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Transposable elements and early evolution of sex chromosomes in fish

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Abstract

In many organisms, the sex chromosome pair can be recognized due to heteromorphy; the Y and W chromosomes have often lost many genes due to the absence of recombination during meiosis and are frequently heterochromatic. Repetitive sequences are found at a high proportion on such heterochromatic sex chromosomes and the evolution and emergence of sex chromosomes has been connected to the dynamics of repeats and transposable elements. With an amazing plasticity of sex determination mechanisms and numerous instances of independent emergence of novel sex chromosomes, fish represent an excellent lineage to investigate the early stages of sex chromosome differentiation, where sex chromosomes often are homomorphic and not heterochromatic. We have analyzed the composition, distribution, and relative age of TEs from available sex chromosome sequences of seven teleost fish. We observed recent bursts of TEs and simple repeat accumulations around young sex determination loci. More strikingly, we detected transposable element (TE) amplifications not only on the sex determination regions of the Y and W sex chromosomes, but also on the corresponding regions of the X and Z chromosomes. In one species, we also clearly demonstrated that the observed TE-rich sex determination locus originated from a TE-poor genomic region, strengthening the link between TE accumulation and emergence of the sex determination locus. Altogether, our results highlight the role of TEs in the initial steps of differentiation and evolution of sex chromosomes.

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Abbreviations

BAC:

Bacterial artificial chromosome

bp:

Base pair

Chr:

Chromosome

ERV:

Endogenous retrovirus

GSD:

Genetic sex determination

LINE (or SINE):

Long (or short) interspersed nuclear element

LG:

Linkage group

LTR:

Long terminal repeats

Mb (or kb):

Mega bases (or kilobases)

Myr:

Million years

nt:

Nucleotides

PAR:

Pseudo-autosomal regions

SD:

Sex determination

SNP:

Single nucleotide polymorphism

TEs:

Transposable elements

TIR:

Terminal inverted repeat

X SD region:

Sex-determining region of the X chromosome

Y SD region:

Sex-determining region of the Y chromosome

References

  • Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Amores A, Catchen J, Nanda I et al (2014) A RAD-Tag genetic map for the platyfish (Xiphophorus maculatus) reveals mechanisms of karyotype evolution among teleost fish. Genetics 197:625–641

    Article  PubMed Central  PubMed  Google Scholar 

  • Anderson JL, Rodriguez Mari A, Braasch I et al (2012) Multiple sex-associated regions and a putative sex chromosome in zebrafish revealed by RAD mapping and population genomics. PLoS One 7:e40701

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bachtrog D (2003) Adaptation shapes patterns of genome evolution on sexual and asexual chromosomes in Drosophila. Nat Genet 34:215–219

    Article  CAS  PubMed  Google Scholar 

  • Bachtrog D (2013) Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14:113–124

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bellott DW, Skaletsky H, Pyntikova T et al (2010) Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466:612–616

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bradley KM, Breyer JP, Melville DB et al (2011) An SNP-based linkage map for zebrafish reveals sex determination loci. G3 (Bethesda) 1:3–9

  • Britten RJ, Davidson EH (1971) Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q Rev Biol 46:111–138

    Article  CAS  PubMed  Google Scholar 

  • Chalopin D, Naville M, Plard F et al (2015) Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates. Genome Biol Evol 7:567–580

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Charlesworth B, Charlesworth D (2000) The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci 355:1563–1572

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity (Edinb) 95:118–128

    Article  CAS  Google Scholar 

  • Chaumeil J, Waters PD, Koina E et al (2011) Evolution from XIST-independent to XIST-controlled X-chromosome inactivation: epigenetic modifications in distantly related animals. PLoS One 6:19040

    Article  Google Scholar 

  • Chen S, Zhang G, Shao C et al (2014) Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 46:253–260

    Article  CAS  PubMed  Google Scholar 

  • Cioffi MB, Martins C, Bertollo LA (2009) Comparative chromosome mapping of repetitive sequences. Implications for genomic evolution in the fish, Hoplias malabaricus. BMC Genet 10:34, Erratum 14:24

    Article  PubMed Central  PubMed  Google Scholar 

  • Cioffi MB, Martins C, Bertollo LA (2010) Chromosome spreading of associated transposable elements and ribosomal DNA in the fish Erythrinus erythrinus. Implications for genome change and karyoevolution in fish. BMC Evol Biol 10:271

