Skull evolution and the terrestrialization and radiation of tetrapods

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

Abstract

Our proposal brings together world class expertise and cutting-edge methods to answer a key question in the history of life: how did vertebrates conquer the land? We address this question by testing four key hypotheses derived from long-standing assertions that selection acted upon the skull to drive adaptations for improved terrestrial feeding during the water to land transition. Our methods offer a means to shift away from analogy-driven assertions of evolutionary history towards rigorous testable hypotheses founded upon mechanical principles, and will set a benchmark for future studies in evolutionary biomechanics.

For the first 200 million years of their history, vertebrates lived an aquatic existence. Between 385 and 350 million years ago they evolved a host of anatomical features that ultimately enabled vertebrates to conquer land. This reorganization of the vertebrate skeleton created the basic tetrapod body plan of a consolidated head with mobile neck, arms and legs with digits and air breathing lungs. This plan has persisted, subject to modification, ever since and is shared by all terrestrial vertebrates. It was proposed over 50 years ago that tetrapods modified their skull bones and jaw muscles to create a stronger and 'more efficient' structure, capable of forceful biting for feeding on land. This reorganization is seen as key to their subsequent radiations, enabling tetrapods to expand into new ecological niches by feeding on terrestrial plants, large prey and hard or tough food. It has been proposed that these modifications came at the cost of reduced hydrodynamic efficiency and a slower bite, and could only be achieved by the loss of suction feeding and the evolution of rib-based breathing, thus freeing the skull from its roles in aquatic locomotion, drawing prey into the mouth and pumping air into the lungs.

These ideas have been perpetuated in textbooks for decades, yet are based on out-dated simple line drawings of skulls and jaw closing muscles, and remain to be tested. We now have a rich and informative fossil record that documents changes in skull shape across the water to land transition. However, until now, we have lacked the means to test these hypotheses in a quantitative, rigorous way. In this proposal we will determine how changes in skull form and function enabled vertebrates to feed in a terrestrial environment and document the sequence of evolutionary changes and trade-offs that lead to their conquering of land. We will integrate principles from palaeontology and biology to reconstruct skull anatomy in 14 fossil tetrapods. Mathematical and mechanical principles will then be used to test the hypothesis that changes to skull anatomy resulted in tetrapod skulls evolving from hydrodynamically streamlined broad, flat skulls that could deliver a rapid (but weak) bite to strongly built skulls that could produce a more effective, forceful bite. New evolutionary modelling methods will assess how selection for skull strength or hydrodynamic efficiency shaped the evolution of the tetrapod skull.

Our project will produce methodological advances that can be applied more broadly to evolutionary transitions and radiations, and to address long standing questions linking form and function. Palaeontologists, anatomists, biomechanists, evolutionary and developmental biologists and engineers will benefit from this work, which will establish new international collaborations. Its visual aspect and focus on early tetrapods will appeal to the general public, offering engagement opportunities and generating media interest. Members of our team are leaders in developing and validating methods for reconstructing and simulating the musculoskeletal anatomy and function of fossil organisms and have been involved in developing new methods for modelling how function has shaped form in deep time. The time is therefore ripe to apply our knowledge and skills to one of the key events in the history of life and our ow

Planned Impact

Fossil animals are tremendously popular and the transition of our ancestors from water to land captures the public imagination. The defining fossils represent 'missing links' and the outcomes of the event - limbs with digits, a weight-bearing skeleton, air-breathing and a strong bite - are evident across all living tetrapods, including humans. Moreover, the public is fascinated by HOW scientists know what long-extinct animals looked like and how they lived.

The primary aim of our impact plan is to educate and engage beneficiaries in early tetrapod palaeobiology, evolutionary processes and new, interdisciplinary methods for understanding how animals work by showcasing exciting UK science. By determining what happened to the function of the skull as it dramatically changed shape across this transition, we will reveal new (and in some cases, surprising) insights on this key moment in our evolutionary history.

1. Who could potentially benefit from the proposed research?

The main non-academic beneficiaries of this research will be the general public (school children, adults and amateur scientists), museums and galleries, educators and media organizations.

