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

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.