Shaw Daniel E, Ross Wynter D, Lambert Alexis V, White Michael A
Department of Genetics, University of Georgia, Athens, Georgia, United States of America.
PLoS Genet. 2025 Sep 29;21(9):e1011875. doi: 10.1371/journal.pgen.1011875. eCollection 2025 Sep.
Sex chromosomes often evolve unique patterns of gene expression during spermatogenesis. In many species, sex-linked genes are downregulated during meiosis in response to asynapsis of the heterogametic sex chromosome pair (meiotic sex chromosome inactivation; MSCI). This process has evolved convergently across many taxa with independently derived sex chromosomes. Our understanding how quickly MSCI can evolve and whether it is connected to the degree of sequence degeneration remains limited. Teleost fish are a noteworthy group to investigate MSCI because sex chromosomes have evolved repeatedly across species, often over short evolutionary timescales. Here, we investigate whether MSCI occurs in the threespine stickleback fish (Gasterosteus aculeatus), which have an X and Y chromosome that evolved less than 26 million years ago. Using single-cell RNA-seq, we found that the X and Y chromosomes do not have a signature of MSCI, maintaining gene expression across meiosis. Using immunofluorescence, we also show the threespine stickleback do not form a condensed sex body around the X and Y, a feature of MSCI in many species. We did not see patterns of gene content evolution documented in other species with MSCI. Y-linked ampliconic gene families were expressed across multiple stages of spermatogenesis, rather than being restricted to post-meiotic stages, like in mammals. Our work shows MSCI does not occur in the threespine stickleback fish and has not shaped the evolution of the Y chromosome. In addition, the absence of MSCI in the threespine stickleback suggests this process may not be a conserved feature of teleost fish, despite overall sequence degeneration and structural evolution of the Y chromosome, and argues for additional investigation in other species. We also observed testis-dependent differences in coding and expression evolution for X-linked genes, revealing evidence of testis specific faster-X effect and gene-by-gene dosage compensation.
性染色体在精子发生过程中常常进化出独特的基因表达模式。在许多物种中，性连锁基因在减数分裂期间会因异配性别染色体对的联会异常而下调（减数分裂性染色体失活；MSCI）。这一过程在许多具有独立起源性染色体的分类群中趋同进化。我们对于MSCI进化的速度以及它是否与序列退化程度相关的理解仍然有限。硬骨鱼是研究MSCI的一个值得关注的类群，因为性染色体在物种间反复进化，通常是在较短的进化时间尺度上。在这里，我们研究MSCI是否发生在三刺鱼（Gasterosteus aculeatus）中，其X和Y染色体的进化时间不到2600万年。通过单细胞RNA测序，我们发现X和Y染色体没有MSCI的特征，在整个减数分裂过程中保持基因表达。利用免疫荧光，我们还表明三刺鱼不会在X和Y周围形成浓缩的性小体，而这是许多物种中MSCI的一个特征。我们没有看到在其他具有MSCI的物种中记录的基因含量进化模式。Y连锁扩增基因家族在精子发生的多个阶段都有表达，而不是像在哺乳动物中那样仅限于减数分裂后阶段。我们的研究表明，MSCI在三刺鱼中不会发生，并且没有塑造Y染色体的进化。此外，三刺鱼中不存在MSCI表明，尽管Y染色体存在整体序列退化和结构进化，但这一过程可能不是硬骨鱼的保守特征，这也支持在其他物种中进行进一步研究。我们还观察到X连锁基因在编码和表达进化中存在睾丸依赖性差异，揭示了睾丸特异性快X效应和逐基因剂量补偿的证据。
