Stable but turbulent: the two faces of the germline-restricted chromosome of passerine birds

Abstract Germline-restricted chromosomes (GRCs) are essential, supernumerary chromosomes that undergo programmed elimination in somatic cells and are only retained in the germline. Despite their recurrent emergence across animals, their genetic composition, function and evolution remain poorly understood. Here we present the most complete and contiguous GRC assemblies, including one nearly telomere-to-telomere GRC assembly, from four closely related passerine bird species, providing an unprecedented insight into the GRC’s composition and its evolution over short evolutionary timescales. We show that the passerine GRC is highly enriched in repetitive sequences, with massive, species-specific satellite expansions resulting in enormous differences in GRC size among species. Among mostly recently added sequences, we found only two ancestral genes dating back to the presumed GRC origin, offering clues to its essential function. Importantly, we demonstrate that the GRC undergoes extensive fine-scale within-chromosome rearrangements and copy number changes resulting in little collinearity between species. Our findings indicate that programmed DNA elimination has profoundly changed the GRC’s evolution by altering the selection pressures and mutational mechanisms it is exposed to. This makes the GRC an extraordinarily dynamic element in an otherwise stable avian karyotype, retaining core functions while diversifying rapidly, with important implications for germline biology, adaptive evolution and speciation. Competing Interest Statement The authors have declared no competing interest. Data availability Raw sequence data and GRC assemblies have been uploaded to NCBI (bioproject PRJNA1400222). GRC assemblies have also been uploaded onto figshare (10.6084/m9.figshare.31343230).