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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

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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.

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The authors declare that they have no competing interests.

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

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Correspondence to Manfred Schartl.

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Responsible Editors: Maria Assunta Biscotti, Pat Heslop-Harrison and Ettore Olmo.

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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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