2. How might the potential beneficiaries benefit?
Fossil animals serve as a gateway to inspire the public to better understand our world and the scientific principles underpinning it. The public will gain an enhanced understanding of how evolutionary processes created the modern biosphere (particularly the origin of all living tetrapods, including humans) and how methods from other disciplines - mathematics and engineering - are important for understanding how living and fossil animals work. Museums will benefit from enhanced knowledge of their specimens and, as part of our impact plan, we will use the project's highly visual results to create a custom-designed travelling exhibit showcasing our work in at least four museums in the East of England and Bristol. By creating a touring exhibit, we aim to maximize our reach and benefit participating museums by providing new information on early tetrapods and increasing visitor footfall (for further details see Pathways to Impact). The UK educational community will be another beneficiary of the information generated by this research, as it is of direct relevance to core topics in the National Curriculum for Science, which introduces fossils, evolution and biomechanics at various stages of primary and secondary education. Via our STEM ambassador programme and Bristol Centre for Public Engagement, teachers will receive tailored information for courses on numeracy, science and engineering. The fish-tetrapod transition provides an excellent example of a sequence of fossils that evolve in an easy to understand, step-wise fashion. School children and their teachers will also benefit by witnessing UK science directly linked to required topics. UK and international media organizations are also key stakeholders given high levels of public interest in fossils and natural history. Finally, this project will strengthen the UK's competitive advantage in palaeobiology and animal biomechanics, resulting in lasting international partnerships.

3. What will be done during and after the project to increase the likelihood of the research reaching the identified beneficiaries and maximise the likelihood of the identified benefits being achieved?

The greatest impact of the project will be felt through the exhibition, to which we will contribute new information, 3D digital and physical models, and videos from mechanical simulations. As a travelling exhibition at least four museums will benefit from this exhibit - further details are contained in Pathways to Impact. Working with the Bristol Centre for Public Engagement we will produce factsheets tailored to school children of all ages. Finally, working closely with Bristol's proactive press office will ensure that project results are disseminated to the widest possible audience.

Publications

10 25 50
 
Description We employed a new method to characterise the evolution of jaw shape in fishes and early tetrapods. Our data contradict the early burst model of jaws achieving maximum variance in shape early in their evolution, and support the suggestion that early tetrapod jaws are simple in shape and similar to other closely related fishes - i.e. they have not yet evolved terrestrial adaptations. We have a paper due out Friday March 18th that further shows how early jaws were optimised for strength and speed. We also published a detailed description and functional analysis of the early tetrapod Whatcheeria deltae.

In an extensive study of bite force in living fish and amphibians and reptiles, we have characterised the bite force profile of extant terrestrial and aquatic animals that phylogenetically and functionally bracket extinct early tetrapods. We have used kinematic data from living animals to generate computational models of muscular and jaw function in fossils As the grant has been delayed by COVID and so further outcomes are still to be published.
Exploitation Route Other academic uses are already adopting our pipeline of characterising empirical and also theoretical shapes. We envisage that this new methodology will prove very useful to the community.
Sectors Education

Culture

Heritage

Museums and Collections

 
Description This work is on-going, but we have begun creating a 3D model as part of the impact plan.
First Year Of Impact 2018
Sector Education,Culture, Heritage, Museums and Collections
Impact Types Cultural

Societal

 
Title CT scans of Crassigyrinus scoticus (BGS specimen GSE4722) 
Description MicroCT data of the left lower jaw of the Carboniferous stem tetrapod Crassigyrinus scoticus (GSE 4722), which was scanned in three parts (the specimen is preserved in three parts). The specimen was scanned at the Natural History Museum's Imaging and Analysis Centre on a Nikon XH 225 microCT scanner in February 2013 and reconstructed as DICOM image stacks. All three parts were scanned at 210 kV and 240 mA. Part 1 represents the anterior part of the jaw and the scan produced 1995 transverse slices with a resolution of 0.1271 mm/voxel. Part 2 represents the middle part of the jaw and the scan produced 1995 transverse slices with a resolution of 0.1099 mm/voxel. Part 3 represents the posterior part of the jaw and the scan produced 1687 transverse slices with a resolution of 0.1099 mm/voxel. It was collected by Laura Porro and Jennifer Clack for anatomical description of the specimen and further biomechanical analyses. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL https://www2.bgs.ac.uk/nationalgeosciencedatacentre/citedData/catalogue/79ebcef0-16c6-44dc-afef-4b8c...
 
