Identification of the master sex determining gene in Northern pike (Esox lucius) reveals restricted sex chromosome differentiation

Teleost fishes, thanks to their rapid evolution of sex determination mechanisms, provide remarkable opportunities to study the formation of sex chromosomes and the mechanisms driving the birth of new master sex determining (MSD) genes. However, the evolutionary interplay between the sex chromosomes...

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Published inbioRxiv
Main Authors Pan, Qiaowei, Feron, Romain, Yano, Ayaka, Guyomard, Rene, Jouanno, Elodie, Vigouroux, Estelle, Wen, Ming, Jean-Mickael Busnel, Bobe, Julien, Jean-Paul Concordet, Parrinello, Hugues, Journot, Laurent, Klopp, Christophe, Lluch, Jerome, Roques, Celine, Postlethwait, John, Schartl, Manfred, Herpin, Amaury, Guiguen, Yann
Format Paper
LanguageEnglish
Published Cold Spring Harbor Cold Spring Harbor Laboratory Press 13.02.2019
Subjects
AMH gene
Chromosomes
Esox lucius
Fish
Gene duplication
Genes
Genomes
Nucleotide sequence
Recombination
Sex chromosomes
Sex determination
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Summary:Teleost fishes, thanks to their rapid evolution of sex determination mechanisms, provide remarkable opportunities to study the formation of sex chromosomes and the mechanisms driving the birth of new master sex determining (MSD) genes. However, the evolutionary interplay between the sex chromosomes and the MSD genes they harbor is rather unexplored. We characterized a male-specific duplicate of the anti-Müllerian hormone (amh) as the MSD gene in Northern Pike (Esox lucius), using genomic and expression evidences as well as by loss-of-function and gain-of-function experiments. Using RAD-Sequencing from a family panel, we identified Linkage Group (LG) 24 as the sex chromosome and positioned the sex locus in its sub-telomeric region. Furthermore, we demonstrated that this MSD originated from an ancient duplication of the autosomal amh gene, which was subsequently translocated to LG24. Using sex-specific pooled genome sequencing and a new male genome sequence assembled using Nanopore long reads, we also characterized the differentiation of the X and Y chromosomes, revealing a small male-specific insertion containing the MSD gene and a limited region with reduced recombination. Our study depicts an unexpected level of limited differentiation within a pair of sex chromosomes harboring an old MSD gene in a wild population of teleost fish, highlights the pivotal role of genes from the amh pathway in sex determination, as well as the importance of gene duplication as a mechanism driving the turnover of sex chromosomes in this clade.
DOI:10.1101/549527