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 X1X2Y systems in six other species, offer a valuable model to study sex chromosome turnovers. We characterised X1X2Y 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 X1X2Y 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.

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Department of Ecology and Vertebrate Zoology University of Lodz Lodz Poland

Department of Ecology Faculty of Science Charles University Prague Czech Republic

Department of Experimental Biology Genetics Area University of Jaen Jaén Spain

Department of Genetics and Microbiology Faculty of Science Charles University Prague Czech Republic

Department of Zoology Faculty of Science Charles University Prague Czech Republic

Institute of Biochemistry and Biophysics Friedrich Schiller University Jena Jena Germany

Institute of Computer Science Masaryk University Brno Czech Republic

Institute of Entomology Biology Centre of the Czech Academy of Sciences České Budějovice Czech Republic

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic

Jena University Hospital Friedrich Schiller University Institute of Human Genetics Jena Germany

Laboratory of Fish Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences Liběchov Czech Republic

Leibniz Institute on Aging Fritz Lipmann Institute Jena Germany

Severtsov Institute of Ecology and Evolution Russian Academy of Sciences Moscow Russia

University of South Bohemia Faculty of Science České Budějovice Czech Republic

Zobrazit více v PubMed

Abbott, J. K. , Nordén A. K., and Hansson B.. 2017. “Sex Chromosome Evolution: Historical Insights and Future Perspectives.” Proceedings of the Royal Society B: Biological Sciences 284: 20162806. 10.1098/rspb.2016.2806. PubMed DOI PMC

Adolfi, M. C. , Herpin A., and Schartl M.. 2021. “The Replaceable Master of Sex Determination: Bottom‐Up Hypothesis Revisited.” Philosophical Transactions of the Royal Society B 376: 20200090. 10.1098/rstb.2020.0090. PubMed DOI PMC

Alonge, M. , Soyk S., Ramakrishnan S., et al. 2019. “RaGOO: Fast and Accurate Reference‐Guided Scaffolding of Draft Genomes.” Genome Biology 20: 224. 10.1186/s13059-019-1829-6. PubMed DOI PMC

Al‐Rikabi, A. , Liehr L. B., and Liehr T.. 2020. “Glass‐Needle Based Chromosome Microdissection—How to Set up Probes for Molecular Cytogenetics?” Video Journal of Clinical Research 2: 100004VAM08AR2020. 10.5348/100004VAM08AR2020TR. DOI

Andrews, S. 2010. “FastQC: A Quality Control Tool for High Throughput Sequence Data.” http://www.bioinformatics.babra ham.ac.uk/projects/fastqc/.

Bachtrog, D. , Mank J. E., Peichel C. L., et al. 2014. “Sex Determination: Why So Many Ways of Doing It?” PLoS Biology 12: e1001899. 10.1371/journal.pbio.1001899. PubMed DOI PMC

Bartáková, V. , Bryjová A., Polačik M., et al. 2025. “Phylogenomics and Population Genomics of PubMed DOI

Bartáková, V. , Reichard M., Blažek R., Polačik M., and Bryja J.. 2015. “Terrestrial Fishes: Rivers Are Barriers to Gene Flow in Annual Fishes From the African Savanna.” Journal of Biogeography 42: 1832–1844. 10.1111/jbi.12567. DOI

Bartáková, V. , Reichard M., Janko K., et al. 2013. “Strong Population Genetic Structuring in an Annual Fish, PubMed PMC

Bertollo, L. A. C. , Cioffi M. B., and Moreira‐Filho O.. 2015. “Direct Chromosome Preparation From Freshwater Teleost Fishes.” In Fish Cytogenetic Techniques Ray‐Fin Fishes and Chondrichthyans, edited by Ozouf‐Costaz C., Pisano E., Foresti F., and de Almeida‐Toledo L. F., 21–26. CRC Press, Inc. 10.1201/b18534-4. DOI

Blažek, R. , Polačik M., Kačer P., et al. 2017. “Repeated Intraspecific Divergence in Life Span and Aging of African Annual Fishes Along an Aridity Gradient.” Evolution 71: 386–402. 10.1111/evo.13127. PubMed DOI

Bolger, A. M. , Lohse M., and Usadel B.. 2014. “Trimmomatic: A Flexible Trimmer for Illumina Sequence Data.” Bioinformatics 30: 2114–2120. 10.1093/bioinformatics/btu170. PubMed DOI PMC

Brůna, T. , Hoff K. J., Lomsadze A., Stanke M., and Borodovsky M.. 2021. “BRAKER2: Automatic Eukaryotic Genome Annotation With GeneMark‐EP+ and AUGUSTUS Supported by a Protein Database.” NAR Genomics and Bioinformatics 3: lqaa108. 10.1093/nargab/lqaa108. PubMed DOI PMC

