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

龟壳确实是结构和进化生物学的奇迹。它是一种复合特征，包括一系列仅在海龟中已知的骨骼，但它也整合了大量的脊椎、肋骨和肩带元素。海龟的肩胛骨(肩胛骨)位于胸腔内，而所有其他爬行动物和哺乳动物的肩胛骨都在肋骨外部，这清楚地表明，海龟代表着一个挑战，无法理解这种明显戏剧性的进化变化是如何发生的。海龟是如何以及为什么获得如此独特的体型的，这是比较生物学历史上最长期存在的问题之一，也是一个非常悬而未决的问题。弄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种群联系起来的过渡性化石。由于缺乏关于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最先进化以及这些特征为海龟祖先提供了哪些选择优势等截然不同的假设。这个项目将通过协调来自最近发现的化石的新的解剖学数据，更详细地了解调控海龟特有特征产生的发育机制，以及来自广泛多样性的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精炼的海龟进化模型，它不仅有助于我们了解海龟的起源，还将作为如何解决跨越深处的困难进化问题的指南。海龟，尤其是化石海龟的广泛吸引力，也确保了这个项目将通过博物馆展览和外展活动为所有年龄和背景的人提供令人兴奋的教育机会。现在获取和分析基因组数据的相对容易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。这种模式面临着最大的挑战，树冠分支被极长的树干谱系分开，其中一个比较著名的例子是海龟的起源和它们有壳的身体平面。我们的项目建立在发育、分类学和化石记录的最新发现基础上，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目标：(1)使用高分辨率成像和进化分析，以化石记录为基础，建立龟干血统骨骼表型中特征转化的身份、功能和进化动力学；(2)利用密集采样的现代海龟和羊膜外群的个体发育序列，结合发育中的实验方法，建立龟冠和总种群的形态发生、调节和生长的祖先模式；(3)使用不同的分析方法来解决泛甲壳动物在现存和灭绝羊膜动物中的系统发育地位，并阐明一个时间校准的进化模型，该模型综合了形态、发育和遗传数据来描述海龟的出现及其特征。在寻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方面，该项目与NSF的十大想法之一--“理解生命规则：从基因类型预测表型”--高度一致。该奖项反映了NSF的法定使命，并通过使用基金会的智力优势和更广泛的影响审查标准进行评估，被认为值得支持。

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.