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Jaws emerge: Insight from placoderms to resolve the evolutionary emergence of gnathostomes

Final Report Summary - JAWS EMERGE (Jaws emerge: Insight from placoderms to resolve the evolutionary emergence of gnathostomes)

The origin and early evolution of vertebrates is thought to have been underpinned by two factors: new embryological cell populations that were capable of producing skeletal tissues and a trend towards increasingly active food acquisition. Both phenomena culminated in the origin of predators with the coordinated key innovations of teeth and jaws, laying the foundation for the adaptive radiation on which extant vertebrate biodiversity is based. This thesis has been challenged by recent discoveries. Therefore we set out to test the recent hypotheses that tooth-like structures in jawless vertebrates predate the origin of jaws and that teeth are present in basal jawed vertebrates, the placoderms.

Using X-ray microtomography and synchrotron radiation X-ray tomographic microscopy, we studied the development of the structures. We reveal that the supposed tooth-like structures associated with the gill arches in the primitive jawless vertebrate Loganellia scotica are internal scales, which are organised into fused patches and rows. They grow along a particular vector and therefore are different to the discrete external scales. This sequential development differs to tooth whorls of jawed vertebrates in slight curvature and opposite sequence of addition of the scales. The test of the phylogenetic distribution of these internal scales and teeth in vertebrates indicates that they represent rather a convergence than the establishment of the developmental pattern of teeth in jawed vertebrates. The available evidence suggests that internal odontodes evolved through the expansion of odontogenic competence from external to internal epithelia.

The controversially discussed occurrence of teeth in derived members of the earliest jawed vertebrates, the placoderms, is tested. Morphologically these are teeth possessing dentine and a pulp-cavity, in a developmental view these are teeth in one row. Against traditional hypotheses our data suggests that teeth are added sequentially in rows like in ischnacanthid acanthodians, lungfish and basal chondrichthyans. Therefore, this evidence suggests that teeth in vertebrates developed in a row from a transitional epithelial lamina. This type of tooth addition corresponds to the replacement in teleost fish such as salmon or zebrafish. This suggests that teeth developed in a shallow folding of the epithelial lamina and not in a shark-like permanent deep dental lamina. Against recent hypotheses the jaws of derived placoderms are formed of separate ossifications. This is unique and will bear future evidence for the modular development of jaws and the homology of ossifications in jawed vertebrates. The test of functional differences during ontogeny shows that jaws receive relatively less stress and get therefore relatively more stable during their life history. Together with the wear of the first teeth and the development of a wear-facet this suggests a change of function during development. The micro-wear analysis of early ontogenetic stages and therefore probably juvenile specimens, show smooth surfaces comparable to recent fish, feeding on non-abrasive food items.

Teeth evolved probably with jaws in placoderms and the recent hypothesis that teeth developed before jaws is not evident from our data. Therefore the radiation of vertebrates is linked to the modular evolution of jaws and teeth.

This first combined study using the three lines of evidence: development, function and ecology to test hypotheses around the evolution of jaws and teeth bears the potential to have a great influence on palaeobiology, evolutionary biology and developmental genetics. This holistic approach is applied and continued in the successive NERC-project: teeth and jaws.