Camacho, C. , Coulouris G., Avagyan V., et al. 2009. “BLAST+: Architecture and Applications.” BMC Bioinformatics 10: 421. 10.1186/1471-2105-10-421. PubMed DOI PMC

Cellerino, A. , Valenzano D. R., and Reichard M.. 2016. “From the Bush to the Bench: The Annual PubMed DOI

Chan, P. P. , and Lowe T. M.. 2019. “tRNAscan‐SE: Searching for tRNA Genes in Genomic Sequences.” In Gene Prediction. Methods in Molecular Biology, edited by Kollmar M., vol. 1962, 1–14. Humana. 10.1007/978-1-4939-9173-0_1. PubMed DOI PMC

Charlesworth, D. 2021. “The Timing of Genetic Degeneration of Sex Chromosomes.” Philosophical Transactions of the Royal Society B 376: 20200093. 10.1098/rstb.2020.0093. PubMed DOI PMC

Charlesworth, D. , and Charlesworth B.. 1980. “Sex Differences in Fitness and Selection for Centric Fusions Between Sex‐Chromosomes and Autosomes.” Genetics Research 35: 205–214. 10.1017/S0016672300014051. PubMed DOI

Charlesworth, D. , Charlesworth B., and Marais G.. 2005. “Steps in the Evolution of Heteromorphic Sex Chromosomes.” Heredity 95: 118–128. 10.1038/sj.hdy.6800697. PubMed DOI

Cioffi, M. B. , Yano C. F., Sember A., and Bertollo L. A. C.. 2017. “Chromosomal Evolution in Lower Vertebrates: Sex Chromosomes in Neotropical Fishes.” Genes 8, no. 10: 258. 10.3390/genes8100258. PubMed DOI PMC

Cui, R. , Medeiros T., Willemsen D., et al. 2019. “Relaxed Selection Limits Lifespan by Increasing Mutation Load.” Cell 178: 385–399.e20. 10.1016/j.cell.2019.06.004. PubMed DOI

Danecek, P. , Bonfield J. K., Liddle J., et al. 2021. “Twelve Years of SAMtools and BCFtools.” GigaScience 10: giab008. 10.1093/gigascience/giab008. PubMed DOI PMC

Darolti, I. , Almeida P., Wright A. E., and Mank J. E.. 2022. “Comparison of Methodological Approaches to the Study of Young Sex Chromosomes: A Case Study in PubMed DOI PMC

De Coster, W. , D'Hert S., Schultz D. T., Cruts M., and Van Broeckhoven C.. 2018. “NanoPack: Visualizing and Processing Long‐Read Sequencing Data.” Bioinformatics 34: 2666–2669. 10.1093/bioinformatics/bty149. PubMed DOI PMC

de Moraes, R. L. , Sember A., Bertollo L. A. C., et al. 2019. “Comparative Cytogenetics and Neo‐Y Formation in Small‐Sized Fish Species of the Genus PubMed DOI PMC

Deon, G. A. , Glugoski L., Vicari M. R., et al. 2020. “Highly Rearranged Karyotypes and Multiple Sex Chromosome Systems in Armored Catfishes From the Genus PubMed DOI PMC

Dobin, A. , and Gingeras T. R.. 2015. “Mapping RNA‐Seq Reads With STAR.” Current Protocols in Bioinformatics 51: 11–14. 10.1002/0471250953.bi1114s51. PubMed DOI PMC

Dorn, A. , Musilová Z., Platzer M., Reichwald K., and Cellerino A.. 2014. “The Strange Case of East African Annual Fish: Aridification Correlates With Diversification for a Savannah Aquatic Group?” BMC Evolutionary Biology 14: 210. 10.1186/s12862-014-0210-3. PubMed DOI PMC

Edvardsen, R. B. , Wallerman O., Furmanek T., et al. 2022. “Heterochiasmy and the Establishment of PubMed DOI PMC

El Taher, A. , Ronco F., Matschiner M., Salzburger W., and Böhne A.. 2021. “Dynamics of Sex Chromosome Evolution in a Rapid Radiation of Cichlid Fishes.” Science Advances 7: eabe8215. 10.1126/sciadv.abe8215. PubMed DOI PMC

Ewulonu, U. V. , Haas R., and Turner B. J.. 1985. “A Multiple Sex Chromosome System in the Annual Killifish, DOI

Ferchaud, A.‐L. , Mérot C., Normandeau E., et al. 2022. “Chromosome‐Level Assembly Reveals a Putative Y‐Autosomal Fusion in the Sex Determination System of the Greenland Halibut ( PubMed DOI PMC

Feron, R. , and Jaron K. S.. 2021. SexGenomicsToolkit/PSASS: 3.1.0. Zenodo. 10.5281/zenodo.4442702. DOI

