Nonpathological inflammation drives the development of an avian flight adaptation

Bird tails transitioned during the Mesozoic from long to shortened and distally fused. Fusion of the distalmost vertebrae manifests as the bony pygostyle, a trait retained in extant avians that contributes to flight aerodynamics. Here, we investigate the mechanism responsible for pygostyle formation. Transcriptomic profiling and histology reveal that the immune system is responsible 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, observed for the first time in birds, forms differently in fused versus unfused regions of the tail, and its deterioration in the pygostyle is crucial to the cascade of events that eventually lead to ankylosis. The Complement cascade, vasculogenesis, 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 an inflammatory response. These studies suggest that a universal mechanism for bone repair has been co-opted in avian evolution for the formation of a flight-adapted tail structure. Overall design: 8-10 week old chicken Intervertebral disc RNA samples. 4 samples from degenerating pygostyle ivds and 4 from permanent ivds.