Homomorphic sex chromosomes and their turnover are common in teleosts. We investigated the evolution of nascent sex chromosomes in several populations of two sister species of African annual killifishes, Nothobranchius furzeri and N. kadleci, focusing on their under-studied repetitive landscape. We combined bioinformatic analyses of the repeatome with molecular cytogenetic techniques, including comparative genomic hybridization, fluorescence in situ hybridization with satellite sequences, ribosomal RNA genes (rDNA) and bacterial artificial chromosomes (BACs), and immunostaining of SYCP3 and MLH1 proteins to mark lateral elements of synaptonemal complexes and recombination sites, respectively. Both species share the same heteromorphic XY sex chromosome system, which thus evolved prior to their divergence. This was corroborated by sequence analysis of a putative master sex determining (MSD) gene gdf6Y in both species. Based on their divergence, differentiation of the XY sex chromosome pair started approximately 2 million years ago. In all populations, the gdf6Y gene mapped within a region rich in satellite DNA on the Y chromosome long arms. Despite their heteromorphism, X and Y chromosomes mostly pair regularly in meiosis, implying synaptic adjustment. In N. kadleci, Y-linked paracentric inversions like those previously reported in N. furzeri were detected. An inversion involving the MSD gene may suppress occasional recombination in the region, which we otherwise evidenced in the N. furzeri population MZCS-121 of the Limpopo clade lacking this inversion. Y chromosome centromeric repeats were reduced compared with the X chromosome and autosomes, which points to a role of relaxed meiotic drive in shaping the Y chromosome repeat landscape. We speculate that the recombination rate between sex chromosomes was reduced due to heterochiasmy. The observed differences between the repeat accumulations on the X and Y chromosomes probably result from high repeat turnover and may not relate closely to the divergence inferred from earlier SNP analyses.

Biology Centre of the Czech Academy of Sciences Institute of Entomology Ceske Budejovice Czech Republic

Department of Botany and Zoology Masaryk University Brno Czech Republic

Department of Ecology and Vertebrate Zoology University of Łódź Lodz Poland

Department of Ecology Faculty of Science Charles University Prague Czech Republic

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

Department of Zoology Faculty of Science Charles University Prague Czech Republic

Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic

Institute of Biochemistry and Biophysics Friedrich Schiller University Jena Jena Germany

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic

Institute of Zoology Chisinau Moldova

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

Leibniz Institute on Aging Fritz Lipmann Institute Jena Germany

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

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Advances in Understanding the Karyotype Evolution of Tetrapulmonata and Two Other Arachnid Taxa, Ricinulei and Solifugae

Comparative cytogenetics of three Zoraptera species as a basis for understanding chromosomal evolution in Polyneoptera insects

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

Fast satellite DNA evolution in Nothobranchius annual killifishes

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

Karyotype differentiation in the Nothobranchiusugandensis species group (Teleostei, Cyprinodontiformes), seasonal fishes from the east African inland plateau, in the context of phylogeny and biogeography