COLLABORATIVE RESEARCH: Integrative Approaches to the Turtle Body Plan: Evolutionary Origins of Structural Complexity in an Enigmatic Lineage

龟壳是结构和进化生物学的一个奇迹。这是一个复合特征，包括一系列只在海龟中已知的骨骼，但它也整合了大量的椎骨，肋骨和肩带元素。海龟的肩胛骨（肩胛骨）位于肋骨的内侧，而所有其他爬行动物和哺乳动物的肩胛骨都在肋骨的外侧，这清楚地表明，海龟代表了一个挑战，要理解这种明显的戏剧性进化变化是如何发生的。海龟究竟是如何以及为什么获得了如此独特的身体结构，这是比较生物学史上存在时间最长的问题之一，也是一个至今仍未解决的问题。澄清海龟起源的最大障碍是缺乏将海龟与其他已知爬行动物群体联系起来的过渡化石。由于缺乏有关海龟祖先的直接证据，导致了关于海龟在爬行动物生命树中的位置，现代海龟身体计划的哪些特征首先进化，以及这些特征为海龟祖先提供了哪些选择性优势的截然不同的假设。该项目将通过协调最近发现的化石中的新解剖数据，更详细地了解调节海龟特定性状产生的发育机制以及各种爬行动物的遗传序列模式来解决这些问题。最终产品将是一个高度完善的海龟进化模型，不仅有助于我们理解海龟的起源，而且将作为如何解决跨时间的进化难题的指南。海龟的广泛吸引力，特别是化石海龟，也确保了该项目将通过博物馆展览和推广活动为所有年龄和背景的人提供令人兴奋的教育机会。现在可以相对容易地获得和分析基因组数据，为推断发育系统的进化及其由此产生的表型提供了前所未有的机会。这种范式面临着最大的挑战，其中冠状分支被极长的茎谱系分开，其中一个比较著名的例子是海龟的起源和它们的贝壳身体计划。我们的项目建立在发展，系统学和化石记录的最新发现的基础上，以促进我们对早期海龟进化及其与比较生物学中广泛问题的相关性的理解。该项目的目标可以概括为四个方面：（1）利用高分辨率成像和进化分析，根据化石记录，确定龟干谱系骨骼表型特征转变的身份、功能和进化动力学;（2）使用现代海龟和外类群的密集采样个体发育系列，结合开发中的实验方法，建立龟冠和整个群体的形态发生、调节和生长的祖先模式;（3）使用不同的分析方法来解决泛龟鳖类在现存和灭绝的龟鳖类中的系统发育位置，并阐明一个时间校准的进化模型，该模型整合了描述龟类出现及其特征的形态、发育和遗传数据。在追求理解脊椎动物身体计划的基本原则以及该计划可能发生重大变化的机制的过程中，该项目与NSF的10大理念之一-“理解生命规则：从基因型预测表型”高度一致。该奖项反映了NSF的法定使命，并被认为是值得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的支持。

The turtle shell is truly a wonder of structural and evolutionary biology. It is a compound feature that includes a series of bones known only in turtles, but it also integrates a large number of vertebrae, ribs, and shoulder girdle elements. That the turtle scapula (shoulder blade) lies inside of the rib cage, whereas all other reptiles and mammals have the scapula on the outside of the ribs, is a clear indication that turtles represent a challenge to understand how such apparently dramatic evolutionary change occurs. Exactly how and why turtles acquired such a peculiar body plan is one of the longest standing problems in the history of comparative biology, and one that remains very much unresolved. The largest impediment to clarifying the origin of turtles has been the lack of transitional fossils linking turtles to other known reptile groups. This absence of direct evidence regarding turtle ancestry has resulted in strikingly disparate hypotheses as to where turtles sit within the reptile tree of life, what features of the modern turtle body plan evolved first, and what selective advantages these features provided turtle ancestors. This project will address these problems by coordinating novel anatomical data from recently discovered fossils, a more detailed understanding of the developmental mechanisms that regulate the production of turtle-specific traits, and the patterns of genetic sequences from a wide diversity of reptiles. The end product will be a highly refined model of turtle evolution that will not only facilitate our understanding of turtle origins but will serve as a guide for how to tackle difficult evolutionary problems across deep time. The broad appeal of turtles, and especially fossil turtles, also ensures that this project will deliver exciting educational opportunities for people of all ages and backgrounds through museum exhibits and outreach activities.The relative ease with which genomic data can now be acquired and analyzed provides unprecedented opportunities for inferring the evolution of developmental systems and their resultant phenotypes. This paradigm faces its greatest challenge where crown clades are separated by extremely long stem lineages, with one of the more famous examples being the origin of turtles and their shelled body plan. Our project builds on recent discoveries in development, systematics, and the fossil record to advance our understanding of early turtle evolution and its relevance for broad-based questions in comparative biology. The goals of the project can be summarized under four objectives: (1) use high-resolution imaging and evolutionary analyses to establish the identity, functionality, and evolutionary dynamics of character transformations in the skeletal phenotype of the turtle stem lineage based on the fossil record; (2) use densely sampled ontogenetic series of modern turtles and amniote outgroups, integrated with experimental approaches in development, to establish ancestral patterns of morphogenesis, regulation, and growth for the turtle crown and total group; (3) use diverse analytical approaches to address the phylogenetic position of Pan-Testudines among both extant and extinct amniotes and to articulate a time-calibrated evolutionary model that integrates morphological, developmental, and genetic data in describing the emergence of turtles and their characteristic features. In its pursuit to understand the basic principles that underlie the vertebrate body plan and the mechanisms through which large changes to this plan can occur, this project is highly congruent with one of NSF’s 10 Big Ideas — “Understanding the Rules of Life: Predicting Phenotype from Genotype.”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.