Multiple Origins of Sex Chromosomes in <i>Nothobranchius</i> Killifishes

Sex chromosomes have evolved repeatedly across eukaryotes. The emergence of a sex-determining (SD) locus is expected to progressively restrict recombination, driving convergent molecular differentiation. However, evidence from taxa like teleost fishes, representing over half of vertebrate species with unmatched diversity in SD systems, challenges this model. Teleost sex chromosomes are often difficult to detect as they experience frequent turnovers, resetting the differentiation process. Nothobranchius killifishes, which include the XY system shared by N. furzeri and N. kadleci and X<sub>1</sub>X<sub>2</sub>Y systems in six other species, offer a valuable model to study sex chromosome turnovers. We characterised X<sub>1</sub>X<sub>2</sub>Y systems in five killifish species and found that sex chromosomes evolved at least four times independently. Sex-determining regions resided near centromeres or predicted chromosome rearrangement breakpoints in N. brieni and N. guentheri, suggesting recombination cold spots may facilitate sex chromosome evolution. Chromosomes representing the XY system in N. furzeri/N. kadleci were sex-linked also in the outgroup Fundulosoma thierryi, with several genes, including gdf6, residing in the region of differentiation. Although the X<sub>1</sub>X<sub>2</sub>Y systems of N. guentheri, N. lourensi (both Coastal clade), and N. brieni (Kalahari clade) involved different chromosomes, they shared a potential SD region. We uncovered two sex-linked evolutionary strata of distinct age in N. guentheri. However, its potential SD gene amhr2 was located in the younger stratum and is hence unlikely to be the ancestral SD gene in this lineage. Our findings suggest recombination landscapes shape sex chromosome turnover and that certain synteny blocks are repeatedly co-opted as sex chromosomes in killifishes.

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Journal
Molecular Ecology
Published
2025-07-24
DOI
https://doi.org/10.1111/mec.70029
Primary Topic
Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
Type
article
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article

Multiple Origins of Sex Chromosomes in Nothobranchius Killifishes

Jana Štundlová, Marie Altmanová, Petr Nguyen, Christoph Englert et al.
Molecular Ecology
Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
article

Multiple Origins of Sex Chromosomes in Nothobranchius Killifishes

Jana Štundlová, Marie Altmanová, Petr Nguyen, Christoph Englert, Matyáš Hiřman, Petr Ráb, Sergey A. Simanovsky, Thomas Liehr, Alexandr Sember, Pablo Mora, E. Yu. Krysanov, Tomáš Pavlica, Anna Voleníková, Marek Jankásek, Martin Reichard, Ahmed Al‐Rikabi, Monika Hospodářská, Kseniya Bobryshava, Nikolas Tolar, Karolína Janečková
article en

Abstract

Sex chromosomes have evolved repeatedly across eukaryotes. The emergence of a sex-determining (SD) locus is expected to progressively restrict recombination, driving convergent molecular differentiation. However, evidence from taxa like teleost fishes, representing over half of vertebrate species with unmatched diversity in SD systems, challenges this model. Teleost sex chromosomes are often difficult to detect as they experience frequent turnovers, resetting the differentiation process. Nothobranchius killifishes, which include the XY system shared by N. furzeri and N. kadleci and X<sub>1</sub>X<sub>2</sub>Y systems in six other species, offer a valuable model to study sex chromosome turnovers. We characterised X<sub>1</sub>X<sub>2</sub>Y systems in five killifish species and found that sex chromosomes evolved at least four times independently. Sex-determining regions resided near centromeres or predicted chromosome rearrangement breakpoints in N. brieni and N. guentheri, suggesting recombination cold spots may facilitate sex chromosome evolution. Chromosomes representing the XY system in N. furzeri/N. kadleci were sex-linked also in the outgroup Fundulosoma thierryi, with several genes, including gdf6, residing in the region of differentiation. Although the X<sub>1</sub>X<sub>2</sub>Y systems of N. guentheri, N. lourensi (both Coastal clade), and N. brieni (Kalahari clade) involved different chromosomes, they shared a potential SD region. We uncovered two sex-linked evolutionary strata of distinct age in N. guentheri. However, its potential SD gene amhr2 was located in the younger stratum and is hence unlikely to be the ancestral SD gene in this lineage. Our findings suggest recombination landscapes shape sex chromosome turnover and that certain synteny blocks are repeatedly co-opted as sex chromosomes in killifishes.

Molecular EcologyVol. 34(16)
Universidad de Jaén (ES), Czech Academy of Sciences (CZ), Charles University (CZ), Masaryk University (CZ), University of South Bohemia in České Budějovice (CZ), University of Łódź (PL), Czech Academy of Sciences, Institute of Animal Physiology and Genetics (CZ), Institute of Entomology (CZ), Leibniz Institute on Aging - Fritz Lipmann Institute (FLI) (DE), Jena University Hospital (DE), Czech Academy of Sciences, Institute of Vertebrate Biology (CZ), Severtsov Institute of Ecology and Evolution (RU), Czech Academy of Sciences, Institute of Computer Science (CZ), Czech Academy of Sciences, Biology Centre (CZ), Friedrich Schiller University Jena (DE)
Univerzita Karlova v Praze, Université de Moncton, Australian Government, European Commission, Ministerstvo Školství, Mládeže a Tělovýchovy, Grantová Agentura České Republiky, Akademie Věd České Republiky, Universidad de Jaén, Leibniz-Gemeinschaft
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Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
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