Gnathostome dental pattern and the evolution of chondrichthyan dentitions

Lead Research Organisation: The Natural History Museum
Department Name: Earth Sciences

Abstract

One of the most significant vertebrate innovations was the evolution of jaws, and on these jaws, teeth arranged into functional dentitions. These dentitions allowed vertebrates to radiate into a number of major groups, including sharks (Chondrichthyes) and bony fishes (Osteichthyes). Along with these are a variety of fossil groups whose dentitions have been difficult to understand and interpret. Because these fossil groups are closer to the origin of jaws and teeth, it is crucial that we try to better understand how their dentitions evolved.

One way to do this is to study how the dentitions of living groups developed and then apply these observations, as far as possible, to the development of dentitions in fossil taxa. The group Osteichthyes includes well-known fish such as the tuna, salmon, seahorse, coelacanth, lungfish and also tetrapods. Osteichthyan dentitions have been intensely studied in recent years, and we even understand what genes are involved in producing these dentitions. Despite this, even within this group we know nothing about tooth development of more primitive osteichthyans, such as the paddlefish and gar. As well, and perhaps somewhat surprisingly, we know very little about how genes control development of shark and ray dentitions. The goal of our project is to study development in a broad range of chondrichthyans to find common developmental characters of these dentitions that can be compared to osteichthyan dentitions and in the future, to the more primitive, problematic fossil taxa.

Shark teeth are plentiful in the fossil record and features they show are important in identifying different species. Chondrichthyans show a wide variety of dentitions, ranging from large numbers of almost microscopic teeth along the jaw (in filter-feeding sharks such as Rhincodon, the Whale shark), to the pavement-like dentition in rays, to a dentition in which teeth change along the jaw from biting to crushing (Heterodontus, the Port Jackson shark). This diversity has made it difficult to find common patterns of dentition development that could be used to compare to the problematic fossil vertebrates mentioned above. Sharks and rays also possess other 'tooth-like' structures such as the gill rakers in the filter-feeding basking shark Cetorhinus and 'teeth' along the rostrum of sawfish and sawsharks.

Our project will study specimens of a wide range of modern sharks and rays of different growth stages in order to investigate the patterns of tooth development within the jaws and changes in the number and shape of teeth during growth. A number of exceptionally well-preserved fossils will also be studied in order to place the modern forms within a wider context within the Chondrichthyes. Additionally, we will study embryos of a shark, ray and a basal bony fish and will record the genes controlling their tooth development that will allow us to compare underlying mechanisms of the formation of teeth in all vertebrates.

Planned Impact

1) Academic Beneficiaries: see 'Academic Beneficiaries' page.
2) Citizen Scientists: Shark teeth/dentitions have a high degree of interest among amateur collectors/researchers. In the fossil fish collections at the Natural History Museum, London (NHM), shark teeth represent a large portion of donations to the collection, and general enquiries. This is due to the easy availability of relevant shark-bearing geological formations outside London. Our work will be of interest to these citizen scientists as it will provide new characters to help them identify and classify their fossil finds, and illustrate a new aspect to their fossils (ontogeny, or how teeth/dentitions develop through growth) that they may not have considered. In this way, our project will contribute to increasing public awareness and understanding of scientific issues. We will develop an outreach/learning packet that can be modified to meet the needs of these beneficiaries; our team members will use these and each plan to attend one internal (e.g., NHM Nature Live), and two external UK events per year of the grant, to better disseminate our research and increase the impact of our work (see role of 'virtual palaeontology', below). We can also reach citizen scientists via NHM websites such as 'Nature Plus' (http://www.nhm.ac.uk/natureplus/index.jspa) and KEEmu, where we can blog project progress, including strong visuals such as reconstructed CT-scans, histological images, gene expression results, etc.
3) Students (schools) and adult education: These beneficiaries will overlap with 'citizen scientists', but we will modify our outreach events to maximize our impact with these beneficiaries. After initial discussions, we could tailor our outreach packet for individual schools and curricula. For example, we would be more specimen-oriented (Recent shark jaws, histological slides, cleared and stained specimens) for a biology class. For a class interested in the technological side of our research, we could focus on CT-scanning (using images and videos on a portable laptop) and 3-D rapid prototyping (both aspects of outreach and education via 'virtual palaeontology', Rahman et al., 2012. Evo Edu Outreach DOI 10.1007/s12052-012-0458-2). By disseminating our results in this flexible, adaptive way, we will contribute to the scientific culture in the UK and Europe. Students could also access websites as above.
4) Museums, galleries and aquaria: Given the wide public interest in shark teeth/dentitions, our work will be beneficial to museums and galleries that may be able to incorporate our results into exhibitions or for use in museum talks or public engagement. For example, PI Johanson regularly contributes to NHM public engagement via 'Nature Live', 'Science Uncovered' and 'A-levels' schools programme. Project Partner Sansom has already liaised with the Sea Life Centre in Birmingham such that we will provide them a version of our outreach to use. The Sea Life Centre has a network throughout Europe providing opportunities for outreach in continental Europe as well (targeting facilities in Germany).
5) Staff working on this project: Staff will acquire important skills from either CT-scanning (NHM, KCL), including using the software needed to structurally render this data, or, analysis of gene expression patterns via in situ hybridization. These are highly mature technologies and used in a wide variety of research programs involving both fossil and extant specimens. In this way, our project will train and deliver highly skilled researchers and technicians. Additionally, the PDRA (Sheffield) will travel to the lab of Project Partner Marcus Davis (Kennesaw State University), having the opportunity to develop their skills and interact in a new lab environment. Our timeline suggests these benefits acrue within the first year with respect to the CT-scanning, and within the first two years for the molecular work.