Feron, R. , Zahm M., Cabau C., et al. 2020. “Characterization of a Y‐Specific Duplication/Insertion of the Anti‐Mullerian Hormone Type II Receptor Gene Based on a Chromosome‐Scale Genome Assembly of Yellow Perch, PubMed DOI PMC

Filatov, D. A. 2024. “Evolution of a Plant Sex Chromosome Driven by Expanding Pericentromeric Recombination Suppression.” Scientific Reports 14: 1373. 10.1038/s41598-024-51153-0. PubMed DOI PMC

Flynn, J. M. , Hubley R., Goubert C., et al. 2020. “RepeatModeler2 for Automated Genomic Discovery of Transposable Element Families.” Proceedings of the National Academy of Sciences of the United States of America 117: 9451–9457. 10.1073/pnas.1921046117. PubMed DOI PMC

Fricke, R. , Eschmeyer W. N., and Van der Laan R.. 2025. “Eschmeyer's Catalog of Fishes: Genera, Species, References.” http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp.

Furness, A. I. 2016. “The Evolution of an Annual Life Cycle in Killifish: Adaptation to Ephemeral Aquatic Environments Through Embryonic Diapause.” Biological Reviews of the Cambridge Philosophical Society 91: 796–812. 10.1111/brv.12194. PubMed DOI

Garrison, E. , and Marth G.. 2012. “Haplotype‐Based Variant Detection From Short‐Read Sequencing (Version 2).” arXiv. 10.48550/ARXIV.1207.3907. DOI

Gil‐Fernández, A. , Saunders P. A., Martín‐Ruiz M., et al. 2020. “Meiosis Reveals the Early Steps in the Evolution of a Neo‐XY Sex Chromosome Pair in the African Pygmy Mouse PubMed DOI PMC

Guan, D. , McCarthy S. A., Wood J., Howe K., Wang Y., and Durbin R.. 2020. “Identifying and Removing Haplotypic Duplication in Primary Genome Assemblies.” Bioinformatics 36: 2896–2898. 10.1093/bioinformatics/btaa025. PubMed DOI PMC

Guiguen, Y. , Fostier A., and Herpin A.. 2018. “Sex Determination and Differentiation in Fish: Genetic, Genomic, and Endocrine Aspects.” In Sex Control in Aquaculture, edited by Wang H. P., Piferrer F., and Chen S.‐L., 1st ed., 35–63. John Wiley & Sons.

Haenel, Q. , Laurentino T. G., Roesti M., and Berner D.. 2018. “Meta‐Analysis of Chromosome‐Scale Crossover Rate Variation in Eukaryotes and Its Significance to Evolutionary Genomics.” Molecular Ecology 27: 2477–2497. 10.1111/mec.14699. PubMed DOI

Herpin, A. , and Schartl M.. 2015. “Plasticity of Gene‐Regulatory Networks Controlling Sex Determination: Of Masters, Slaves, Usual Suspects, Newcomers, and Usurpators.” EMBO Reports 16: 1260–1274. 10.15252/embr.201540667. PubMed DOI PMC

Herpin, A. , Schartl M., Depincé A., et al. 2021. “Allelic Diversification After Transposable Element Exaptation Promoted PubMed DOI PMC

Holley, G. , Beyter D., Ingimundardottir H., et al. 2021. “Ratatosk: Hybrid Error Correction of Long Reads Enables Accurate Variant Calling and Assembly.” Genome Biology 22: 28. 10.1186/s13059-020-02244-4. PubMed DOI PMC

Hospodářská, M. , Mora P., Voleníková A. C., et al. 2024. “Sex Chromosome Turnover in African Annual Killifishes of the Genus DOI

Hu, C. K. , and Brunet A.. 2018. “The African Turquoise Killifish: A Research Organism to Study Vertebrate Aging and Diapause.” Aging Cell 17: e12757. 10.1111/acel.12757. PubMed DOI PMC

Hu, J. , Fan J., Sun Z., and Liu S.. 2020. “NextPolish: A Fast and Efficient Genome Polishing Tool for Long‐Read Assembly.” Bioinformatics 36: 2253–2255. 10.1093/bioinformatics/btz891. PubMed DOI

Huang, Y. Q. , Zhang X. H., Bian C., et al. 2025. “Allelic Variation and Duplication of the PubMed DOI PMC

Humann, J. L. , Lee T., Ficklin S., and Main D.. 2019. “Structural and Functional Annotation of Eukaryotic Genomes With GenSAS.” In Gene Prediction. Methods in Molecular Biology, edited by Kollmar M., vol. 1962. Humana. 10.1007/978-1-4939-9173-0_3. PubMed DOI

Ieda, R. , Hosoya S., Tajima S., et al. 2018. “Identification of the Sex‐Determining Locus in Grass Puffer ( PubMed DOI PMC

Imarazene, B. , Du K., Beille S., et al. 2021. “A Supernumerary “B‐Sex” Chromosome Drives Male Sex Determination in the Pachón Cavefish, PubMed DOI PMC

Jay, P. , Jeffries D., Hartmann F. E., Véber A., and Giraud T.. 2024. “Why Do Sex Chromosomes Progressively Lose Recombination?” Trends in Genetics 40: 564–579. 10.1016/j.tig.2024.03.005. PubMed DOI

Killick, R. , and Eckley I. A.. 2014. “Changepoint: An R Package for Changepoint Analysis.” Journal of Statistical Software 58: 1–19. https://www.jstatsoft.org/article/view/v058i03.

