CAREER: Investigating the deep origin and evolution of the bird beak by synthesizing the fossil record and comparative embryology of archosaurian reptiles

我们的星球上充满了各种形状和大小的生命，它们通过生态和血统以无数种方式相互联系。了解地球生物多样性是如何以及为什么形成的一种方法是追溯一次大进化辐射的历史，确定导致其成功的关键事件。在陆地脊椎动物中，鸟类在物种数量、工程和地理分布方面都很突出。该项目将探索支撑鸟类多样性的信号创新之一的历史和胚胎发育：喙。在此过程中，该项目将发现在进化过程中喙是如何形成的，以及在每只鸟的早期存在中喙是如何重新组装的。鸟喙是一项“关键创新”，是一种促成后续成功的技术进步。它是一种非常有效和多用途的生物工具，其复杂而高效的结构经过修改，可以吸收花蜜（蜂鸟）和肉（猛禽）等不同的食物。在很多方面，鸟类的多样性就是喙的多样性。鸟喙在鸟类飞行的进化过程中也是不可或缺的：在鸟类的恐龙祖先中，第一批鸟喙似乎扮演了“代手”的角色，取代了融合在翅膀上的手指。这个项目将使用记录了3亿年爬行动物进化的化石来确定导致鸟喙进化的步骤。特别是，他们将寻求发现先前存在的解剖结构，特别是古代祖龙的掠食性颌骨是如何被吸收和重新排列以形成喙的，并将寻找折衷和相互依赖（整合和模块化）的经典进化（和工程）现象的特征。该项目还研究了现代鸟类的胚胎喙是如何形成的，以及它的发育与爬行动物的鼻子有何不同——特别是，将现代胚胎与化石和化石胚胎进行比较，是否可以告诉我们，鸟类喙的哪些部分是在爬行动物胚胎解剖学的后期“调整”或补充形成的，哪些是真正的“新的”。关于鸟类和现存恐龙在现代世界变得如此多样化和丰富的宏大叙事自然是引人注目的，所生成的数据往往是惊人的和美丽的。该项目将把他们的研究成果，包括这些数据的数字图像和3D打印，纳入他们在耶鲁大学教授的课程，以及为K-12教室设计的工具包和课程，重点是低收入城市学校。除了交换材料和知识之外，该项目的调查人员还将访问教室，此外，还将为K-12学生及其老师进行校园研究和收集设施的参观，其中许多学生来自STEM中代表性不足的群体，目的是与学校、教师和学生建立长期关系。该项目还将在新装修的耶鲁皮博迪博物馆（Yale Peabody Museum）设计展览，展示这项工作的发现。最后，项目团队将在整个项目期间进行一系列在线和面对面的公开讲座和问答环节。鸟喙是生物工程的奇迹，也是鸟类辐射的关键创新。该项目将研究从茎类爬行动物到冠类鸟类的喙的形态组装，同时，将喙的胚胎组装与爬行动物的鼻子进行比较。特别是，该项目将测试共同选择的假设，随后是进一步的新颖性和约束释放，即鸟类头部的起源来自祖先的始祖龙头部，然后是新颌的起源来自祖先的鸟类动力系统。这将通过结合化石和现存分类群的3D CT成像，以及使用系统发育bracketing重建软组织解剖来完成。形状和变形的分析将是三维的和定量的。该项目将使用各种方法进一步测试围绕主要软组织结构的骨骼元素的集成和模块化假设，特别是将阐明空间包装或空间竞争造成的约束和权衡。这将通过定量分析进化轨迹和发育轨迹来完成（部分使用整个免疫染色胚胎的高保真共聚焦成像重建）。最后，该项目将利用结合胚胎、化石和化石胚胎的综合方法，试图揭示鸟类头骨进化起源中不同的个体发生或发育过程的相对贡献，即终端添加和早期转化。特别是，该项目将包括重建祖先的进化序列（来自化石数据）和个体发生序列（化石和现存）的组合分析，并将定量评估这些序列的对应或不对应。最终，该项目将全面展示导致独特鸟类状况的进化和发展序列，并将深入了解其起源过程中的转变现象和进化动态。该项目是与地球科学部沉积地质与古生物学项目共同资助的。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

Our planet teems with life in a vast array of shapes and sizes, interconnected in myriad ways by ecology and by descent. One way to understand how and why Earth’s biodiversity came to be is to trace the history of a great evolutionary radiation deteremine the key events that contributed to its success. Among land vertebrates, birds stand out in terms of species number, engineering, and geographic spread. This project will explore both the history and the embryonic development of one of the signal innovations that underpins bird diversity: the beak. In doing so, the project will discover the way in which the beak was built during evolution and the way in which it is assembled anew during the early existence of each individual bird. The avian beak is a “key innovation,” a sort of technological advance that enabled subsequent success. It is a remarkably effective and versatile biological tool whose complex and efficient architecture has been modified for taking in food as disparate as nectar (hummingbirds) and flesh (birds of prey). The diversity of birds is, in many ways, a diversity of beaks. The beak was also integral to the evolution of bird flight: the first beaks, in the dinosaurian ancestors of birds, seem to have acted as “surrogate hands” to replace the fingers fused and incorporated into the wing. This project will use fossils that document 300 million years of reptile evolution to determine the steps that led to the evolution of the bird beak. They will, in particular, seek to discover how pre-existing anatomical structures, especially the predatory jaws of ancient archosaurs were co-opted and rearranged to make the beak, and will search for signatures of the classic evolutionary (and engineering) phenomena of tradeoffs and co-dependencies (integration and modularity). The project also investigates how the embryonic beak is formed in modern birds and how its development differs from that of the reptilian snout — in particular, whether comparisons of