Price Peter D, Parkus Sylvie M, Lloyd Victoria J, Alston Ben T, Bradshaw Sasha L, Bates Sadé, Hughes Margaret A, Paterson Steve, Burke Terry, Darolti Iulia, Pomiankowski Andrew, Wright Alison E
Ecology and Evolutionary Biology, School of Biosciences, University of Sheffield, Sheffield, United Kingdom.
Department of Genetics, Evolution and Environment, University College London, London, United Kingdom.
PLoS Genet. 2025 Sep 18;21(9):e1011816. doi: 10.1371/journal.pgen.1011816. eCollection 2025 Sep.
Sex-linked meiotic drivers limit the inheritance of the alternate sex chromosome in the heterogametic sex, subsequently skewing the offspring sex ratio. They consequently have large impacts on genome evolution, adaptation, and the emergence and maintenance of sexually selected traits. Despite this, our understanding of their molecular basis and consequences for gametogenesis and sex chromosome regulation more broadly has focused on a handful of model organisms, primarily Drosophila and mouse, which are not representative of the broad diversity of reproductive modes and drive systems in nature. Here, we employ single-cell RNA sequencing (scRNA-seq) to investigate a sex-linked meiotic driver in the Malaysian stalk-eyed fly, Teleopsis dalmanni. First, we produce a comprehensive single-cell atlas of the male T. dalmanni gonad and identify major testis cell types. We then provide a comprehensive profile of the cellular and transcriptional landscape of the testis, providing evidence for a lack of complete meiotic sex chromosome inactivation and complex trajectory of dosage compensation. Second, by contrasting single-cell expression data between drive and standard testes, we provide insight into the consequences of a meiotic driver for the transcriptomic landscape of the testis and sex chromosome regulation. Importantly, we show that the presence of a meiotic driver does not perturb fundamental patterns of X-linked regulation. Our results provide insight into how the meiotic driver might bias its transmission to the next generation and highlight genes with perturbed expression as a potential consequence of the disruption of spermatogenesis.
性连锁减数分裂驱动因子限制了异配性别中另一条性染色体的遗传，进而扭曲了后代的性别比例。因此，它们对基因组进化、适应性以及性选择性状的出现和维持有重大影响。尽管如此，我们对其分子基础以及对配子发生和性染色体调控更广泛的影响的理解，主要集中在少数几种模式生物上，主要是果蝇和小鼠，而它们并不能代表自然界中广泛多样的生殖模式和驱动系统。在这里，我们采用单细胞RNA测序（scRNA-seq）来研究马来西亚 stalk-eyed 蝇（Teleopsis dalmanni）中的一种性连锁减数分裂驱动因子。首先，我们构建了雄性 T. dalmanni 性腺的全面单细胞图谱，并确定了主要的睾丸细胞类型。然后，我们提供了睾丸细胞和转录图谱的全面概况，为缺乏完全的减数分裂性染色体失活和复杂的剂量补偿轨迹提供了证据。其次，通过对比驱动型和标准型睾丸的单细胞表达数据，我们深入了解了减数分裂驱动因子对睾丸转录组景观和性染色体调控的影响。重要的是，我们表明减数分裂驱动因子的存在不会干扰X连锁调控的基本模式。我们的结果深入揭示了减数分裂驱动因子可能如何偏向其向下一代的传递，并突出了表达受到干扰的基因，这些基因是精子发生破坏的潜在后果。
