Despite decades of cytogenetic and genomic research of dynamic sex chromosome evolution in teleost fishes, multiple sex chromosomes have been largely neglected. In this review, we compiled available data on teleost multiple sex chromosomes, identified major trends in their evolution and suggest further trajectories in their investigation. In a compiled dataset of 440 verified records of fish sex chromosomes, we counted 75 multiple sex chromosome systems with 60 estimated independent origins. We showed that male-heterogametic systems created by Y-autosome fusion predominate and that multiple sex chromosomes are over-represented in the order Perciformes. We documented a striking difference in patterns of differentiation of sex chromosomes between male and female heterogamety and hypothesize that faster W sex chromosome differentiation may constrain sex chromosome turnover in female-heterogametic systems. We also found no significant association between the mechanism of multiple sex chromosome formation and percentage of uni-armed chromosomes in teleost karyotypes. Last but not least, we hypothesized that interaction between fish populations, which differ in their sex chromosomes, can drive the evolution of multiple sex chromosomes in fishes. This underlines the importance of broader inter-population sampling in studies of fish sex chromosomes. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.

Departamento de Genética e Evolução Universidade Federal de São Carlos Rod Washington Luiz km 235 cep 13565 905 São Carlos Brazil

Department of Ecology Faculty of Science Charles University Viničná 7 128 44 Prague Czech Republic

Faculty of Science University of South Bohemia Branišovská 1760 370 05 České Budějovice Czech Republic

Laboratory of Fish Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences Rumburská 89 277 21 Liběchov Czech Republic

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The Tree of Sex consortium: a global initiative for studying the evolution of reproduction in eukaryotes

Multiple Origins of Sex Chromosomes in Nothobranchius Killifishes

Repetitive DNAs and differentiation of the ZZ/ZW sex chromosome system in the combtail fish Belontia hasselti (Perciformes: Osphronemidae)

Satellite DNAs and the evolution of the multiple X1X2Y sex chromosomes in the wolf fish Hoplias malabaricus (Teleostei; Characiformes)

Heteromorphic ZZ/ZW sex chromosomes sharing gene content with mammalian XX/XY are conserved in Madagascan chameleons of the genus Furcifer

Turnover of sex chromosomes in the Lake Tanganyika cichlid tribe Tropheini (Teleostei: Cichlidae)

Homeology of sex chromosomes in Amazonian Harttia armored catfishes supports the X-fission hypothesis for the X1X2Y sex chromosome system origin

Turnover of multiple sex chromosomes in Harttia catfish (Siluriformes, Loricariidae): a glimpse from whole chromosome painting

Madagascar Leaf-Tail Geckos (Uroplatus spp.) Share Independently Evolved Differentiated ZZ/ZW Sex Chromosomes

Adding New Pieces to the Puzzle of Karyotype Evolution in Harttia (Siluriformes, Loricariidae): Investigation of Amazonian Species

Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

Preface

A brief review of vertebrate sex evolution with a pledge for integrative research: towards 'sexomics'

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