Kitano, J. , Ansai S., Takehana Y., and Yamamoto Y.. 2024. “Diversity and Convergence of Sex Determination Mechanisms in Teleost Fish.” Annual Review of Animal Biosciences 12: 233–259. 10.1146/annurev-animal-021122-113935. PubMed DOI

Kitano, J. , and Peichel C. L.. 2012. “Turnover of Sex Chromosomes and Speciation in Fishes.” Environmental Biology of Fishes 94: 549–558. 10.1007/s10641-011-9853-8. PubMed DOI PMC

Kitano, J. , Ross J. A., Mori S., et al. 2009. “A Role for a Neo‐Sex Chromosome in Stickleback Speciation.” Nature 461: 1079–1083. 10.1038/nature08441. PubMed DOI PMC

Kligerman, A. D. , and Bloom S. E.. 1977. “Rapid Chromosome Preparations From Solid Tissues of Fishes.” Journal of the Fisheries Research Board of Canada 34: 266–269. 10.1139/f77-039. DOI

Kolmogorov, M. , Bickhart D. M., Behsaz B., et al. 2020. “metaFlye: Scalable Long‐Read Metagenome Assembly Using Repeat Graphs.” Nature Methods 17: 1103–1110. 10.1038/s41592-020-00971-x. PubMed DOI PMC

Kolmogorov, M. , Yuan J., Lin Y., and Pevzner P. A.. 2019. “Assembly of Long, Error‐Prone Reads Using Repeat Graphs.” Nature Biotechnology 37: 540–546. 10.1038/s41587-019-0072-8. PubMed DOI

Koren, S. , Walenz B. P., Berlin K., Miller J. R., Bergman N. H., and Phillippy A. M.. 2017. “Canu: Scalable and Accurate Long‐Read Assembly via Adaptive PubMed DOI PMC

Kratochvíl, L. , Stöck M., Rovatsos M., et al. 2021. “Expanding the Classical Paradigm: What We Have Learnt From Vertebrates About Sex Chromosome Evolution.” Philosophical Transactions of the Royal Society, B: Biological Sciences 376: 20200097. 10.1098/rstb.2020.0097. PubMed DOI PMC

Krueger, F. , James F., Ewels P., et al. 2023. “FelixKrueger/TrimGalore: V0.6.10—Add Default Decompression Path (0.6.10).” Zenodo. 10.5281/ZENODO.7598955. DOI

Krysanov, E. , and Demidova T.. 2018. “Extensive Karyotype Variability of African Fish Genus PubMed DOI PMC

Krysanov, E. , Demidova T., and Nagy B.. 2016. “Divergent Karyotypes of the Annual Killifish Genus PubMed DOI PMC

Krysanov, E. Y. , Nagy B., Watters B. R., Sember A., and Simanovsky S. A.. 2023. “Karyotype Differentiation in the PubMed DOI PMC

Kuhl, H. , Euclide P. T., Klopp C., et al. 2024. “Multi‐Genome Comparisons Reveal Gain‐And‐Loss Evolution of the Anti‐Mullerian Hormone Receptor Type 2 Gene as a Candidate Master Sex‐Determining Gene in Percidae.” BMC Biology 22: 141. 10.1186/s12915-024-01935-9. PubMed DOI PMC

Kuhl, H. , Guiguen Y., Höhne C., et al. 2021. “A 180 Myr‐Old Female‐Specific Genome Region in Sturgeon Reveals the Oldest Known Vertebrate Sex Determining System With Undifferentiated Sex Chromosomes.” Philosophical Transactions of the Royal Society, B: Biological Sciences 376: 20200089. PubMed PMC

Laetsch, D. R. , and Blaxter M. L.. 2017. “BlobTools: Interrogation of Genome Assemblies.” F1000Research 6: 1287. 10.12688/f1000research.12232.1. DOI

Lagesen, K. , Hallin P., Rødland E. A., Stærfeldt H.‐H., Rognes T., and Ussery D. W.. 2007. “RNAmmer: Consistent and Rapid Annotation of Ribosomal RNA Genes.” Nucleic Acids Research 35: 3100–3108. 10.1093/nar/gkm160. PubMed DOI PMC