    Article  PubMed Central  PubMed  Google Scholar 

  • Cioffi MB, Kejnovsky E, Marquioni V et al (2012) The key role of repeated DNAs in sex chromosome evolution in two fish species with ZW sex chromosome system. Mol Cytogenet 5:28

    Article  CAS  Google Scholar 

  • Cocca E, Petraccioli A, Morescalchi MA et al (2015) Laser microdissection-based analysis of the Y sex chromosome of the Antarctic fish Chionodraco hamatus (Nothothenioidei Channichthyidae). Comp Cytogenet 9:1–15

    Article  PubMed Central  PubMed  Google Scholar 

  • Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364

    Article  CAS  Google Scholar 

  • Ellegren H, Hultin-Rosenberg L, Brunström B et al (2007) Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol 5:40

    Article  PubMed Central  PubMed  Google Scholar 

  • Ellegren H (2007) Molecular evolutionary genomics of birds. Cytogenet Genome Res 117:120–130

    Article  CAS  PubMed  Google Scholar 

  • Ellison CE, Bachtrog D (2013) Dosage compensation via transposable element mediated rewiring of a regulatory network. Science 342:846–850

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Faber-Hammond JJ, Phillips RB, Brown KH (2015) Comparative analysis of the shared sex-determination region (SDR) among salmonid fishes. Genome Biol Evol 7:1972–1987

  • Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397–405

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fischer C, Bouneau L, Coutanceau et al (2004) Global heterochromatic colocalization of transposable elements with ministallites in the compact genome pufferfish Tetraodon nigroviridis. Gene 336:175–183

    Article  CAS  PubMed  Google Scholar 

  • Fredga K (1988) Aberrant chromosomal sex-determining mechanisms in mammals, with special reference to species with XY females. Philos Trans R Soc Lond B Biol Sci 322:83–95

    Article  CAS  PubMed  Google Scholar 

  • Froschauer A, Korting C, Katagiri T (2002) Construction and initial analysis of bacterial artificial chromosome (BAC) contigs from the sex-determining region of the platyfish Xiphophorus maculatus. Gene 295:247–254

    Article  CAS  PubMed  Google Scholar 

  • Graves JA (2006) Sex chromosome specialization and degeneration in mammals. Cell 124:901–914

    Article  PubMed  Google Scholar 

  • Graves JA, Koina E, Sankovic N (2006) How the gene content of human sex chromosomes evolved. Curr Opin Genet Dev 16:219–224

    Article  PubMed  Google Scholar 

  • Gurbich TA, Bachtrog D (2008) Gene content evolution on the X chromosome. Curr Opin Genet Dev 18:493–498

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Herpin A, Braasch I, Kracussling M et al (2010) Transcriptional rewiring of the sex determining dmrt1 gene duplicate by transposable elements. PLoS Genet 6:e1000844

    Article  PubMed Central  PubMed  Google Scholar 

  • Hollister JD, Gaut BS (2009) Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 19:1419–1428

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hornung U, Herpin A, Schartl M (2007) Expression of the male determining gene dmrt1bY and its autosomal coorthologue dmrt1a in medaka. Sex Dev 1:197–206

    Article  CAS  PubMed  Google Scholar 

  • Howe K, Clark MD, Torroja CF et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hughes JF, Skaletsky H, Pyntikova T et al (2010) Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature 463:536–539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hughes JF, Skaletsky H, Brown LG (2012) Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes. Nature 483:82–86

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kallman KD, Schreibman MP (1973) A sex-linked gene controlling gonadotrop differentiation and its significance in determining the age of sexual maturation and size of the platyfish, Xiphophorus maculatus. Gen Comp Endocrinol 21:287–304

    Article  CAS  PubMed  Google Scholar 

  • Kamiya T, Kai W, Tasumi S et al (2012) A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (Fugu). PLoS Genet 8:e1002798

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kasahara M, Naruse K, Sasaki S (2007) The medaka draft genome and insights into vertebrate evolution. Nature 447:714–719

    Article  CAS  PubMed  Google Scholar 

  • Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed Central  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kitano J, Ross JA, Mori S et al (2009) A role for a neo-sex chromosome in stickleback speciation. Nature 461:1079–1083

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kondo M, Hornung U, Nanda I et al (2006) Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res 16:815–826

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lampert KP, Schmidt C, Fischer P et al (2010) Determination of onset of sexual maturation and mating behavior by melanocortin receptor 4 polymorphisms. Curr Biol 20:1729–1734

