Origin of the avian respiratory system: a CT-study of postcranial pneumaticity in basal archosaurs

现存鸟类（超过9000种）的惊人成功部分归功于它们独特的呼吸系统，这是高代谢和飞行的关键进化创新的基础。这个系统包括肺和一系列复杂的相互连接的气囊。气囊允许空气通过肺部单向流动，从而允许非常有效的气体交换。气囊的延伸物穿透并使附近的骨骼（包括椎骨和肢体）退化，从而产生减少骨骼质量的相关效果。相比之下，鸟类的近亲鳄鱼缺乏气囊和相应的气动特征。现在有压倒性的证据表明，鸟类是兽脚亚目恐龙的直接后裔。许多以前被认为是鸟类独有的特征首先出现在恐龙中（例如羽毛，育雏行为）。鸟类的气囊系统是另一个这样的功能：它存在于兽脚亚目和蜥脚亚目恐龙（以及翼龙）中，这是根据椎骨中的气动特征推断出来的，这些特征几乎与在现存鸟类中看到的相同。然而，气囊系统的起源知之甚少：对于气囊和呼吸系统是否存在于兽脚类、蜥脚类和翼龙的共同祖先中，或者它们是否在这三个群体中独立进化，没有达成共识。此外，最近在亲缘关系较远的三叠纪初龙中发现了可能存在呼吸能力的证据，这引发了一个有争议的假设，即呼吸能力（以及由此推断的气囊和一些类似鸟类的呼吸能力）可能存在于鸟类和鳄鱼的最后一个共同祖先中，随后在鳄鱼中消失。如果这是真的，这将需要彻底改变我们对鸟类和鳄鱼的非凡生物学以及它们如何进化的理解。了解鸟类呼吸系统的起源显然是解释各种祖龙谱系的成功和多样性的基础。然而，主要的备选假设尚未得到检验。我们提出了一个试点研究，以测试解释鸟类呼吸起源的替代假设。这项工作是及时的，因为最近对恐龙和鸟类呼吸系统的浓厚兴趣，研究小组的可用性和自然历史博物馆新的微型X射线计算机断层扫描（CT）设施。我们将确定是否存在气动结构在选定的三叠纪祖龙的椎骨，谎言接近鳄鱼和鸟类的共同祖先。脊柱畸形的识别将基于外部和内部椎骨解剖结构：后者的数据以前不可用，但将使用CT扫描获得-这是解决该问题的一种全新方法。将记录单个骨骼和整个骨骼中的气动结构的程度，并通过将这些特征的存在/不存在映射到当前的祖龙进化树上来确定气动结构的分布。这将使我们能够确定：当无脊椎动物出现在祖龙;是否收购（或损失）无脊椎动物是一个单一的事件或发生在多个独立的场合;和进化序列中的气囊系统的不同组成部分出现。如果证明基基首龙类没有呼吸系统，就可以推翻祖先首龙类中存在类似鸟类的呼吸系统的假设，并支持另一种假设，即气囊的起源较晚。然而，如果在原始的主龙类中确定了呼吸系统，这个项目将证明气囊系统的进化比目前假设的更复杂，并将促进未来对鸟类和鳄鱼呼吸系统起源的研究。这项工作对古生物学家、动物学家和生理学家具有根本的重要性。

The incredible success of living birds (>9000 species) results, in part, from their unique respiratory system, which underpins the key evolutionary innovations of high metabolism and flight. This system comprises the lungs and a complex array of interconnected air sacs. The air sacs allow a unidirectional flow of air through the lungs, permitting exceptionally efficient gas-exchange. Extensions from the air sacs penetrate and pneumatize nearby bones, including vertebrae and limb elements, with the associated effect of reducing skeletal mass. In contrast, the closest living relatives of birds, crocodiles, lack air sacs and corresponding pneumatic features. There is now overwhelming evidence that birds are direct descendents of theropod dinosaurs. Many features previously regarded as uniquely avian appeared first among dinosaurs (e.g. feathers, brooding behaviour). The avian air sac system is another such feature: its presence in theropod and sauropod dinosaurs (and pterosaurs) has been inferred on the basis of pneumatic features in vertebrae that are almost identical to those seen in living birds. However, the origin of the air sac system is poorly understood: there is no consensus on whether air sacs and pneumaticity were present in the common ancestor of theropods, sauropods and pterosaurs, or whether they evolved independently in these three groups. Furthermore, possible evidence of pneumaticity has recently been identified in more distantly related Triassic archosaurs, prompting the controversial hypothesis that pneumaticity (and, by inference, air sacs and some bird-like respiratory capabilities) may have been present in the last common ancestor of birds and crocodiles, and subsequently lost in crocodilians. If true, this would require radical alteration of our understanding of the remarkable biology of birds and crocodiles and how they evolved. Understanding the origin of the avian respiratory system is clearly fundamental to explaining the success and diversity of the various archosaur lineages. However, the main alternative hypotheses have not yet been tested. We propose a pilot study to test alternative hypotheses explaining the origin of bird-like respiration. This work is timely, given recent intensive interest in dinosaur and bird respiratory systems, the availability of the research team and a new micro X-ray Computed Tomography (CT) facility at the Natural History Museum. We will determine the presence/absence of pneumatic structures in the vertebrae of selected Triassic archosaurs that lie close to the common ancestry of crocodiles and birds. The identification of pneumaticity will be based on external and internal vertebral anatomy: the latter data were previously unavailable, but will be obtained using CT scans - an entirely novel approach to this problem. The extent of pneumaticity, both within individual bones and throughout the skeleton, will be documented and the distribution of pneumatic structures will be determined by mapping the presence/absence of these features onto current archosaur evolutionary trees. This will permit us to establish: when pneumaticity appeared in archosaurs; whether the acquisition (or loss) of pneumaticity was a single event or occurred on multiple independent occasions; and the evolutionary sequence in which the different components of the air sac system appeared. Demonstrating the absence of pneumaticity in basal archosaurs would falsify hypotheses that a bird-like respiratory system was present in the ancestral archosaur, and support alternative hypotheses suggesting a later origin of air sacs. However, if pneumaticity is identified in primitive archosaurs this project will demonstrate that evolution of the air sac system is more complex than currently assumed and will facilitate future investigations into the origins of avian and crocodilian respiratory systems. This work will be of fundamental importance to palaeontologists, zoologists and physiologists.