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

PLoS Genet. 2019 Aug 22;15(8):e1008013. doi: 10.1371/journal.pgen.1008013. eCollection 2019 Aug.

Abstract

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 evidence 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 reveals an unexpectedly low level of differentiation between a pair of sex chromosomes harboring an old MSD gene in a wild teleost fish population, and highlights both 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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Anti-Mullerian Hormone / genetics*
  • Chromosome Mapping
  • Esocidae / physiology*
  • Female
  • Gene Duplication
  • Gene Knockdown Techniques
  • Male
  • Phylogeny
  • Sex Chromosomes / genetics*
  • Sex Determination Processes / genetics*
  • Synteny

Substances

  • Anti-Mullerian Hormone

Grants and funding

This project was supported by funds from the “Agence Nationale de la Recherche” and the “Deutsche Forschungsgemeinschaft” (ANR/DFG, PhyloSex project, 2014-2016) to YG and MS. The GeT core facility (JL, CR), Toulouse, France and the MGX facility, Montpellier, France (LJ, HP) were supported by France Génomique National infrastructure, funded as part of “Investissement d’avenir” program managed by Agence Nationale pour la Recherche (contract ANR-10-INBS-09). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.