Lahn, B. T. , and Page D. C.. 1999. “Four Evolutionary Strata on the Human X Chromosome.” Science 286: 964–967. 10.1126/science.286.5441.964. PubMed DOI

Langmead, B. , and Salzberg S. L.. 2012. “Fast Gapped‐Read Alignment With Bowtie 2.” Nature Methods 9: 357–359. 10.1038/nmeth.1923. PubMed DOI PMC

Levan, A. K. , Fredga K., and Sandberg A. A.. 1964. “Nomenclature for Centromeric Position on Chromosomes.” Hereditas 52: 201–220. 10.1111/j.1601-5223.1964.tb01953.x. DOI

Li, H. 2018. “Minimap2: Pairwise Alignment for Nucleotide Sequences.” Bioinformatics 34: 3094–3100. 10.1093/bioinformatics/bty191. PubMed DOI PMC

Li, H. , and Durbin R.. 2009. “Fast and Accurate Short Read Alignment With Burrows–Wheeler Transform.” Bioinformatics 25: 1754–1760. 10.1093/bioinformatics/btp324. PubMed DOI PMC

Li, H. , Handsaker B., Wysoker A., et al. 2009. “The Sequence Alignment/Map Format and SAMtools.” Bioinformatics 25: 2078–2079. 10.1093/bioinformatics/btp352. PubMed DOI PMC

Li, M. , Sun Y., Zhao J., et al. 2015. “A Tandem Duplicate of Anti‐Mülllerian Hormone With a Missense SNP on the Y Chromosome Is Essential for Male Sex Determination in Nile Tilapia, PubMed DOI PMC

Li, M. , Zhang R., Fan G., et al. 2021. “Reconstruction of the Origin of a Neo‐Y Sex Chromosome and Its Evolution in the Spotted Knifejaw, PubMed DOI PMC

Lichilín, N. , El Taher A., and Böhne A.. 2021. “Sex‐Biased Gene Expression and Recent Sex Chromosome Turnover.” Philosophical Transactions of the Royal Society B 376: 20200107. 10.1098/rstb.2020.0107. PubMed DOI PMC

Lisachov, A. , Tishakova K., Romanenko S., et al. 2023. “Robertsonian Fusion Triggers Recombination Suppression on Sex Chromosomes in PubMed DOI PMC

Lomsadze, A. , Burns P. D., and Borodovsky M.. 2014. “Integration of Mapped RNA‐Seq Reads Into Automatic Training of Eukaryotic Gene Finding Algorithm.” Nucleic Acids Research 42: e119. 10.1093/nar/gku557. PubMed DOI PMC

Lukšíková, K. , Pavlica T., Altmanová M., et al. 2023. “Conserved Satellite DNA Motif and Lack of Interstitial Telomeric Sites in Highly Rearranged African PubMed DOI

MacLeod‐Bigley, M. L. M. , and Boulding E. G.. 2023. “High‐Density Linkage Maps Detail Sex‐Specific Regions of Suppressed Recombination Near Fusions of Polymorphic Chromosomes in Purebred and Hybrid North American Atlantic Salmon ( PubMed DOI

Manni, M. , Berkeley M. R., Seppey M., Simão F. A., and Zdobnov E. M.. 2021. “BUSCO Update: Novel and Streamlined Workflows Along With Broader and Deeper Phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and Viral Genomes.” Molecular Biology and Evolution 38: 4647–4654. 10.1093/molbev/msab199. PubMed DOI PMC

Marçais, G. , and Kingsford C.. 2011. “A Fast, Lock‐Free Approach for Efficient Parallel Counting of Occurrences of PubMed DOI PMC

Martin, M. 2011. “Cutadapt Removes Adapter Sequences From High‐Throughput Sequencing Reads.” EMBnet J 17: 10–12. 10.14806/ej.17.1.200. DOI

Meisel, R. P. 2020. “Evolution of Sex Determination and Sex Chromosomes: A Novel Alternative Paradigm.” BioEssays 42: 1900212. 10.1002/bies.20200152. PubMed DOI

Miller, D. , and Hawley R.. 2017. “Meiotic Recombination: Taking the Path Less Traveled.” Current Biology 27: R19–R41. 10.1016/j.cub.2016.11.002. PubMed DOI

Mora, P. , Hospodářská M., Chung Voleníková A., et al. 2024. “Sex‐Biased Gene Content Is Associated With Sex Chromosome Turnover in Danaini Butterflies.” Molecular Ecology 33: e17256. 10.1111/mec.17256. PubMed DOI PMC

Morinaga, C. , Saito D., Nakamura S., et al. 2007. “The PubMed DOI PMC

Nagy, B. 2018. “

Nagy, B. , and Watters B. R.. 2022. “A Review of the Conservation Status of Seasonal DOI

