Journal Article

Massive expansion of sex-specific SNPs, transposon-related elements, and neocentromere formation shape the young W-chromosome from the mosquitofish Gambusia affinis

Guiguen, Yann, Müller, Stefan, University of New South Wales [Sydney] (UNSW), Ludwig-Maximilians University [Munich] (LMU), Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Stöck, Matthias, Universität Innsbruck [Innsbruck] = University of Innsbruck, Pichler, Maria, Laboratoire de Physiologie et Génomique des Poissons = Fish Physiology and Genomics Institute (LPGP) ; Structure Fédérative de Recherche en Biologie et Santé de Rennes (Biosit : Biologie - Santé - Innovation Technologique)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Lamatsch, Dunja, K, Julius-Maximilians-Universität Würzburg = University of Würzburg [Würsburg, Germany] (JMU), Du, Kang, Texas State University, Schartl, Manfred, Hiroshima University (HU), Nakagawa, Shinichi

2023

Overview

Background The Western mosquitofish, Gambusia affinis, is a model for sex chromosome organization and evolution of female heterogamety. We previously identified a G. affinis female-specific marker, orthologous to the aminomethyl transferase (amt) gene of the related platyfish (Xiphophorus maculatus). Here, we have analyzed the structure and differentiation of the G. affinis W-chromosome, using a cytogenomics and bioinformatics approach. Results The long arm of the G. affinis W-chromosome (Wq) is highly enriched in dispersed repetitive sequences, but neither heterochromatic nor epigenetically silenced by hypermethylation. In line with this, Wq sequences are highly transcribed, including an active nucleolus organizing region (NOR). Female-specific SNPs and evolutionary young transposable elements were highly enriched and dispersed along the W-chromosome long arm, suggesting constrained recombination. Wq copy number expanded elements also include female-specific transcribed sequences from the amt locus with homology to TE. Collectively, the G. affinis W-chromosome is actively differentiating by sexspecific copy number expansion of transcribed TE-related elements, but not (yet) by extensive sequence divergence or gene decay. Conclusions The G. affinis W-chromosome exhibits characteristic genomic properties of an evolutionary young sex chromosome. Strikingly, the observed sex-specific changes in the genomic landscape are confined to the W long arm, which is separated from the rest of the W-chromosome by a neocentromere acquired during sex chromosome evolution and may thus have become functionally insulated. In contrast, W short arm sequences were apparently shielded from repeat-driven differentiation, retained Z-chromosome like genomic features, and may have preserved pseudoautosomal properties.

• Publisher: CCSD,BioMed Central,Springer Science and Business Media LLC,BioMed Central Ltd,Springer Nature B.V,BMC
• Subject: [SDV]Life Sciences [q-bio] / Analysis / Animals / Bioinformatics / Biology (General) / Biomedical and Life Sciences / Chromosomes / Copy number / Cyprinodontiformes / Cyprinodontiformes - genetics / Differentiation / Dispersion / Divergence / DNA Transposable Elements / DNA Transposable Elements - genetics / Evolution / Evolution, Molecular / Female / Females / Fish / Gambusia affinis / Genes / Genetic aspects / Genetic research / Genomes / Genomics / Homology / Hybridization / Life Sciences / Male / Males / Neocentromere / Nucleoli / Poeciliidae / Polymorphism, Single Nucleotide / QH301-705.5 / Recombination / Reptiles & amphibians / Research Article / Sequences / Sex / Sex chromosome evolution / Sex Chromosomes / Sex Chromosomes - genetics / Single nucleotide polymorphisms / Single-nucleotide polymorphism / SNP accumulation / Transposable element / Transposons / W-specific non-coding gonadal expression / ZZ/ZW sex chromosomes
• ISBN: 0009890603000