Evolution of axial regionalization in Aves during the Mesozoic and its impact on the survival of modern lineages to K/Pgmass extinction

Abstract

The axial column of Neornithes (modern birds) is characterized by regional fusions in caudal vertebrae (pygostyle), lumbosacrals (synsacrum), and thoracics (notarium in several taxa) that provide a rigid and stable axis during flight. Such a configuration integrates into a body plan highly suited for wing-assisted locomotion (with feathered forelimbs, modified girdles, and crouched limbs) that evolved from running dinosaurs and stem birds over the last ~150 million years. Shifts in count numbers and fusion of vertebrae have had paramount implications on the avian diversification and flight refinement. However, how the organization of precaudal vertebrae evolved across the dinosaur–bird lineage, and how and when the highly tuned axial column of neornithines was acquired are unexplored. Here, we quantify vertebral numbers in pennaraptoran dinosaurs –including Aves—, and show how the axial configuration of birds was driven from different shifts between two primary developmental mechanisms of body-axis organization: segmentation and homeotic regionalization. We demonstrate that the configuration highly tuned for flight of modern birds was not fully acquired until the appearance of Neornithes. The acquisition of a trunk-sacrum configuration more efficient to deal with stresses derived from the flapping flight could be a key factor in the survivorship of neornithines and the extinction of non-neornithine birds during the end-Cretaceous mass extinction event.