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Chromosome Research

, Volume 23, Issue 3, pp 545–560 | Cite as

Transposable elements and early evolution of sex chromosomes in fish

  • Domitille Chalopin
  • Jean-Nicolas Volff
  • Delphine Galiana
  • Jennifer L. Anderson
  • Manfred SchartlEmail author
Original Article

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.

Keywords

Sex chromosomes Transposable elements Fish 

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

Notes

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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Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Domitille Chalopin
    • 1
    • 2
  • Jean-Nicolas Volff
    • 1
  • Delphine Galiana
    • 1
  • Jennifer L. Anderson
    • 3
    • 4
  • Manfred Schartl
    • 5
    Email author
  1. 1.Institut de Génomique Fonctionnelle de Lyon, CNRS UMR5242Ecole Normale Supérieure de LyonLyonFrance
  2. 2.Department of GeneticsUniversity of GeorgiaAthensUSA
  3. 3.INRA, Fish Physiology and Genomics (UR1037)RennesFrance
  4. 4.Department of Organismal BiologyUppsala UniversityUppsalaSweden
  5. 5.Department Physiological Chemistry, BiozentrumUniversity of Wuerzburg, and Comprehensive Cancer Center Mainfranken, University Clinic WuerzburgWuerzburgGermany

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