Teeth and jaws: evolutionary emergence of a model organogenic system and the adaptive radiation of gnathostomes

超过99.8%的现存脊椎动物是颌口动物（有颌和牙齿的脊椎动物），因此颌口动物的起源代表了动物进化中最重要的事件之一。人们普遍认为，牙齿和下颚是支撑有颌脊椎动物适应性辐射的关键创新，并使它们能够将在此前150亿年间主导脊椎动物群落的无颌近亲推向灭绝。最近的三项发现挑战了这一长期以来的假设：(a)“牙齿”在下颚之前进化（因此牙齿和下颚的起源并不协调）；(b)所有有颌脊椎动物谱系都是原始无牙的，并且各自独立进化出牙齿；(c)对最原始有颌脊椎动物进化关系的一次重大修正，推翻了长期以来确立的观点，即已灭绝的两个主要原始有颌脊椎动物群体——板皮动物和棘足动物——实际上是许多不同的群体，它们与现存的有颌脊椎动物——鲨鱼和硬骨鱼（后者包括我们自己的进化谱系）——在程度上有联系。这不仅仅是一种系统发育上的精确：它揭示了冠颌口动物身体结构的漫长而有序的构建，包括所谓的颌和牙齿进化创新的组装。这些发现的影响远远超出了进化生物学的范畴，因为牙齿是理解器官发育一般原理的核心模型，而这些理论在很大程度上依赖于这样一个假设：所有脊椎动物的牙齿都是从一个共同的祖先进化而来的，鲨鱼可以被认为是原始状态的代表。这似乎不再是情况，我们对这种模式有机系统的进化的理解是混乱的。因此，我们面临着认识的重大转变，需要对有颌脊椎动物起源的解释进行彻底的重新表述，但现有的数据无法胜任这项工作。我们对无颌脊椎动物的“牙齿”的功能一无所知，而无牙有颌脊椎动物的进食也一直不是批判性分析的主题。后来，每个谱系中有牙齿的代表如何进食是未知的，因此，咬口辐射的最终原因也是未知的。此外，我们甚至不知道辐射是什么时候发生的：与颌骨的起源同时发生，与后来牙齿的趋同发生，还是两者都不发生？我们甚至不能自信地知道牙齿趋同进化的新假设是否正确，因为没有全面的进化树来测试无牙的形式是出现在接近基部的地方，还是出现在更高级的啮齿动物谱系中，我们的初步调查显示，这些“无牙”的形式似乎拥有kosha牙齿。我们建议通过一个创新的多学科研究计划，将四位研究者独特和互补的专业知识与尖端的高科技方法相结合，来解决这个问题。现有的关于已灭绝的无颌和基颌脊椎动物的下颌和牙齿功能的假设将通过牙齿微磨损分析进行测试，这将为脊椎动物如何进食及其食物的性质提供直接证据。我们将使用复杂而强大的计算机模型来确定颌骨和牙齿是如何被设计成适合它们的功能的。这些模型将使用来自先进同步辐射x射线层析显微镜的高分辨率数据。这是一种超级ct扫描，它将以3D的方式揭示“无颌牙”、牙齿和颌骨的内部微观结构，让我们了解它们是如何生长和被替换的。反过来，这将使我们能够测试有关牙齿发育进化的假设。我们的研究将使我们能够为有颌脊椎动物的出现和辐射提供新的、有力的解释，更重要的是，可以论证的是，一个模型发育模块的进化起源：颌齿系统

More than 99.8% of living vertebrates are gnathostomes (vertebrates with jaws and teeth), and the origin of gnathostomes thus represents one of the most significant episodes in animal evolution. Teeth and jaws are widely held to be the key innovation that underpinned the adaptive radiation of jawed vertebrates, and allowed them to drive their jawless relatives, which had dominated vertebrate communities for the preceding 150 Myr, to extinction. Three recent discoveries challenge this long-cherished hypothesis: (a) 'teeth' evolved before jaws (thus tooth and jaw origin was not coordinated); (b) all lineages of jawed vertebrates were primitively toothless, and each evolved teeth independently; and (c) a major revision of evolutionary relationships of the most primitive jawed vertebrates has overturned the long established view that two principal groups of extinct primitive jawed vertebrates - placoderms and acanthodians - are in fact many different groups that are related by degree to the living jawed vertebrates - sharks and bony fishes (that latter including our own evolutionary lineage). This is not merely a phylogenetic nicety: it reveals a protracted and sequential construction of the bodyplan of crown-gnathostomes, including the assembly of the supposed evolutionary innovation of jaws and teeth. The impact of these discoveries is felt well beyond evolutionary biology because teeth are a core model for understanding the general principles of organ development, and these theories rely heavily upon the assumption that all vertebrate teeth evolved from a common ancestor and that sharks can be taken to represent the primitive condition. This no longer appears to be the case and our understanding of the evolution of this model organogenic system is in disarray. Thus, we are faced with a major shift in our understanding, requiring a complete reformulation of explanations of the origin of jawed vertebrates, but existing data are not up to the job. We know nothing concerning the function of 'teeth' in jawless vertebrates, and feeding in toothless jawed vertebrates has not been the subject of critical analysis. How feeding in later, toothed representatives of each lineage compared is unknown and, as a consequence, so is the ultimate cause of the gnathostome radiation. Furthermore, we do not even know when the radiation occurred: coincident with the origin of jaws, with the later convergent acquisition of teeth, or neither? We do not even know confidently whether the new hypothesis of convergent tooth evolution is correct, because there are no comprehensive evolutionary trees that test whether toothless forms appeared near the base or higher up within gnathostome lineages, and our initial investigations have revealed that these 'toothless' forms appear to possess kosha teeth. We propose to tackle this problem through an innovative multidisciplinary research programme combining the unique and complementary expertise of the four investigators with cutting edge, hi-tech methods. Existing hypotheses of jaw and tooth function among extinct jawless and basal jawed vertebrates will be tested using tooth microwear analysis, which provides direct evidence of how vertebrates ate and the nature of their food. We will use sophisticated and powerful computer models to determine how jaws and teeth were engineered to fit their function. These models will use high-resolution data from advanced Synchrotron Radiation X-ray Tomographic Microscopy. A kind of super-CAT-scanning, this will reveal in 3D the internal microstructure of 'jawless teeth', teeth and jaws, allowing us to understand how they grew and were replaced. This in turn will allow us to test hypotheses concerning the evolution of tooth development. Our research will allow us to provide new, robust explanations for the emergence and radiation of jawed-vertebrates and - arguably more importantly - the evolutionary origin of a model developmental module: the jaw-tooth system