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A bird’s white-eye view on neosex chromosome evolution

Thibault Leroy, Yoann Anselmetti, Marie-Ka Tilak, Sèverine Bérard, Laura Csukonyi, Maëva Gabrielli, Céline Scornavacca, Borja Milá, Christophe Thébaud, Benoit Nabholz
doi: https://doi.org/10.1101/505610
Thibault Leroy
1ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France
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Yoann Anselmetti
1ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France
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Marie-Ka Tilak
1ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France
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Sèverine Bérard
1ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France
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Laura Csukonyi
1ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France
2Laboratoire Evolution et Diversité Biologique (EDB), UMR 5174 CNRS – Université Paul Sabatier – IRD, Toulouse, France
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Maëva Gabrielli
2Laboratoire Evolution et Diversité Biologique (EDB), UMR 5174 CNRS – Université Paul Sabatier – IRD, Toulouse, France
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Céline Scornavacca
1ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France
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Borja Milá
3National Museum of Natural Sciences (MNCN), Spanish National Research Council (CSIC), Madrid, Spain
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Christophe Thébaud
2Laboratoire Evolution et Diversité Biologique (EDB), UMR 5174 CNRS – Université Paul Sabatier – IRD, Toulouse, France
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Benoit Nabholz
1ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France
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  • For correspondence: benoit.nabholz@umontpellier.fr
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ABSTRACT

Chromosomal organization is relatively stable among avian species, especially with regards to sex chromosomes. Members of the large Sylvioidea clade however have a pair of neo-sex chromosomes which is unique to this clade and originate from a parallel translocation of a region of the ancestral 4A chromosome on both W and Z chromosomes. Here, we took advantage of this unusual event to study the early stages of sex chromosome evolution. To do so, we sequenced a female (ZW) of two Sylvioidea species, a Zosterops borbonicus and a Z. pallidus. Then, we organized the Z. borbonicus scaffolds along chromosomes and annotated genes. Molecular phylogenetic dating under various methods and calibration sets confidently confirmed the recent diversification of the genus Zosterops (1-3.5 million years ago), thus representing one of the most exceptional rates of diversification among vertebrates. We then combined genomic coverage comparisons of five males and seven females, and homology with the zebra finch genome (Taeniopygia guttata) to identify sex chromosome scaffolds, as well as the candidate chromosome breakpoints for the two translocation events. We observed reduced levels of within-species diversity in both translocated regions and, as expected, even more so on the neoW chromosome. In order to compare the rates of molecular evolution in genomic regions of the autosomal-to-sex transitions, we then estimated the ratios of non-synonymous to synonymous polymorphisms (πN/πS) and substitutions (dN/dS). Based on both ratios, no or little contrast between autosomal and Z genes was observed, thus representing a very different outcome than the higher ratios observed at the neoW genes. In addition, we report significant changes in base composition content for translocated regions on the W and Z chromosomes and a large accumulation of transposable elements (TE) on the newly W region. Our results revealed contrasted signals of molecular evolution changes associated to these autosome-to-sex chromosome transitions, with congruent signals of a W chromosome degeneration yet a surprisingly weak support for a fast-Z effect.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 24, 2019.
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A bird’s white-eye view on neosex chromosome evolution
Thibault Leroy, Yoann Anselmetti, Marie-Ka Tilak, Sèverine Bérard, Laura Csukonyi, Maëva Gabrielli, Céline Scornavacca, Borja Milá, Christophe Thébaud, Benoit Nabholz
bioRxiv 505610; doi: https://doi.org/10.1101/505610
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A bird’s white-eye view on neosex chromosome evolution
Thibault Leroy, Yoann Anselmetti, Marie-Ka Tilak, Sèverine Bérard, Laura Csukonyi, Maëva Gabrielli, Céline Scornavacca, Borja Milá, Christophe Thébaud, Benoit Nabholz
bioRxiv 505610; doi: https://doi.org/10.1101/505610

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