    Article  CAS  PubMed  Google Scholar 

  • Lee BY, Hulata G, Kocher TD (2004) Two unlinked loci controlling the sex of blue tilapia (Oreochromis aureus). Heredity (Edinb) 92:543–549

    Article  CAS  Google Scholar 

  • Lenormand T, Dutheil J (2005) Recombination difference between sexes: a role for haploid selection. PLoS Biol 3:e63

    Article  PubMed Central  PubMed  Google Scholar 

  • Lyon MF (2003) The Lyon and the LINE hypothesis. Semin Cell Dev Biol 14:313–318

    Article  CAS  PubMed  Google Scholar 

  • Mank JE, Ellegren H (2009) All dosage compensation is local: gene-by-gene regulation of sex-biased expression on the Z chicken chromosome. Heredity (Edinb) 102:312–320

    Article  CAS  Google Scholar 

  • Mank JE, Avise JC (2009) Evolutionary diversity and turn-over of sex determination in teleost fishes. Sex Dev 3:60–67

    Article  CAS  PubMed  Google Scholar 

  • Marshall Graves JA (2008) Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Annu Rev Genet 42:565–586

    Article  CAS  PubMed  Google Scholar 

  • Marshall Graves JA, Peichel CL (2010) Are homologies in vertebrate sex determination due to shared ancestry or to limited options? Genome Biol 11:205

    Article  PubMed Central  PubMed  Google Scholar 

  • Matsubara K, Tarui H, Toriba M et al (2006) Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci U S A 103:18190–18195

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Morgan T (1912) Complete linkage in the second chromosome of the male of Drosophila. Science 36:719–720

    Google Scholar 

  • Myosho T, Otake H, Masuyama H et al (2012) Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 191:163–170

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nagai Y, Ohno S (1977) Testis-determining H-Y antigen in XO males of the mole-vole (Ellobius lutescens). Cell 10:729–732

    Article  CAS  PubMed  Google Scholar 

  • Nanda I, Volff JN, Weis S et al (2000) Amplification of a long terminal repeat-like element on the Y chromosome of the platyfish, Xiphophorus maculatus. Chromosoma 109:173–180

    Article  CAS  PubMed  Google Scholar 

  • Nanda I, Kondo M, Hornung U et al (2002) A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci U S A 99:11778–11783

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nanda I, Schories S, Tripathi N et al (2014) Sex chromosome polymorphism in guppies. Chromosoma 123:373–383

    Article  CAS  PubMed  Google Scholar 

  • Peichel CL, Ross JA, Matson CK et al (2004) The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr Biol 14:1416–1424

    Article  CAS  PubMed  Google Scholar 

  • Poltronieri J, Marquioni V, Bertollo LA et al (2014) Comparative chromosomal mapping of microsatellites in Leporinus species (Characiformes, Anostomidae): unequal accumulation on the W chromosomes. Cytogenet Genome Res 142:40–45

    Article  CAS  PubMed  Google Scholar 

  • Schartl M (2004) Sex chromosome evolution in non-mammalian vertebrates. Curr Opin Genet Dev 14:634–641

    Article  CAS  PubMed  Google Scholar 

  • Schartl M, Walter RB, Shen Y et al (2013) The genome of the platyfish, Xiphophorus maculatus, provides insights into evolutionary adaptation and several complex traits. Nat Genet 45:567–572

    Article  CAS  PubMed  Google Scholar 

  • Shirak A, Seroussi E, Cnaani A et al (2006) Amh and Dmrta2 genes map to tilapia (Oreochromis spp.) linkage group 23 within quantitative trait locus regions for sex determination. Genetics 174:1573–1581

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Soh YQ, Alföldi J, Pyntikova T et al (2014) Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell 159:800–813

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Steinemann S, Steinemann M (2005) Y chromosomes: born to be destroyed. Bioessays 27:1076–1083

    Article  CAS  PubMed  Google Scholar 

  • Takeda H (2008) Draft genome of the medaka fish: a comprehensive resource for medaka developmental genetics and vertebrate evolutionary biology. Develop Growth Differ 50(Suppl 1):S157–S166

    Article  CAS  Google Scholar 

  • Takehana Y, Matsuda M, Myosho T et al (2014) Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena. Nat Commun 5:4157

    Article  CAS  PubMed  Google Scholar 

  • Terencio ML, Schneider CH, Gross MC et al (2012) Repetitive sequences associated with differentiation of W chromosome in Semaprochilodus taeniurus. Genetica 140:505–512

