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

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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