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Development of teeth and jaws in the earliest jawed vertebrates

Abstract

Teeth and jaws constitute a model of the evolutionary developmental biology concept of modularity1 and they have been considered the key innovations underpinning a classic example of adaptive radiation2. However, their evolutionary origins are much debated. Placoderms comprise an extinct sister clade3 or grade4,5 to the clade containing chondrichthyans and osteichthyans, and although they clearly possess jaws, previous studies have suggested that they lack teeth6,7,8, that they possess convergently evolved tooth-like structures9,10,11 or that they possess true teeth12. Here we use synchrotron radiation X-ray tomographic microscopy (SRXTM)13 of a developmental series of Compagopiscis croucheri (Arthrodira) to show that placoderm jaws are composed of distinct cartilages and gnathal ossifications in both jaws, and a dermal element in the lower jaw. The gnathal ossification is a composite of distinct teeth that developed in succession, polarized along three distinct vectors, comparable to tooth families. The teeth are composed of dentine and bone, and show a distinct pulp cavity that is infilled centripetally as development proceeds. This pattern is repeated in other placoderms, but differs from the structure and development of tooth-like structures in the postbranchial lamina and dermal skeleton of Compagopiscis and other placoderms. We interpret this evidence to indicate that Compagopiscis and other arthrodires possessed teeth, but that tooth and jaw development was not developmentally or structurally integrated in placoderms. Teeth did not evolve convergently among the extant and extinct classes of early jawed vertebrates but, rather, successional teeth evolved within the gnathostome stem-lineage soon after the origin of jaws. The chimaeric developmental origin of this model of modularity reflects the distinct evolutionary origins of teeth and of component elements of the jaws.

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Figure 1: Evolutionary relationships of principal groups of vertebrates.
Figure 2: Lower-jaw element of Compagopiscis croucheri , Late Devonian period, Australia.
Figure 3: Virtual development of a Compagopiscis croucheri lower jaw, Late Devonian period, Australia.
Figure 4: Histological comparison of the Compagopiscis croucheri cusps on jaws, dermal bone and postbranchial lamina, with the jaws and pectoral fins of the antiarch Bothriolepis species, both Late Devonian, Australia, and the jaw of a buchanosteid arthrodire, Early Devonian, Saudi Arabia.

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Acknowledgements

We thank S. Bengtson, J. Cunningham, D. Murdock, S. Giles and A. Hetherington for help at the TOMCAT beamline; K. Robson-Brown for help at the Micro-CT, and H. Lélièvre and G. Clément for loan of specimens. The study was funded by EU grant FP7 MC-IEF (to M.R. and P.C.J.D.), Australian Research Council Grant DP 110101127 (to Z.J. and K.T.), Natural Environment Research Council grant NE/G016623/1 (to P.C.J.D.) and the Paul Scherrer Institut (P.C.J.D.).

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M.R., P.C.J.D. and Z.J. conceived the project. K.T. acid-prepared WAM specimens. M.R., P.C.J.D., F.M. and M.S. collected the data. M.R. analysed the data. All authors contributed to the interpretation of the data and the writing of the manuscript.

Corresponding authors

Correspondence to Martin Rücklin or Philip C. J. Donoghue.

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The authors declare no competing financial interests.

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Rücklin, M., Donoghue, P., Johanson, Z. et al. Development of teeth and jaws in the earliest jawed vertebrates. Nature 491, 748–751 (2012). https://doi.org/10.1038/nature11555

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