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Evolution of jaws and teeth - new insights into key innovations and the origin of Gnathostomes

Final Report Summary - TOOTHJAW (Evolution of jaws and teeth - new insights into key innovations and the origin of Gnathostomes)

The emergence of jawed vertebrates (gnathostomes) is a pivotal event in vertebrate evolution, based on the evolution of jaws with teeth, to represent a key vertebrate innovation, allowing jawed vertebrates to outcompete their jawless rivals. Recent discoveries however, shed a different light on the evolution of teeth and jaws: tooth-like structures were found on gill arches in a primitive jawless vertebrate, indicating that teeth evolved prior to jaws; and the first jawed vertebrates appear to be toothless. These data demonstrate that tooth and jaw evolution were not coordinated, contradicting previous scenarios.

Among living gnathostomes, the two major groups are chondrichthyans (shark, rays) and osteichthyans (bony jawed vertebrates). We lack insight into the development of teeth and jaws in early osteichthyans. Our current knowledge is based only on two members of this group, representing two important laboratory models: the zebrafish, an actinopterygian, and mouse, a sarcopterygian tetrapod. However, zebrafish and Mouse are derived osteichthyans, and not representative the early osteichthyans.

The question of how vertebrate jaws and teeth evolved is best answered in a multidisciplinary approach, providing necessary phylogenetic and developmental context to interpret data from basal osteichthyans. Only then can we find new hypotheses of how complex modules evolved. My proposed project offers a rare opportunity to investigate evolution and assembly of a jaws and teeth. A pivotal part of this project will employ cutting edge 3D imaging techniques to analyze fossil data, essential because organisms in which these modules first evolved are long extinct. Only data fossil jawed vertebrates can answer the specific question of how jaws and teeth evolved, fundamental to understanding jawed vertebrate origins, and thus, our own evolution.

Objective 1. What is the phylogenetic distribution of developmentally tooth-like structures among early osteichthyans?
Objective 2. How did tooth patterning change among stem-osteichthyans, early actinopterygians and early sarcopterygians?
Objective 3. What is the relationship between changes in tooth-function and tooth-patterning during early evolution of gnathostomes?

Work performed:
To address the above mentioned objectives, I generated 3D data from fossil specimens (basal actionpterygian and osteichthyan taxa) using Micro-CT scanning models at the Natural History Museum imaging facility. For comparison with extant taxa, I used the laboratory model Zebrafish Danio rerio, and the basal actinopterygian Polypterus senegalus. I obtained SRXTM models for and Polypterus senegalus embryonic and larval stages that cover tooth development, at the SLS synchrotron in Switzerland.

Polypterus senegalus occupies a unique phylogenetic position at the base of the actinopterygian clade, and retains many ancestral features, such as an scales and dermatocranium sharing components with teeth: dentin, enameloid, a pulp cavity and a bony base of attachment. Therefore, we compared tooth development to that of body scales and dermal skull bones in Polypterus.

After the first 24 months of the project, all 3D models have been computationally segmented and tooth development has been analysed in Polypterus, Danio and the fossils Raynerius, Cheirolepis and Onychodus. Additionally, dermatocranium and dermal scales in Polypterus were analysed and compared to tooth development.

We compared gene expression patterns for a selection of genes known to be involved in tooth development, to those in scale development. I travelled to Prague to carry out wet lab work in Dr. Robert Cerny’s lab at Charles University in Prague. I obtained useful gene expression data for tooth and dermatocranium development, but not for scale development since the selected larvae were slightly too young. This wet lab work provided preliminary data for further studies.

1) Formation of the oral dentition in Polypterus is very different to that of sharks, which have been studied intensively in relation to tooth evolution. Oral dentition development initiates in the lower jaw first; in the upper jaw slightly later. Teeth are added in a zig-zag pattern in between teeth already anchored in the jaw bones.
2)) Replacement teeth develop all at approximately the same time, when the formation of jaw is nearly complete. Their location is slightly posterior and medial to the functional teeth; they are visible as a series of small enameloid cones at a small distance from the jaw bones (not yet anchored to the jaw bones).
3) Development of teeth, integumental skeleton and dermatocranium are slightly different in timing, but very similar processes.
4) Development of the integumental skeleton and dermatocranium are not controlled by odontodes (dental structures) as suggested in the classical patterning theories. The osteogenic compartment of the integumental skeleton and dermatocranium was always considered a mere rudiment, but it appears to play an important role in formation of these structures.
5) Additionally, we produced four dimensional data of integumentary skeleton, and dermatocranium development in Polypterus senegalus. These data are valuable for assessing the classical theories of tooth evolution, as well as dermal skeleton formation. Our developmental data show that evolution of development of integumentary skeleton and dermatocranium is not controlled by odontogenic tissues, as assumed by the classical patterning theories.
6) We produced a four dimensional developmental series of pharyngeal dentition in Danio rerio, an important model species in biomedical studies. These data will be compared to those of Polypterus senegalus and to the fossil specimens.
7) In collaboration with another research group, we compared enameloid and other enamel-like tissues in a large number of fossil taxa (chondrichthyans, osteichthyans, placoderms, acanthodes and ostracoderms) from literature, and applied phylogenetic analyses to reconstruct the ancestral state and the evolution of enameloid and enamel-like structures.

This project will form the foundation for all future work on evolution of dentitions in Osteichthyans, also providing insight in our own evolution, and the general principles of development.