    Article  CAS  PubMed  Google Scholar 

  • Tripathi N, Hoffmann M, Weigel D et al (2009) Linkage analysis reveals the independent origin of Poeciliid sex chromosomes and a case of atypical sex inheritance in the guppy (Poecilia reticulata). Genetics 182:365–374

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Van Doorn GS, Kirkpatrick M (2010) Transitions between male and female heterogamety caused by sex-antagonistic selection. Genetics 186:629–645

    Article  PubMed Central  PubMed  Google Scholar 

  • Veyrunes F, Waters PD, Miethke P et al (2008) Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res 18:965–973

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vicoso B, Charlesworth B (2006) Evolution of the X chromosome: unusual patterns and processes. Nat Rev Genet 7:645–653

    Article  CAS  PubMed  Google Scholar 

  • Vicoso B, Emerson JJ, Zektser Y et al (2013) Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol 11:e1001643

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Volff JN, Schartl M (2001) Variability of genetic sex determination in poeciliid fishes. Genetica 111:101–110

    Article  CAS  PubMed  Google Scholar 

  • Volff JN, Schartl M (2002) Sex determination and sex chromosome evolution in the medaka, Oryzias latipes, and the platyfish, Xiphophorus maculatus. Cytogenet Genome Res 99:170–177

    Article  CAS  PubMed  Google Scholar 

  • Volff JN, Körting C, Froschauer A et al (2003) The Xmrk oncogene can escape nonfunctionalization in a highly unstable subtelomeric region of the genome of the fish Xiphophorus. Genomics 82:470–479

    Article  CAS  PubMed  Google Scholar 

  • Volff JN (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28:913–922

    Article  CAS  PubMed  Google Scholar 

  • Volff JN, Nanda I, Schmid M et al (2007) Governing sex determination in fish: regulatory putsches and ephemeral dictators. Sex Dev 1:85–99

    Article  PubMed  Google Scholar 

  • Volff JN, Selz Y, Hoffmann C et al (2013) Gene amplification and functional diversification of melanocortin 4 receptor at an extremely polymorphic locus controlling sexual maturation in the platyfish. Genetics 195:1337–1352

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • White MA, Kitano J, Peichel CL (2015) Purifying selection maintains dosage-sensitive genes during degeneration of the threespine stickleback Y chromosome. Mol Biol Evol

  • Wicker T, Sabot F, Hua-Van A et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982

    Article  CAS  PubMed  Google Scholar 

  • Wilson CA, McCluskey BM, Amores A et al (2014) Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains. Genetics 198:1291–1308

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshida K, Makino T, Yamaguchi K et al (2014) Sex chromosome turnover contributes to genomic divergence between incipient stickleback species. PLoS Genet 10:e1004223

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants to M.S. from the Deutsche Forschungsgemeinschaft (SCHA 408/12-1, SCHA 408/10-1), to JNV from the French Agence Nationale de la Recherche (ANR blanche seXYphophorus) and to JLA from the French Agence Nationale de la Recherche (ANR-13-ISV7-0005 PHYLOSEX). We also sincerely thank Minkyu Park for his computational help.

Conflict of interest

The authors declare that they have no competing interests.

Compliance with ethical standards

This article does not contain any studies with human or animal subjects performed by any of the authors.

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Author notes

  1. Domitille Chalopin

    Present address: Department of Genetics, University of Georgia, Athens, GA, USA

  2. Jennifer L. Anderson

    Present address: Department of Organismal Biology, Uppsala University, Uppsala, Sweden

Authors and Affiliations

  1. Institut de Génomique Fonctionnelle de Lyon, CNRS UMR5242, Ecole Normale Supérieure de Lyon, Lyon, France

    Domitille Chalopin, Jean-Nicolas Volff & Delphine Galiana

  2. INRA, Fish Physiology and Genomics (UR1037), Campus de Beaulieu, Rennes, France

    Jennifer L. Anderson

  3. Department Physiological Chemistry, Biozentrum, University of Wuerzburg, and Comprehensive Cancer Center Mainfranken, University Clinic Wuerzburg, Wuerzburg, Germany

    Manfred Schartl

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  1. Domitille Chalopin
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Correspondence to Manfred Schartl.

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Chalopin, D., Volff, JN., Galiana, D. et al. Transposable elements and early evolution of sex chromosomes in fish. Chromosome Res 23, 545–560 (2015). https://doi.org/10.1007/s10577-015-9490-8

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