Stephen J. Palmer,et al.  GTF2IRD2 from the Williams–Beuren critical region encodes a mobile-element-derived fusion protein that antagonizes the action of its related family members , 2012, Journal of Cell Science.

[59]  D. Joyce,et al.  Gene duplication in an African cichlid adaptive radiation , 2014, BMC Genomics.

[60]  M. Ungerer,et al.  Transcriptional Dynamics of LTR Retrotransposons in Early Generation and Ancient Sunflower Hybrids , 2013, Genome biology and evolution.

[61]  R. C. Karn,et al.  The role of retrotransposons in gene family expansions: insights from the mouse Abp gene family , 2013, BMC Evolutionary Biology.

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

[63]  A. Nolte,et al.  The genomics of incompatibility factors and sex determination in hybridizing species of Cottus (Pisces) , 2013, Heredity.

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

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

[66]  D. Coughlin,et al.  Thermal acclimation in rainbow smelt, Osmerus mordax, leads to faster myotomal muscle contractile properties and improved swimming performance , 2013, Biology Open.

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

[68]  Yunfeng Ling,et al.  Multiplexed target detection using DNA-binding dye chemistry in droplet digital PCR. , 2013, Analytical chemistry.

[69]  Erich Bornberg-Bauer,et al.  Genome‐wide patterns of standing genetic variation in a marine population of three‐spined sticklebacks , 2013, Molecular ecology.

[70]  C. Parisod,et al.  Transposable elements and microevolutionary changes in natural populations , 2013, Molecular ecology resources.

[71]  Vaishali Katju,et al.  Copy-number changes in evolution: rates, fitness effects and adaptive significance , 2013, Front. Genet..

[72]  Helga Thorvaldsdóttir,et al.  Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration , 2012, Briefings Bioinform..

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

[74]  P. Andolfatto,et al.  HOW COMMON IS HOMOPLOID HYBRID SPECIATION? , 2014, Evolution; international journal of organic evolution.

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

[76]  D. Cooper,et al.  SVA retrotransposon insertion-associated deletion represents a novel mutational mechanism underlying large genomic copy number changes with non-recurrent breakpoints , 2014, Genome Biology.

[77]  M. P. Guerreiro Interspecific hybridization as a genomic stressor inducing mobilization of transposable elements in Drosophila , 2014, Mobile genetic elements.

[78]  J. S. Hermansen,et al.  Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species , 2014, PLoS genetics.

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

[80]  B. Langmead,et al.  Lighter: fast and memory-efficient sequencing error correction without counting , 2014, Genome Biology.

[81]  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.

[82]  Hanlee P. Ji,et al.  Correction to High Sensitivity Detection and Quantitation of DNA Copy Number and Single Nucleotide Variants with Single Color Droplet Digital PCR , 2015, Analytical chemistry.

[83]  D. Tautz,et al.  A Revised Design for Microarray Experiments to Account for Experimental Noise and Uncertainty of Probe Response , 2013, PloS one.

[84]  M. P. Guerreiro,et al.  Changes of Osvaldo expression patterns in germline of male hybrids between the species Drosophila buzzatii and Drosophila koepferae , 2015, Molecular Genetics and Genomics.

[85]  Nicholas W. Roberts,et al.  Cyp27c1 Red-Shifts the Spectral Sensitivity of Photoreceptors by Converting Vitamin A1 into A2 , 2015, Current Biology.

[86]  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.

[87]  M. Tress,et al.  The Evolutionary Fate of Alternatively Spliced Homologous Exons after Gene Duplication , 2015, Genome biology and evolution.

[88]  G. Fain Phototransduction: Making the Chromophore to See Through the Murk , 2015, Current Biology.

[89]  Matthew E. Ritchie,et al.  limma powers differential expression analyses for RNA-sequencing and microarray studies , 2015, Nucleic acids research.

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

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

[92]  Srikanth Gottipati,et al.  Evidence for the fixation of gene duplications by positive selection in Drosophila , 2016, Genome research.

[93]  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.

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