Origin and evolutionary trajectories of brown algal sex chromosomes

Research on the biology and evolution of sex chromosomes has primarily focused on diploid XX/XY and ZW/ZZ systems. In contrast, the rise, evolution and demise of U/V systems has remained an enigma. Here we analyse genomes of nine brown algal species with different sexual systems to determine the history of their sex determination. U/V sex chromosomes emerged between 450 and 224 million years ago, when a region containing the pivotal male-determinant MIN ceased recombining. Seven ancestral genes within the sex-determining region show remarkable conservation over this vast evolutionary time, although nested inversions caused expansions of the sex locus, independently in each lineage. We evaluate whether these expansions are associated with increased morphological complexity and sexual differentiation, and show that taxonomically restricted genes evolve unexpectedly often in U and V chromosomes. We also investigate two situations in which U/V-linked regions have changed. First, we demonstrate that convergent evolution of two monoicous species occurred by ancestral males acquiring U-specific genes. Second, the Fucus dioecious system involves new sex-determining gene(s), acting upstream of formerly V-specific genes during development. Both situations have led to the demise of U and V chromosomes and erosion of their specific genomic characteristics.

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Publication Details

Journal
Nature Ecology & Evolution
Published
2025-08-25
DOI
https://doi.org/10.1038/s41559-025-02838-w
Citations
8
Primary Topic
Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
Type
article
Field-Weighted Citation Impact
14.54

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article

Origin and evolutionary trajectories of brown algal sex chromosomes

Olivier Godfroy, Akira F. Peters, Guillaume Cossard, Rory J. Craig et al.
8 citations
Nature Ecology & Evolution
Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
14.54
article

Origin and evolutionary trajectories of brown algal sex chromosomes

Olivier Godfroy, Akira F. Peters, Guillaume Cossard, Rory J. Craig, Patrick Wincker, Svenja Heesch, Elena Avdievich, Josué Barrera‐Redondo, Gareth A. Pearson, Komlan Avia, Masakazu Hoshino, France Denœud, Zofia Nehr, Daniel Liesner, Loraine Brillet-Guéguen, Susana M. Coelho, Kenny A. Bogaert, Jeremy Mark Cock, Jean‐Marc Aury, Gonçalo Leiria, Agnieszka P. Lipinska, Fabian B. Haas, R. Luthringer, Erica Dinatale, Pengfei Liu, Galice Hoarau
article en
8 citations

Abstract

Research on the biology and evolution of sex chromosomes has primarily focused on diploid XX/XY and ZW/ZZ systems. In contrast, the rise, evolution and demise of U/V systems has remained an enigma. Here we analyse genomes of nine brown algal species with different sexual systems to determine the history of their sex determination. U/V sex chromosomes emerged between 450 and 224 million years ago, when a region containing the pivotal male-determinant MIN ceased recombining. Seven ancestral genes within the sex-determining region show remarkable conservation over this vast evolutionary time, although nested inversions caused expansions of the sex locus, independently in each lineage. We evaluate whether these expansions are associated with increased morphological complexity and sexual differentiation, and show that taxonomically restricted genes evolve unexpectedly often in U and V chromosomes. We also investigate two situations in which U/V-linked regions have changed. First, we demonstrate that convergent evolution of two monoicous species occurred by ancestral males acquiring U-specific genes. Second, the Fucus dioecious system involves new sex-determining gene(s), acting upstream of formerly V-specific genes during development. Both situations have led to the demise of U and V chromosomes and erosion of their specific genomic characteristics.

Nature Ecology & EvolutionVol. 9(11)
Centre National de la Recherche Scientifique (FR), Santen (Japan) (JP), Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR), Université Paris-Saclay (FR), Nord University (NO), Station Biologique de Roscoff (FR), Instituto Tecnológico Superior de Irapuato (MX), Sorbonne Université (FR), Laboratoire de Biologie Intégrative des Modèles Marins (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Génomique Métabolique du Genoscope (FR), Max Planck Institute for Developmental Biology (DE), Genoscope (FR), Santé de la Vigne et Qualité du Vin (FR), CEA Paris-Saclay (FR), Institut Français de la Vigne et du Vin (FR), Département Biologie et Amélioration des Plantes (FR), Max Planck Institute for Biology (DE), Centro de Ciências do Mar do Algarve, Instituto Politécnico Nacional (MX), Kobe University (JP), Université de Strasbourg (FR), University of Algarve (PT)
Gordon and Betty Moore Foundation, Alexander von Humboldt-Stiftung, Institut Français de Bioinformatique, Agence Nationale de la Recherche, Bundesministerium für Bildung und Forschung, Max-Planck-Gesellschaft, Centre National de la Recherche Scientifique, Région Bretagne, German Network for Bioinformatics Infrastructure, Sorbonne Université, Horizon 2020 Framework Programme, Japan Society for the Promotion of Science
Openalex Percentile: Top 1%
Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
14.54
DOIOpen Access PDFOpenAlex
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