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

Lead Research Organisation: University of Bristol
Department Name: Earth Sciences

Abstract

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

Publications

10 25 50
 
Description Our key findings to date are:



1. Resolving the primitive nature of teeth and jaws in vertebrates, including the composition of the jaw in the earliest jawed vertebrates, resolution of debate over the absence/presence of teeth placoderms did indeed possess teeth) and elucidation of their tooth replacement pattern.



2. Demonstration that the pharyngeal tooth-like scales of jawless thelodonts did in deed develop and were replaced like true teeth, but that they evolved convergently on vertebrate teeth; they are not an early manifestation of teeth before jaws.



3. Findings 1+2 above have allowed us to reject the hypothesis that teeth evolved before jaws, representing a distinct skeletal system from that of the dermal skeleton. Rather, we find evidence that teeth evolved long after the dermal skeleton, presumably through extension of the odontogenic capacity of the external dermis to the internal dermis and endoderm.



4. Our functional analyses have demonstrated that the ecological diversity of vertebrates increased dramatically after the origin of jaws, soon adopting much of the ecological diversity that we see currently in marine/ fresh water vertebrates.
Exploitation Route None obvious We have exploited these results so far through publication in the leading journals Nature and Evolution & Development.
Sectors Education,Environment

URL http://palaeo.gly.bris.ac.uk/donoghue/
 
Description Swiss Light Source, non PX Beamlines
Amount SFr. 448,000 (CHF)
Organisation Paul Scherrer Institute 
Sector Academic/University
Country Switzerland
Start 01/2015 
End 07/2016
 
Title Data from 'Apparatus architecture of the conodont Nicoraella kockeli (Gondolelloidea, Prioniodinina) constrains functional interpretations' 
Description Data from: Jinyuan Huang, Carlos Martínez-Pérez, Shixue Hu, Qiyue Zhang, Kexin Zhang, Changyong Zhou, Wen Wen, Tao Xie, Michael J. Benton, Zhong-Qiang Chen, Mao Luo and Philip C. J. Donoghue. 2019. Apparatus architecture of the conodont Nicoraella kockeli (Gondolelloidea, Prioniodinina) constrains functional interpretations. Palaeontology. This dataset is composed of three dimensional models of component elements and an architectural model of the skeletal apparatus of the conodont Nicoraella kockeli, based principally on tomographic data from an articulated skeletal assemblage (pm028-18-wy1-C1) from the Middle Triassic Luoping Biota, Yunnan Province, southwestern China; reconstruction of the apparatus architecture was supplemented by additional fused clusters also characterised by synchrotron X-Ray tomographic microscopy. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
URL https://data.bris.ac.uk/data/dataset/p515kyhwv3ec29zo7an2psqju/
 
Title Data from Dhanda et al. (2018) The apparatus architecture of Erismodus quadridactylus and its implications for the prioniodinin apparatus bauplan. Papers in Palaeontology 
Description Tomographic data and associated computed tomographic models. Tom Davies is Deputy Data Steward. 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
 
Title Data from Ferrón et al. 2020. Computational Fluid Dynamics Suggests Ecological Diversification among Stem-Gnathostomes. Current Biology. 
Description This dataset contains COMSOL Multiphysics files including computational fluid dynamics analyses on three dimensional models of eight taxa of Osteostraci (i.e., Boreaspis, Cephalaspis, Hemicyclaspis, Holeaspis, Kiaeraspis, Spatulaspis, Stensopelta, and Tremataspis). Tom Davies is Deputy Data Steward. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL https://data.bris.ac.uk/data/dataset/1bjnv53uzx5dm2nw0q2tdtbqji/
 
Title Data from Gai et al. (2019) The head circulatory system of Galeaspida (Vertebrata; stem-Gnathostomata) revealed by synchrotron X-ray tomographic microscopy. Palaeoworld 
Description This dataset contains six dimensional synchrotron x-ray (SRXTM) and one microfocus (XTM) datasets and computed tomographic datasets from seven galeaspid neurocrania from the Maoshan Formation (late Llandovery to early Wenlock, Silurian) of Zhejiang, China. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
 
Title Data from O'Shea et al. The dermal skeleton of the jawless vertebrate Tremataspis mammilata (Osteostraci, stem-Gnathostomata) 
Description Synchrotron x-ray tomographic datasets of the dermal skeleton of Tremataspis mammillata from the Middle Silurian of Saaremaa, Estonia Tom Davies is Deputy Data Steward. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
 
Title Data: Response to "placoderms and the evolutionary origin of teeth" 
Description X-ray tomographic slice data of recent chondrichthyan teeth. 
Type Of Material Database/Collection of data 
Year Produced 2016 
Provided To Others? Yes  
 
Title Histology and affinity of anaspids, and the early evolution of the vertebrate dermal skeleton 
Description Synchrotron x-ray tomographic datasets of anaspid scales. Keating, J. N. & Donoghue, P. C. J. 2016. Histology and affinity of anaspids, and the early evolution of the vertebrate dermal skeleton. Proceedings of the Royal Society B. 
Type Of Material Database/Collection of data 
Year Produced 2016 
Provided To Others? Yes  
 
Title Romundina and the evolutionary origin of teeth 
Description X-ray tomographic slice data of early vertebrate tooth plates and scales. 
Type Of Material Database/Collection of data 
Year Produced 2015 
Provided To Others? Yes  
 
Title Translating taxonomy into the evolution of conodont feeding ecology 
Description Synchrotron x-ray tomographic analyses of the Polygnathus xylus xylus clusters and the derived 3D models. 
Type Of Material Database/Collection of data 
Year Produced 2016 
Provided To Others? Yes