Publications

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Johanson Z (2017) Paleobiology: A Tooth for a Tooth. in Current biology : CB

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Martin KJ (2016) Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles. in Proceedings of the National Academy of Sciences of the United States of America

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Thiery AP (2017) Spatially restricted dental regeneration drives pufferfish beak development. in Proceedings of the National Academy of Sciences of the United States of America

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Underwood C (2016) Sclerorhynchus atavus and the convergent evolution of rostrum-bearing chondrichthyans in Geological Society, London, Special Publications

 
Description Our grant focuses on the dentition of sharks and rays, particularly how teeth are organized into the highly functional dentitions of these animals. We have published our results on the ray dentition, and have three papers published on the unusual teeth on the extended rostrum of sawfish and sawsharks- are these true teeth? We have also published a paper on the dentition of the primitive ray-finned fish, the bichir, for comparison to the sharks and rays. We find that there are common patterns of development and gene expression early in development among these major groups, with modifications for functional feeding only as the animal develops and approaches adulthood. New papers explore the relationship between shark tooth development and taste buds, suggesting that genes associated with taste buds inside the mouth are utilized in tooth development. Additionally, we believe that our work on the sawshark rostrum suggests the presence of a discrete area on the shark skull that controls, in a coordinated fashion, development of the rostrum and teeth. We are now focusing on dentition development in sharks, and our new paper on the squaliform sharks demonstrates early in development, this major group adds teeth in an alternate pattern along the jaw (as in rays), but that in adults, this pattern becomes substantially modified. This shift is responsible for a large component in shark dentition diversity and are writing a paper on the other major clade of interest, the lamniforms. The latter will be a major review paper, tying together all data obtained during the course of this grant. After this, we will have described dentition development in the majority of chondrichthyans, for comparison to other jawed vertebrates, including fossil forms near the base of the jawed vertebrate clade.
Exploitation Route We now have a better understanding of how elasmobranch chondrichthyan dentitions develop, including work from colleague Gareth Fraser on the genes involved. The other major chondrichthyan clade, the Holocephali, is of high research interest at the moment; our results will be of researchers studying dentitions in the Holocephali (including CI Johanson). Our results will also be of interest to researchers studying the origins and evolution of the jawed vertebrate dentition, as we are now able to provide data from one of the major vertebrate clades (Chondrichthyes).
Sectors Education,Environment,Culture, Heritage, Museums and Collections,Other

URL http://chondrichthyes.myspecies.info/
 
Description As outlined in our Portfolio, our findings have been presented on a number of websites, and as part of a number of outreach events. We are also providing our CT-scan images to groups such as ProSea http://www.prosea.info/, and will continue to do so in the future, even after our NERC grant is completed.
First Year Of Impact 2014
Sector Education,Environment,Culture, Heritage, Museums and Collections
Impact Types Cultural,Societal

 
Description Evolution and Development of chondrichthyan dentitions 
Organisation University of Vienna
Country Austria 
Sector Academic/University 
PI Contribution Chondrichthyan specimens, data including CT-scans, rendered CT-scans, images
Collaborator Contribution Chondrichthyan specimens including rare taxa from partner's Japanese colleague, data including CT-scans, rendered CT-scans
Impact Royal Society International Exchange grant submitted, in review Rendered CT-scans of fossil material to be used in upcoming publication and Society of Vertebrate Paleontology, Berlin (2014)
Start Year 2014
 
Description Gnathostome dental pattern and the evolution of chondrichthyan dentitions: NHM scratchpad 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Our NHM scratchpad (http://chondrichthyes.myspecies.info/) is currently our main webpage to disseminate information about our project, including images, upcoming events, and relevant publications. We also will store published data here. Our current research assistant will be developing another website to link to this, to increase our outreach potential.

