Form, function and development of the amniote skull: a case study using lepidosaurs

我们眼睛后面的头盖骨的每一边都有一个巨大的开口，里面有令人瞠目结舌的肌肉。虽然我们物种和其他哺乳动物的头骨只有一个开口，即颞窗，但3亿多年前所有羊膜动物(哺乳动物和爬行动物，包括鸟类)的祖先都有两个开口。在进化过程中，时间窗的数量和形式的变化在教科书中传统上被描述为产生了活的羊膜动物的主要谱系，以及它们在广泛的环境中的多样性。例如，虽然哺乳动物只进化了一个窗孔，但蛇已经失去了它们的颞窗，鳄鱼保留了两个。然而，颞骨窗的进化史比之前认为的要复杂得多，因为相似的窗口法在不同的群体中进化了多次，而且具有相同窗口法的物种在相关骨支架的大小、形状和排列方面往往表现出很大的差异。因为颞窗内有闭口肌，所以在进化过程中，它们的存在或缺失及其形态的变化传统上都与闭口肌的体积、进食力和饮食有关。这些进化变化被解释为胚胎发育过程中头骨骨化方式的变化，这将改变发育中肌肉的位置。然而，我们现在知道，在发育中的胚胎中，肌肉和其他软组织在骨骼元素之前形成，因此我们认为颅骨窗的形成可能是肌肉发育方式的结果。此外，目前尚不清楚窗口及其相关肌肉结构的变化如何影响摄食过程中整个头骨的功能和力学，以及头骨的发育、形态和功能如何相互作用，影响羊膜中头骨的进化。在这个项目中，我们建议通过关注鳞龙(蜥蜴、蜥蜴和蛇)来解决这些问题，鳞龙是现存羊膜动物中最似是而非的类群之一，具有显著的生态和解剖多样性，包括在活羊膜动物中发现的主要类型的窗口。由于缺乏关于非模型动物颅骨和肌肉如何发育的知识，缺乏关于活体动物肌肉特性的比较数据集，以及无法应用计算方法在大样本上推断功能从而对功能和进化做出推断，这些想法和问题的解决受到了阻碍。在这里，我们聚集了一个研究团队，他们是开发和验证成像、重建和模拟肌肉骨骼解剖学、其发展和功能的方法的领导者。该团队将提供大量关于代表鳞龙头骨结构变化的物种的发育数据(150个发育阶段)，以及涵盖所有主要科的成年动物(150个物种)的肌肉骨骼解剖和功能数据。我们将首次集中了解颅骨是如何发育的，骨骼和肌肉形成的相对时间；这如何导致头骨形状、肌肉特性以及头骨形状、肌肉和功能之间的关系(饮食和生态)的变化。我们的项目将产生方法学上的进步，可以更广泛地应用于进化转变和辐射，并解决长期存在的将形式和功能联系在一起的问题。古生物学家、解剖学家、生物机械学家、进化和发育生物学家和工程师将从这项工作中受益，这将建立新的国际合作。它的视觉方面和对蜥蜴和蛇的关注将吸引公众，提供参与机会并引起媒体的兴趣。

Each side of our skull behind our eyes bears a large opening that houses jaw-closing muscles. While the skull of our species and other mammals has a single opening, or temporal fenestra, the ancestors of all amniotes (mammals and reptiles, including birds) more than 300 million years ago had two. Transformations in the number and form of the temporal fenestrae during evolution is traditionally depicted in textbooks as giving rise to the major lineages of living amniotes, and their diversification in a broad array of environments. For instance, while mammals have evolved only one fenestra, snakes have lost their temporal fenestrae, and crocodiles retain two. The evolutionary history of temporal fenestrae is however more complex than previously thought, as similar fenestration has evolved multiple times in different groups, and species that share the same fenestration often exhibit a great variability in terms of size, shape, and arrangement of the associated bony scaffold. Because the temporal fenestrae house the jaw-closing muscles, their presence or absence and changes in their morphology during evolution have been traditionally linked to the volume of the jaw-closing musculature, feeding forces, and diet. These evolutionary changes were interpreted as resulting from changes in the way the skull ossifies during embryonic development, which would alter the position of the developing muscles. Yet, we now know that muscles and other soft tissues form before the skeletal elements in the developing embryos, and we therefore think that the formation of the fenestrae in the cranium might be a consequence of the way muscles develop. In addition, it is still unclear how variation in the fenestration and in its associated musculature influences the functioning and mechanics of the overall skull during feeding, and thus how development, morphology and function of the skull interact to influence the evolution of the skull in amniotes. In this project we propose to address these questions by focusing on lepidosaurs (tuatara, lizards, and snakes), one of the most specious group of living amniotes with a remarkable ecological and anatomical diversity, that encompasses the major types of fenestration found in living amniotes. Addressing these ideas and questions has been hindered by a lack of knowledge on how the skull bones and muscles develop in non-model animals, by the lack of a comparative dataset on muscle properties across living animals and the inability to apply computational approaches to deduce function on large sample sizes and therefore make inferences on function and evolution. Here we bring together a team of researchers who are leaders in developing and validating methods for imaging, reconstructing, and simulating the musculoskeletal anatomy, its development and function. The team will provide large amounts of developmental data (150 developmental stages) on species that represent the variation in skull construction across lepidosaurs, as well as data on musculoskeletal anatomy and function on adult animals (150 species) that encompass all major families. For the first time we will bring together an understanding of how the skull develops, and the relative timing of bone and muscle formation; how this generates variation in skull shape, muscle properties and the relationship between skull shape, muscles, and function (diet and ecology). Our project will produce methodological advances that can be applied more broadly to evolutionary transitions and radiations, and to address long standing questions linking form and function. Palaeontologists, anatomists, biomechanists, evolutionary and developmental biologists and engineers will benefit from this work, which will establish new international collaborations. Its visual aspect and focus on lizards and snakes will appeal to the public, offering engagement opportunities and generating media interest.