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

牙齿和颌：模型器官发生系统的进化出现和颌口动物的适应性辐射

• 批准号: NE/G016623/1
• 负责人: Philip Donoghue
• 金额: $ 40.81万
• 依托单位: University of Bristol
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2009
• 资助国家: 英国
• 起止时间: 2009 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FG016623%2F1
• 关键词: Teeth; jaws; evolutionary; emergence; model

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

超过99.8%的现存脊椎动物是颌口类动物(有颌骨和牙齿的脊椎动物)，因此节口类动物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骨脊椎动物适应性辐射的关键创新，并使它们能够将它们没有下巴的亲戚赶到灭绝，而在过去的150英里里，这些亲戚一直主导着脊椎动物群落。最近的三项发现挑战了这一长期珍视的假说：(A)“牙齿”是在颌骨之前进化的(因此牙齿和颌骨的起源不协调)；(B)有颌骨脊椎动物的所有谱系都是原始的无牙齿的，每个谱系都是独立进化的；(C)对最原始的有颌骨脊椎动物的进化关系进行了重大修订，推翻了长期以来确定的观点，即已灭绝的两个主要原始有颌骨脊椎动物--安太皮动物和棘皮动物--实际上是许多不同的群体，与现存的有颌骨脊椎动物--鲨鱼和带骨鱼类--有一定的亲缘关系(后者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度：它揭示了一个旷日持久的、顺序的冠状口目动物的身体结构，包括颌骨和牙齿的所谓进化创新的组装。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这样一个假设，即所有脊椎动物的牙齿都是从一个共同的祖先进化而来的，鲨鱼可以被视为原始状态的代表。这似乎不再是这样的情况，我们对这一模式有机成因系统的演化的理解是混乱的。因此，我们面临着认识上的重大转变，需要彻底重新解释有颌骨脊椎动物的起源，但现有的数据不能胜任这项工作。我们对无颌脊椎动物的“牙齿”功能一无所知，在无牙有颌脊椎动物中进食也不是批判性分析的主题。后来如何进食，每个血统的牙齿代表如何比较是未知的，因此，也是节口辐射的最终原因是未知的。此外，我们甚至不知道辐射是在什么时候发生的：与颌骨的起源一致，与后来汇聚的牙齿获得一致，还是两者都不？我们甚至不确定收敛牙齿进化的新假说是否正确，因为没有全面的进化树来测试无牙形态是出现在下颌骨谱系的底部附近还是更高的位置，我们的初步调查显示，这些没有牙齿的形态似乎拥有考沙牙。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，该计划将四名调查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。已灭绝的无颌骨脊椎动物和基底有颌骨脊椎动物之间的颌骨和牙齿功能的现有假说将通过牙齿微磨损分析进行验证，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设计出来的，以适应它们的功能。这些模型将使用先进的同步辐射X射线断层扫描显微镜的高分辨率数据。这是一种超级CAT扫描，这将在3D中揭示“无颌牙齿”、牙齿和颌骨的内部微结构，让我们了解它们是如何生长和被替换的。这反过来将使我们能够检验有关牙齿发育进化的假设。我们的研究将使我们能够为颌骨脊椎动物的出现和辐射提供新的、强有力的解释--可以说更重要的是--一个模型发育模块的进化起源：颌齿系统

项目成果

Increasing morphological disparity and decreasing optimality for jaw speed and strength during the radiation of jawed vertebrates.

• DOI: 10.1126/sciadv.abl3644
• 发表时间: 2022-03-18
• 期刊: Science advances
• 影响因子: 13.6
• 作者: Deakin WJ;Anderson PSL;den Boer W;Smith TJ;Hill JJ;Rücklin M;Donoghue PCJ;Rayfield EJ
• 通讯作者: Rayfield EJ

X-ray nanotomography and electron backscatter diffraction demonstrate the crystalline, heterogeneous and impermeable nature of conodont white matter.

• DOI: 10.1098/rsos.202013
• 发表时间: 2021-08
• 期刊: Royal Society open science
• 影响因子: 3.5
• 作者: Atakul-Özdemir A;Warren X;Martin PG;Guizar-Sicairos M;Holler M;Marone F;Martínez-Pérez C;Donoghue PCJ
• 通讯作者: Donoghue PCJ

EARLY VERTEBRATE EVOLUTION

• DOI: 10.1111/pala.12125
• 发表时间: 2014-09-01
• 期刊: PALAEONTOLOGY
• 影响因子: 2.6
• 作者: Donoghue, Philip C. J.;Keating, Joseph N.
• 通讯作者: Keating, Joseph N.

The apparatus composition and architecture of Erismodus quadridactylus and the implications for element homology in prioniodinin conodonts

• DOI: 10.1002/spp2.1257
• 发表时间: 2019-05
• 期刊: Papers in Palaeontology
• 影响因子: 2.3
• 作者: R. Dhanda;D. Murdock;J. Repetski;P. Donoghue;M. P. Smith