Nakamoto, M. , Uchino T., Koshimizu E., et al. 2021. “A Y‐Linked Anti‐Müllerian Hormone Type‐II Receptor Is the Sex‐Determining Gene in Ayu, PubMed DOI PMC

Nakamura, S. , Watakabe I., Nishimura T., et al. 2012. “Hyperproliferation of Mitotically Active Germ Cells due to Defective Anti‐Mullerian Hormone Signaling Mediates Sex Reversal in Medaka.” Development (Cambridge, England) 139: 2283–2287. 10.1242/dev.076307. PubMed DOI

Nambiar, M. , and Smith G. R.. 2016. “Repression of Harmful Meiotic Recombination in Centromeric Regions.” Seminars in Cell & Developmental Biology 54: 188–197. 10.1016/j.semcdb.2016.01.042. PubMed DOI PMC

Nelson, J. S. , Grande T. C., and Wilson M. V. H.. 2016. Fishes of the World. 5th ed. John Wiley & Sons.

Novák, P. , Ávila Robledillo L., Koblížková A., Vrbová I., Neumann P., and Macas J.. 2017. “TAREAN: A Computational Tool for Identification and Characterization of Satellite DNA From Unassembled Short Reads.” Nucleic Acids Research 45: e111. 10.1093/nar/gkx257. PubMed DOI PMC

Pala, I. , Naurin S., Stervander M., Hasselquist D., Bensch S., and Hansson B.. 2012. “Evidence of a Neo‐Sex Chromosome in Birds.” Heredity 108: 264–272. 10.1038/hdy.2011.70. PubMed DOI PMC

Palmer, D. H. , Rogers T. F., Dean R., and Wright A. E.. 2019. “How to Identify Sex Chromosomes and Their Turnover.” Molecular Ecology 28: 4709–4724. 10.1111/mec.15245. PubMed DOI PMC

Pan, Q. , Kay T., Depincé A., et al. 2021. “Evolution of Master Sex Determiners: TGF‐β Signalling Pathways at Regulatory Crossroads.” Philosophical Transactions of the Royal Society B 376: 20200091. 10.1098/rstb.2020.0091. PubMed DOI PMC

Peichel, C. L. , McCann S. R., Ross J. A., et al. 2020. “Assembly of the Threespine Stickleback Y Chromosome Reveals Convergent Signatures of Sex Chromosome Evolution.” Genome Biology 21: 177. 10.1186/s13059-020-02097-x. PubMed DOI PMC

Pennell, M. W. , Kirkpatrick M., Otto S. P., et al. 2015. “Y Fuse? Sex Chromosome Fusions in Fishes and Reptiles.” PLoS Genetics 11: e1005237. 10.1371/journal.pgen.1005237. PubMed DOI PMC

Petzold, A. , Reichwald K., Groth M., et al. 2013. “The Transcript Catalogue of the Short‐Lived Fish PubMed DOI PMC

Ponnikas, S. , Sigeman H., Abbott J. K., and Hansson B.. 2018. “Why Do Sex Chromosomes Stop Recombining?” Trends in Genetics 34: 492–503. 10.1016/j.tig.2018.04.001. PubMed DOI

Pospíšilová, K. , Van't Hof A. E., Yoshido A., et al. 2023. “ PubMed DOI

Qu, M. , Liu Y., Zhang Y., et al. 2021. “Seadragon Genome Analysis Provides Insights Into Its Phenotype and Sex Determination Locus.” Science Advances 7: eabg5196. 10.1126/sciadv.abg5196. PubMed DOI PMC

Quinlan, A. R. , and Hall I. M.. 2010. “BEDTools: A Flexible Suite of Utilities for Comparing Genomic Features.” Bioinformatics 26: 841–842. 10.1093/bioinformatics/btq033. PubMed DOI PMC

Ráb, P. , and Roth P.. 1988. “Cold‐Blooded Vertebrates.” In Methods of Chromosome Analysis, edited by Balicek P., Forejt J., and Rubeš J., 115–124. Cytogenetická Sekce Československé Biologické Společnosti při CSAV.

Ranallo‐Benavidez, T. R. , Jaron K. S., and Schatz M. C.. 2020. “GenomeScope 2.0 and Smudgeplot for Reference‐Free Profiling of Polyploid Genomes.” Nature Communications 11: 1432. 10.1038/s41467-020-14998-3. PubMed DOI PMC

Reichwald, K. , Lauber C., Nanda I., et al. 2009. “High Tandem Repeat Content in the Genome of the Short‐Lived Annual Fish PubMed DOI PMC

Reichwald, K. , Petzold A., Koch P., et al. 2015. “Insights Into Sex Chromosome Evolution and Aging From the Genome of a Short‐Lived Fish.” Cell 163: 1527–1538. 10.1016/j.cell.2015.10.071. PubMed DOI

