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. 8-10 week old chicken Intervertebral disc RNA samples. 4 samples from degenerating pygostyle ivds and 4 from permanent ivds.

鸟类尾部在中生代时期经历了从修长到缩短且远端愈合的演化过程。最远端椎骨的愈合形成了骨质尾综骨（pygostyle），这一特征被现生鸟类保留，并对飞行空气动力学性能具有关键贡献。本研究旨在探究尾综骨形成的分子机制。转录组谱分析（transcriptomic profiling）与组织学研究显示，免疫系统在鸟类演化历史中这一重要适应性特征的形成过程中发挥核心作用。尾综骨的形成始于椎间盘（intervertebral discs, IVDs）内髓核（nucleus pulposus）与纤维环（annulus fibrosus）区域的细胞死亡。髓核在鸟类中为首次被观测到，其在尾部愈合区域与非愈合区域的形成模式存在显著差异，而尾综骨区域髓核的退变对于最终导致骨性强直（ankylosis）的级联反应至关重要。补体级联反应（Complement cascade）、血管生成（vasculogenesis）、嗜中性粒细胞样细胞功能、先天与适应性免疫系统的参与，以及多种其他事件，均与骨折愈合过程中观测到的现象高度相似。相较于普通的软骨内骨化（endochondral ossification），这两个过程的关键共同特征在于存在炎症应答。本研究结果表明，鸟类演化过程中，骨骼修复的通用机制被招募用于形成适应飞行的尾部结构。实验样本取自8-10周龄鸡的椎间盘RNA样本，包含4份退变尾综骨椎间盘样本与4份持久性椎间盘样本。