Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics

A bird’s white-eye view on avian sex chromosome evolution

Leroy, Thibault1 ; Anselmetti, Yoann1 ; Tilak, Marie-Ka1 ; Bérard, Sèverine1 ; Csukonyi, Laura1, 2; Gabrielli, Maëva2 ; Scornavacca, Céline1; Milá, Borja3 ; Thébaud, Christophe2 ; Nabholz, Benoit1  
1 ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France
2 Laboratoire Evolution et Diversité Biologique (EDB), UMR 5174 CNRS – Université Paul Sabatier – IRD, Toulouse, France
3 National Museum of Natural Sciences (MNCN), Spanish National Research Council (CSIC), Madrid, Spain

Corresponding author(s): Nabholz, Benoit (benoit.nabholz@umontpellier.fr)

10.24072/pcjournal.70 - Peer Community Journal, Volume 1 (2021), article no. e63.

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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 (N/S) 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 transitions, with congruent signals of a W chromosome degeneration yet a surprisingly weak support for a fast-Z effect.

Published online:
DOI: 10.24072/pcjournal.70
Type: Research article

Leroy, Thibault 1; Anselmetti, Yoann 1; Tilak, Marie-Ka 1; Bérard, Sèverine 1; Csukonyi, Laura 1, 2; Gabrielli, Maëva 2; Scornavacca, Céline 1; Milá, Borja 3; Thébaud, Christophe 2; Nabholz, Benoit 1

1 ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France
2 Laboratoire Evolution et Diversité Biologique (EDB), UMR 5174 CNRS – Université Paul Sabatier – IRD, Toulouse, France
3 National Museum of Natural Sciences (MNCN), Spanish National Research Council (CSIC), Madrid, Spain
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_70,
     author = {Leroy, Thibault and Anselmetti, Yoann and Tilak, Marie-Ka and B\'erard, S\`everine and Csukonyi, Laura and Gabrielli, Ma\"eva and Scornavacca, C\'eline and Mil\'a, Borja and Th\'ebaud, Christophe and Nabholz, Benoit},
     title = {A bird{\textquoteright}s white-eye view on avian sex chromosome evolution},
     journal = {Peer Community Journal},
     eid = {e63},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.70},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.70/}
}
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%A Anselmetti, Yoann
%A Tilak, Marie-Ka
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%A Gabrielli, Maëva
%A Scornavacca, Céline
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Leroy, Thibault; Anselmetti, Yoann; Tilak, Marie-Ka; Bérard, Sèverine; Csukonyi, Laura; Gabrielli, Maëva; Scornavacca, Céline; Milá, Borja; Thébaud, Christophe; Nabholz, Benoit. A bird’s white-eye view on avian sex chromosome evolution. Peer Community Journal, Volume 1 (2021), article  no. e63. doi : 10.24072/pcjournal.70. https://peercommunityjournal.org/articles/10.24072/pcjournal.70/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100073

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

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