Richter, A. , Mörl H., Thielemann M., et al. 2025. “The Master Male Sex Determinant Gdf6Y of the Turquoise Killifish Arose Through Allelic Neofunctionalization.” Nature Communications 16, no. 1: 540. 10.1038/s41467-025-55899-7. PubMed DOI PMC

Sahara, K. , Marec F., and Traut W.. 1999. “TTAGG Telomeric Repeats in Chromosomes of Some Insects and Other Arthropods.” Chromosome Research 7: 449–460. 10.1023/A:1009297729547. PubMed DOI

Sakamoto, Y. , and Zacaro A. A.. 2009. LEVAN, an ImageJ Plugin for Morphological Cytogenetic Analysis of Mitotic and Meiotic Chromosomes. https://imagej.net/ij/.

Sardell, J. M. , Josephson M. P., Dalziel A. C., Peichel C. L., and Kirkpatrick M.. 2021. “Heterogeneous Histories of Recombination Suppression on Stickleback Sex Chromosomes.” Molecular Biology and Evolution 38: 4403–4418. 10.1093/molbev/msab179. PubMed DOI PMC

Sardell, J. M. , and Kirkpatrick M.. 2020. “Sex Differences in the Recombination Landscape.” American Naturalist 195: 361–379. 10.1086/704943. PubMed DOI PMC

Saunders, P. A. 2019. “Sex Chromosome Turnovers in Evolution.” In: eLS. 10.1002/9780470015902.a0028747. DOI

Saunders, P. A. , and Muyle A.. 2024. “Sex Chromosome Evolution: Hallmarks and Question Marks.” Molecular Biology and Evolution 41: msae218. 10.1093/molbev/msae218. PubMed DOI PMC

Sember, A. , Bohlen J., Šlechtová V., Altmanová M., Symonová R., and Ráb P.. 2015. “Karyotype Differentiation in 19 Species of River Loach Fishes (Nemacheilidae, Teleostei): Extensive Variability Associated With rDNA and Heterochromatin Distribution and Its Phylogenetic and Ecological Interpretation.” BMC Evolutionary Biology 15: 251. 10.1186/s12862-015-0532-9. PubMed DOI PMC

Sember, A. , Nguyen P., Perez M. F., Altmanová M., Ráb P., and Cioffi M. B.. 2021. “Multiple Sex Chromosomes in Teleost Fishes From a Cytogenetic Perspective: State of the Art and Future Challenges.” Philosophical Transactions of the Royal Society, B: Biological Sciences 376: 20200098. 10.1098/rstb.2020.0098. PubMed DOI PMC

Shen, G. , and Wang P.. 2019. “Environmental Sex Determination and Sex Differentiation in Teleosts—How Sex Is Established.” In Sex control in aquaculture, edited by Wang H.‐P., Piferrer F., and Chen S.‐L., 1st ed., 85–116. John Wiley & Sons.

Sigeman, H. , Ponnikas S., Chauhan P., Dierickx E., de Brooke M. L., and Hansson B.. 2019. “Repeated Sex Chromosome Evolution Invertebrates Supported by Expanded Avian Sexchromosomes.” Proceedings of the Royal Society B: Biological Sciences 286: 20192051. 10.1098/rspb.2019.2051. PubMed DOI PMC

Simanovsky, S. A. , Demidova T. B., Spangenberg V. E., et al. 2019. “Multiple Sex Chromosome System X DOI

Smit, A. F. , and Hubley R.. 2008‐2015. “RepeatModeler‐1.0.” http://www.repeatmasker.org.

Smit, A. F. A. , Hubley R., and Green P.. 2013‐2015. “RepeatMasker Open‐4.0.” http://www.repeatmasker.org.

Smith, S. H. , Hsiung K., and Böhne A.. 2023. “Evaluating the Role of Sexual Antagonism in the Evolution of Sex Chromosomes: New Data From Fish.” Current Opinion in Genetics & Development 81: 102078. 10.1016/j.gde.2023.102078. PubMed DOI

Stanke, M. , and Morgenstern B.. 2005. “AUGUSTUS: A Web Server for Gene Prediction in Eukaryotes That Allows User‐Defined Constraints.” Nucleic Acids Research 33: W465–W467. 10.1093/nar/gki458. PubMed DOI PMC

Štundlová, J. , Hospodářská M., Lukšíková K., et al. 2022. “Sex Chromosome Differentiation via Changes in the Y Chromosome Repeat Landscape in African Annual Killifishes PubMed DOI

Sykes, N. T. , Kolora S. R. R., Sudmant P. H., and Owens G. L.. 2023. “Rapid Turnover and Evolution of Sex‐Determining Regions in PubMed DOI

