Reconstruction of the birth of an unexpected male sex chromosome in Atlantic herring

The mechanisms underlying sex determination are astonishingly plastic. Particularly the triggers for the molecular machinery, which unambiguously recalls either the male or female program from a bipotential genome, are highly variable and have evolved independently and repeatedly. Fish show a huge variety of sex determination systems, including both genetic and environmental triggers. The advent of sex chromosomes is assumed to stabilize genetic sex determination. However, the study of sex chromosome evolution is hampered because sex chromosomes are notoriously cluttered with repetitive DNA and pseudogenes. Here we reconstruct the birth of a Y-chromosome in the Atlantic herring. The region is tiny (350 kb) and contains only three intact genes. The male-determining gene BMPR1BBY encodes a truncated form of a BMP1B receptor, which originated by gene duplication and translocation, and underwent rapid protein evolution and transcriptional rewiring. BMPR1BBY phosphorylates SMADs in the absence of a ligand and, thereby, has the potential to induce testis formation. The Y-region contains two male-beneficial genes encoding subunits of the sperm-specific Ca2+ channel CatSper required for male fertility. Our results support the hypothesis that evolution of sex chromosomes requires both a sex-determining factor and sex-beneficial genes. A sex chromosome in Atlantic herring is unexpected because theory predicts that non-genetic, random sex determination should be most efficient in species with large population size.

支撑性别决定的机制展现出惊人的可塑性。其中，调控该分子机制的触发因子——能从双潜能基因组中精准启动雄性或雌性发育程序的因子——尤为多变，且经历了独立且多次的演化。
鱼类的性别决定系统极具多样性，涵盖遗传触发与环境触发两种类型。学界普遍认为，性染色体的出现可使遗传型性别决定更为稳定。然而，性染色体演化的研究常受阻碍——这是因为性染色体往往充斥着重复DNA序列与假基因，这一特性广为人知。
本研究重构了大西洋鲱Y染色体的起源历程。该区域规模极小（仅350千碱基对），仅包含3个完整功能基因。雄性决定基因骨形态发生蛋白受体1BBY（BMPR1BBY）编码一种截短型BMP1B受体，该受体源自基因复制与易位事件，并经历了快速的蛋白质演化与转录重编程。BMPR1BBY可在无配体存在的情况下磷酸化SMAD蛋白，由此具备诱导睾丸发育的潜能。该Y染色体区域还包含两个雄性有益基因，它们编码精子特异性钙通道CatSper的亚基，而CatSper是雄性生育所必需的通道蛋白。
本研究结果支持如下假说：性染色体的演化同时需要性别决定因子与雄性有益基因的协同参与。大西洋鲱中存在性染色体这一发现出人意料，因为相关理论预测：在种群规模庞大的物种中，非遗传型随机性别决定机制的效率应最高。