This is our main portal to disseminate information to the public and scientific researchers.
Year(s) Of Engagement Activity 2014
URL http://chondrichthyes.myspecies.info/
 
Description Attend Lyme Regis Fossil Festival 29 April- 1 May 2016. Manned a table with team members CU and BC, presenting our research (including movies of CT-scans on screen) to the general public. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Manned a table in the Natural History Museum tent, engaged with public with handling specimens of shark dentitions, along with movies of shark dentitions generated from our CT-scans. Engagement involved answering questions and discussion of our research and our impact. Ability to handle actual shark jaws brought people to our table for engagement, impact include a better appreciation of shark diversity among the general public, an increased appreciation of sharks and their potential for research. Appreciation of new technologies (CT-scanning) used in research. BC developed his presentation skills and ability to interest the public in scientific research.
Year(s) Of Engagement Activity 2016
 
Description Attend Open Day, Thomas Hardye School, Dorchester, with BC. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Manned a table at Thomas Hardye School, Dorchester April 28, 2016, with NERC-funded assistant BC. Engaged students in our research with handling specimens and movies derived from CT-scans. This generated questions and discussions about scientific research in general and our research in particular, also the possibility of science as a career. BC developed his presentation skills, particularly with respect to engaging students. Survey conducted at the end of the day demonstrated positive response to our presentation.
Year(s) Of Engagement Activity 2016
 
Description Blast from the Past, Isle of Wight 12-13 November 2016, with team members CU and BC. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Manned a table, with handling specimens of shark dentitions and movies generated from our CT-scan data, at the Dinosaur Isle Museum, Isle of Wight. Outcomes include engagement with general public and students to educate them about sharks and shark diversity, increase presentation skills of NERC-funded assistant BC, and support regional museum by generating public interest in Dinosaur Isle. Team members also made presentations at an evening event held for 'Friends of Dinosaur Isle Museum', promoting our research and supporting this group.
Year(s) Of Engagement Activity 2016
 
Description British Science Association Science Festival (presentation) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Attend British Science Festival Swansea, gave presentation "The new backbone of marine research" with our NERC-funded assistant BC. Presentation made to general public, approximately 40 people attended with questions and discussions afterwards. BC presented technical aspects of our research (CT-scanning), providing him with valuable experience in presenting skills.
Year(s) Of Engagement Activity 2016
 
Description Meeting with Victoria Bendall, Cefas, Lowestoft, to collect porbeagle skulls for research, and to discuss our project 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Other audiences
Results and Impact We met with Victoria Bendall (Cefas) to dissect and remove porbeagle heads and dentitions for our research. CT-scans of this material have been used for Science Uncovered (2015) and in recent team outreach (http://www.nhm.ac.uk/our-science/science-news/2016/february/shark-genes-could-grow-new-human-teeth.html) (https://www.sheffield.ac.uk/news/nr/shark-teeth-human-tooth-loss-study-1.548598). We plan to arrange a more formal outreach event with Victoria and Cefas later in 2016.
Year(s) Of Engagement Activity 2015
 
Description NERC 50th anniversary celebrations 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact I engaged with students and presented our research on chondricthyan dentitions at this NERC event, with shark specimens from our learning/teaching collection, and movies from 3D volume rendered CT-scans of shark dentitions, shown on my laptop.
Year(s) Of Engagement Activity 2015
 
Description Science Uncovered 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Science Uncovered is a research event sponsored by the EU, and attracts a large number of visitors. Our team had a table, laptop and large screen, where we discussed our project on evolution of shark dentitions, using our teaching/learning collection of shark jaws, as well movies from our 3D volume rendered CT-scans of a variety of chondrichthyan dentitions.
Year(s) Of Engagement Activity 2015
 
Description Science Uncovered, Natural History Museum 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? Yes
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Our team participated in Science Uncovered, with a table in the 'Evolution' section. Using specimens and a continually running movie showing rendered CT-scans of shark dentitions, we engaged with audiences for several hours on the night.

The 2014 Science Uncovered event attracted over 8500 visitors to the museum. As part of the yearly European night of science, visitors were local and national but also international, giving our research a wide scope. All team members participating felt that our visitors were enthusiastic and engaged with our research project.
Year(s) Of Engagement Activity 2014
 
Description Science Uncovered, Natural History Museum, attended by BC, September 30 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact NERC-funded assistant BC presented our shark research at Science Uncovered (Part of European Researchers' Night), with handling specimens and movies generated from our CT-scans, along with the Image and Analysis Centre, NHM (IAC). This promoted our research, but was also important for BC, as it demonstrated his skills in presenting research and representing our team on his own, to a large number of people; additionally, his close work that evening with the IAC has resulted in contracts with them for work, after our grant ended.
Year(s) Of Engagement Activity 2016
 
Description See saw: evolution and development of the sawfish and sawshark dentitions 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Our grant-funded research assistant presented our research to this public audience at the Natural History Museum, including images and specimens

Public outreach, career development for assistant
Year(s) Of Engagement Activity 2014
 
Description Travel to Sea Life Centre, Birmingham, to meet staff and discuss outreach possibilities. Meet researchers at University of Birmingham, to discuss data sharing 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Industry/Business
Results and Impact We met with staff at the Sea Life Centre, Birmingham, to discuss possible upcoming outreach events in 2015. These would involve our teaching/learning specimens, as well as our movies of volume rendered CT-scans. We also took the opportunity to meet with colleagues at University of Birmingham, to discuss possibilities for sharing data (e.g., shark scales, from our CT-scans).
Year(s) Of Engagement Activity 2015