Origin of avian genome size and structure in non-avian dinosaurs

Abstract

One of the less well known factors associated with flight in vertebrates is a reduction of the size of the genome. Birds have remarkably small genomes compared with other vertebrates, and bats tend to have smaller genomes than do non-flying mammals. But does flight cause genome loss, or does genome loss predispose animals to take flight? The latter seems to be the case, to judge from an extensive analysis of bone cell volume and genome size in dinosaurs. Genome reduction can be traced deep into the lineage of saurischian dinosaurs — the dinosaur group of which the birds are the only surviving members — but not in ornithischian dinosaurs. A correlate of flight in vertebrates is a reduction of the genome. But does flight cause genome loss, or does genome loss predispose animals to take flight? Histology and statistical techniques shows that genome reduction can be traced deep into the lineage of saurischian dinosaurs. Genome reduction thus joins the morphological features we now associate with birds that can be traced far back into the dinosaurian ancestry. Avian genomes are small and streamlined compared with those of other amniotes by virtue of having fewer repetitive elements and less non-coding DNA1,2. This condition has been suggested to represent a key adaptation for flight in birds, by reducing the metabolic costs associated with having large genome and cell sizes3,4. However, the evolution of genome architecture in birds, or any other lineage, is difficult to study because genomic information is often absent for long-extinct relatives. Here we use a novel bayesian comparative method to show that bone-cell size correlates well with genome size in extant vertebrates, and hence use this relationship to estimate the genome sizes of 31 species of extinct dinosaur, including several species of extinct birds. Our results indicate that the small genomes typically associated with avian flight evolved in the saurischian dinosaur lineage between 230 and 250 million years ago, long before this lineage gave rise to the first birds. By comparison, ornithischian dinosaurs are inferred to have had much larger genomes, which were probably typical for ancestral Dinosauria. Using comparative genomic data, we estimate that genome-wide interspersed mobile elements, a class of repetitive DNA, comprised 5–12% of the total genome size in the saurischian dinosaur lineage, but was 7–19% of total genome size in ornithischian dinosaurs, suggesting that repetitive elements became less active in the saurischian lineage. These genomic characteristics should be added to the list of attributes previously considered avian but now thought to have arisen in non-avian dinosaurs, such as feathers5, pulmonary innovations6, and parental care and nesting7.