Avian Dinosaur Tail Evolution and Bone Fracture Healing

Abstract

Bird tails transitioned during the Mesozoic from long to shortened and distally fused. Fusion of the distalmost vertebrae manifests as the bony pygostyle structure, a trait retained in extant avians that contributes to flight aerodynamics. Here, we investigate the mechanism responsible for pygostyle formation. Transcriptomic profiling and histology in extant tail tissue reveal that the immune system is crucial for this important adaptation in avian evolutionary history. Pygostyle formation commences with cell death in the intervertebral discs, within the nucleus pulposus and annulus fibrosus. The nucleus pulposus, previously thought absent in birds, forms differently in fused versus unfused regions of the tail, and its deterioration in the pygostyle is integral to the cascade of events that eventually lead to ankylosis. The complement and coagulation cascades, angiogenesis, neutrophil-like cell function, involvement of both the innate and adaptive immune systems and multiple additional events mirror those observed during bone fracture healing. The key common denominator in both processes that differentiates them from general endochondral ossification is the inflammatory response. These studies indicate that a universal mechanism for bone repair has been co-opted in avian evolution for the formation of a flight-adapted tail structure.