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

超过99.8%的现存脊椎动物是有颌类（有颌和牙齿的脊椎动物），因此有颌类的起源代表了动物进化中最重要的事件之一。牙齿和颌骨被广泛认为是支撑有颌脊椎动物适应性辐射的关键创新，并使它们能够驱使它们的无颌亲戚灭绝，这些亲戚在之前的1.5亿年里一直统治着脊椎动物群落。最近的三项发现挑战了这一长久以来的假设：（a）“牙齿”在颌骨之前进化（B）所有有颌脊椎动物谱系都是无牙的，并且每个谱系都独立地进化出牙齿;以及（c）对最原始的有颚脊椎动物进化关系的一次重大修订推翻了长期以来的观点，即两个主要的灭绝的原始有颚脊椎动物群，脊椎动物--盾皮动物和棘皮动物--实际上是许多不同的类群，它们在一定程度上与现存的有颚脊椎动物--鲨鱼和硬骨鱼--有亲缘关系（硬骨鱼包括我们自己的进化谱系）。这不仅仅是一个系统发育的精确性：它揭示了冠颚类动物的身体平面的长期和连续的构造，包括颌骨和牙齿的假定进化创新的装配。这些发现的影响远远超出了进化生物学，因为牙齿是理解器官发育一般原理的核心模型，这些理论在很大程度上依赖于所有脊椎动物牙齿都从共同祖先进化而来的假设，鲨鱼可以代表原始状态。这似乎不再是这种情况下，我们的理解这个模型器官系统的演变是混乱的。因此，我们面临着一个重大的转变，我们的理解，需要一个完整的重新解释的起源有颚脊椎动物，但现有的数据是不够的工作。我们对无颌脊椎动物的“牙齿”的功能一无所知，而无齿有颌脊椎动物的进食也没有成为批判性分析的主题。如何喂养在以后，牙齿的代表，每一个血统的比较是未知的，因此，是最终原因的颚口辐射。此外，我们甚至不知道辐射是什么时候发生的：与颌骨的起源一致，与后来的牙齿会聚采集一致，还是两者都不一致？我们甚至不能肯定地知道趋同牙齿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形式是否出现在有颚动物谱系的基部附近或更高的位置，我们的初步调查显示，这些“无牙”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来解决这个问题，该计划将四名研究人员的独特和互补的专业知识与尖端的高科技方法相结合。现有的假设颌骨和牙齿功能之间灭绝无颌和基颌脊椎动物将使用牙齿微磨损分析，这提供了直接的证据，脊椎动物吃和他们的食物的性质进行测试。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的同步辐射X射线层析显微镜的高分辨率数据。这是一种超级CAT扫描，它将以3D方式揭示“无颌牙齿”、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替换的。这反过来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，强有力的解释，而且-可以说更重要的是-一个模型发育模块的进化起源：颌骨-牙齿系统

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