modern embryos with fossils and fossilized embryos can tell us about which parts of the bird beak form by late “tweaking” of, or addition to, a fundamentally reptilian embryonic anatomy and which are truly “new.” The grand narrative of the way in which birds, living dinosaurs, came to be so diverse and abundant in the modern world is naturally compelling, and the data to be generated are often striking and beautiful. The project will incorporate the findings of their work, including digital images and 3D prints of these data, into the courses they teach at Yale and into kits and curricula designed for K-12 classrooms, with a focus on low-income urban schools. Beyond exchange of materials and knowledge, the project's investigators will visit classrooms and will, moreover, conduct on-campus tours of research and collections facilities for K-12 students, many from underrepresented groups in STEM, and their teachers, with the intention of building long-term relationships with schools, teachers and students. The project also will lead to the design of exhibits featuring the discoveries from this work in part of the newly renovated Yale Peabody Museum. Finally, the project team will conduct a series of online and in-person public lectures and question-and-answer sessions throughout the duration of the project. The avian beak is a marvel of biological engineering and a key innovation that enabled the radiation of birds. This project will examine the morphological assembly of the beak from stem reptiles through to crown-clade birds and, simultaneously, the embryonic assembly of the beak as compared to that of the reptilian snout. In particular, the project will test the hypothesis of co-option followed by further novelty and constraint release in the origin of the avian head from the ancestral archosaurian head, then the origin of the neognath jaw apparatus from the ancestral avian kinetic system. This will be accomplished using a combination of 3D CT imaging of fossils and extant taxa, and reconstruction of soft tissue anatomy using phylogenetic bracketing. Analyses of shape and transformation will be three-dimensional and quantitative. The project will further test hypotheses of integration and modularity of skeletal elements surrounding major soft tissue structures using a variety of methods, and in particular will elucidate constraint and tradeoffs resulting from spatial packing or competition for space. This will be accomplished by quantitatively analyzing evolutionary trajectories and developmental trajectories (in part reconstructed using high-fidelity confocal imaging of entire immunostained embryos). Finally, the project will seek to unravel the relative contributions of the distinct ontogenetic or developmental processes of terminal addition and early transformation in the evolutionary origin of the avian skull, using an integrative approach that incorporates embryos, fossils, and fossil embryos. In particular, the project will include both evolutionary sequences of reconstructed ancestors (from fossil data) and ontogenetic sequences (fossil and extant) in combined analyses and will quantitatively assess the correspondence or non-correspondence of these sequences. Ultimately, the project will present a comprehensive picture of the sequence of evolution and development leading to the distinctive avian condition, and will gain insight into the transformational phenomena and evolutionary dynamics in operation during its genesis.This project was jointly funded with the Sedimentary Geology and Paleobiology Program in the Division of Earth Sciences.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.