Hospodářská Monika, Mora Pablo, Voleníková Anna Chung, Al-Rikabi Ahmed, Altmanová Marie, Simanovsky Sergey A, Tolar Nikolas, Pavlica Tomáš, Janečková Karolína, Štundlová Jana, Bobryshava Kseniya, Jankásek Marek, Hiřman Matyáš, Liehr Thomas, Reichard Martin, Krysanov Eugene Yu, Ráb Petr, Englert Christoph, Nguyen Petr, Sember Alexandr
Laboratory of Fish Genetics, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Liběchov, Czech Republic.
University of South Bohemia, Faculty of Science, České Budějovice, Czech Republic.
Mol Ecol. 2025 Aug;34(16):e70029. doi: 10.1111/mec.70029. Epub 2025 Jul 24.
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 XXY systems in six other species, offer a valuable model to study sex chromosome turnovers. We characterised XXY 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 XXY 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.
性染色体在真核生物中反复进化。性决定（SD）位点的出现预计会逐渐限制重组，推动趋同的分子分化。然而，来自硬骨鱼类等类群的证据对这一模型提出了挑战，硬骨鱼类占脊椎动物物种的一半以上，其性决定系统具有无与伦比的多样性。硬骨鱼的性染色体通常很难检测到，因为它们经历频繁的更替，重置了分化过程。鳉鱼，包括弗氏鳉和卡氏鳉共有的XY系统以及其他六个物种的XXY系统，为研究性染色体更替提供了一个有价值的模型。我们对五个鳉鱼物种的XXY系统进行了特征分析，发现性染色体至少独立进化了四次。在布氏鳉和冈氏鳉中，性决定区域位于着丝粒附近或预测的染色体重排断点处，这表明重组冷点可能促进性染色体的进化。在弗氏鳉/卡氏鳉中代表XY系统的染色体在其外类群蒂氏底鳉中也是性连锁的，包括gdf6在内的几个基因位于分化区域。虽然冈氏鳉、卢氏鳉（均为沿海分支）和布氏鳉（卡拉哈里分支）的XXY系统涉及不同的染色体，但它们共享一个潜在的性决定区域。我们在冈氏鳉中发现了两个不同年龄的性连锁进化层。然而，其潜在的性决定基因amhr2位于较年轻的层中，因此不太可能是该谱系中的祖先性决定基因。我们的研究结果表明，重组格局塑造了性染色体的更替，并且某些同线性区段在鳉鱼中被反复选为性染色体。
