Reconstruction of the diapsid ancestral genome permits chromosome evolution tracing in avian and non-avian dinosaurs

Genomic organisation of extinct lineages can be inferred from extant chromosome-level genome assemblies. Here, we apply bioinformatic and molecular cytogenetic approaches to determine the genomic structure of the diapsid common ancestor. We then infer the events that likely occurred along this lineage from theropod dinosaurs through to modern birds. Our results suggest that most elements of a typical ‘avian-like’ karyotype (40 chromosome pairs, including 30 microchromosomes) were in place before the divergence of turtles from birds ~255 mya. This genome organisation therefore predates the emergence of early dinosaurs and pterosaurs and the evolution of flight. Remaining largely unchanged interchromosomally through the dinosaur–theropod route that led to modern birds, intrachromosomal changes nonetheless reveal evolutionary breakpoint regions enriched for genes with ontology terms related to chromatin organisation and transcription. This genomic structure therefore appears highly stable yet contributes to a large degree of phenotypic diversity, as well as underpinning adaptive responses to major environmental disruptions via intrachromosomal repatterning. Ancient diapsids diverged into the lineages leading to turtles and birds over 250 million years ago. Here, the authors use genomic and molecular cytogenetic analyses of modern species to infer the genome structure of the diapsid common ancestor (DCA) and the changes occurring along the lineage to birds through theropod dinosaurs.