Takehana, Y. , Matsuda M., Myosho T., et al. 2014. “Co‐Option of PubMed DOI

Toups, M. A. , Rodrigues N., Perrin N., and Kirkpatrick M.. 2019. “A Reciprocal Translocation Radically Reshapes Sex‐Linked Inheritance in the Common Frog.” Molecular Ecology 28: 1877–1889. 10.1111/mec.14990. PubMed DOI PMC

van der Merwe, P. D. W. , Cotterill F. P. D., Kandziora M., et al. 2021. “Genomic Fingerprints of Palaeogeographic History: The Tempo and Mode of Rift Tectonics Across Tropical Africa Has Shaped the Diversification of the Killifish Genus PubMed DOI

Vara, C. , Paytuví‐Gallart A., Cuartero Y., et al. 2021. “The Impact of Chromosomal Fusions on 3D Genome Folding and Recombination in the Germ Line.” Nature Communications 12: 2981. 10.1038/s41467-021-23270-1. PubMed DOI PMC

Vicoso, B. 2019. “Molecular and Evolutionary Dynamics of Animal Sex‐Chromosome Turnover.” Nature Ecology & Evolution 3: 1632–1641. 10.1038/s41559-019-1050-8. PubMed DOI

Voleníková, A. , Lukšíková K., Mora P., et al. 2023. “Fast Satellite DNA Evolution in PubMed DOI PMC

Völker, M. , and Ráb P.. 2015. “Direct Chromosome Preparation From Regenerating Fin Tissue.” In Fish Cytogenetic Techniques Ray‐Fin Fishes and Chondrichthyans, edited by Ozouf‐Costaz C., Pisano E., Foresti F., and de Almeida‐Toledo L. F., 37–41. CRC Press, Inc. 10.1201/b18534-4. DOI

Vrtílek, M. , Žák J., Pšenička M., and Reichard M.. 2018. “Extremely Rapid Maturation of a Wild African Annual Fish.” Current Biology 28: R822–R824. 10.1016/j.cub.2018.06.031. PubMed DOI

Wang, J. , Tao W., Kocher T. D., and Wang D.. 2024. “Sex Chromosome Turnover and Biodiversity in Fishes.” Journal of Genetics and Genomics 51: 1351–1360. 10.1016/j.jgg.2024.08.008. PubMed DOI

Wen, M. , Pan Q., Jouanno E., et al. 2022. “An Ancient Truncated Duplication of the Anti‐Müllerian Hormone Receptor Type 2 Gene Is a Potential Conserved Master Sex Determinant in the Pangasiidae Catfish Family.” Molecular Ecology Resources 22: 2411–2428. 10.1111/1755-0998.13620. PubMed DOI PMC

Wildekamp, R. H. 1996. A World of Killies. Atlas of the Oviparous Cyprinodontiform Fishes of the World. Vol. III, 330. American Killifish Association.

Wildekamp, R. H. 2004. A World of Killies—Atlas of the Oviparous Cyprinodontiform Fishes of the World. Vol. IV, 398. American Killifish Association.

Willemsen, D. , Cui R., Reichard M., and Valenzano D. R.. 2020. “Intra‐Species Differences in Population Size Shape Life History and Genome Evolution.” eLife 9: e55794. 10.7554/eLife.55794. PubMed DOI PMC

Wright, A. E. , Dean R., Zimmer F., and Mank J. E.. 2016. “How to Make a Sex Chromosome.” Nature Communications 7: 12087. 10.1038/ncomms12087. PubMed DOI PMC

Xu, L. , Ren Y., Wu J., et al. 2024. “Evolution and Expression Patterns of the Neo‐Sex Chromosomes of the Crested Ibis.” Nature Communications 15: 1670. 10.1038/s41467-024-46052-x. PubMed DOI PMC

Yang, F. , Trifonov V., Ng B. L., Kosyakova N., and Carter N. P.. 2009. Generation of Paint Probes by Flowsorted and Microdissected Chromosomes. Fluorescence in Situ Hybridization (FISH)—Application Guide, edited by Liehr T., 2nd ed., 35–52. Springer.

Yano, C. F. , Bertollo L. A. C., Ezaz T., et al. 2017. “Highly Conserved Z and Molecularly Diverged W Chromosomes in the Fish Genus PubMed DOI PMC

Yoshida, K. , Rödelsperger C., Röseler W., et al. 2023. “Chromosome Fusions Repatterned Recombination Rate and Facilitated Reproductive Isolation During PubMed DOI PMC

Yoshido, A. , Sahara K., and Yasukochi Y.. 2015. “Silk Moths (Lepidoptera).” In Protocols for Cytogenetic Mapping of Arthropod Genomes, edited by Sharakhov I. V., 219–256. CRC Press.

Zhou, Q. , Zhang J., Bachtrog D., et al. 2014. “Complex Evolutionary Trajectories of Sex Chromosomes Across Bird Taxa.” Science 346: 1246338. 10.1126/science.1246338. PubMed DOI PMC