Title Data from: Evolution of jaw disparity in fishes 
Description The morphology of the vertebrate lower jaw has been used to infer feeding ecology.; transformations in mandibular shape and structure likely to have facilitated the emergence of different feeding behaviours in vertebrate evolution. Here we present elliptical Fourier shape and principal component analyses, characterizing and comparing the disparity of jaw shape in early gnathostomes and their modern primitively aquatic counterparts. 83% of shape variation is summarized on the first three principal component axes and all component clades of early gnathostomes exhibit overlapping morphological variation. Non-tetrapodomorph Palaeozoic sarcopterygians are more disparate than their extant counterparts whereas extant chondrichthyans are more disparate than their Palaeozoic counterparts. More generally, extant jawed fishes are more disparate than their Palaeozoic relatives largely because of the extensive shape variation exhibited by mandibles of extant actinopterygians. Only some areas of shape space vacated by Palaeozoic gnathostomes have been convergently refilled by living taxa. Characterization of theoretical jaw morphologies demonstrates that less than half of all possible shapes are realised by the jawed fishes that comprise our empirical dataset; many of these morphologies are realised by unrepresented terrestrial tetrapods, implying environmental constraint. Our results are incompatible with the early burst model of clade evolution and contradict the hypothesis that maximum disparity is reached early in the evolutionary history of jawed fishes. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
URL https://datadryad.org/stash/dataset/doi:10.5061/dryad.cq5ff51
 
Title Data from: Evolution of jaw disparity in fishes 
Description  
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
URL https://datadryad.org/resource/doi:10.5061/dryad.cq5ff51.2
 
Title Data from: Evolution of jaw disparity in fishes 
Description  
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
URL https://datadryad.org/resource/doi:10.5061/dryad.cq5ff51.1
 
Title Osteology and digital reconstruction of the skull of the early tetrapod Whatcheeria deltae 
Description The Early Carboniferous stem tetrapod Whatcheeria deltae is among the earliest-branching limbed tetrapods represented by multiple near-complete specimens, making it an important taxon in understanding the vertebrate water-to-land transition. However, all preserved skulls of Whatcheeria suffer from post-mortem crushing and lateral compression, which has made cranial reconstruction problematic. In this study, computed tomography data of three Whatcheeria specimens were segmented using visualization software to digitally separate each individual skull bone from matrix. Digital methods were used to repair and retrodeform the bones and produce the first complete three-dimensional skull reconstruction of Whatcheeria. We provide a revised description of the cranial and lower jaw anatomy of Whatcheeria based on CT data, focusing on sutural morphology and previously unknown anatomical details. Our findings suggest that Whatcheeria had one of the narrowest skulls of any known early tetrapod, a gap between the nasals, and significant overlap of the lacrimal onto the nasal and prefrontal. Sutural morphology is used to infer loading regime in the skull during feeding and suggests the skull of Whatcheeria was well adapted to resist stresses induced by biting large prey with its enlarged anterior fangs. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL https://tandf.figshare.com/articles/dataset/Osteology_and_digital_reconstruction_of_the_skull_of_the...
 
Title Osteology and digital reconstruction of the skull of the early tetrapod Whatcheeria deltae 
Description The Early Carboniferous stem tetrapod Whatcheeria deltae is among the earliest-branching limbed tetrapods represented by multiple near-complete specimens, making it an important taxon in understanding the vertebrate water-to-land transition. However, all preserved skulls of Whatcheeria suffer from post-mortem crushing and lateral compression, which has made cranial reconstruction problematic. In this study, computed tomography data of three Whatcheeria specimens were segmented using visualization software to digitally separate each individual skull bone from matrix. Digital methods were used to repair and retrodeform the bones and produce the first complete three-dimensional skull reconstruction of Whatcheeria. We provide a revised description of the cranial and lower jaw anatomy of Whatcheeria based on CT data, focusing on sutural morphology and previously unknown anatomical details. Our findings suggest that Whatcheeria had one of the narrowest skulls of any known early tetrapod, a gap between the nasals, and significant overlap of the lacrimal onto the nasal and prefrontal. Sutural morphology is used to infer loading regime in the skull during feeding and suggests the skull of Whatcheeria was well adapted to resist stresses induced by biting large prey with its enlarged anterior fangs. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL https://tandf.figshare.com/articles/dataset/Osteology_and_digital_reconstruction_of_the_skull_of_the...
 
Title Osteology and digital reconstruction of the skull of the early tetrapod Whatcheeria deltae 
Description The Early Carboniferous stem tetrapod Whatcheeria deltae is among the earliest-branching limbed tetrapods represented by multiple near-complete specimens, making it an important taxon in understanding the vertebrate water-to-land transition. However, all preserved skulls of Whatcheeria suffer from post-mortem crushing and lateral compression, which has made cranial reconstruction problematic. In this study, computed tomography data of three Whatcheeria specimens were segmented using visualization software to digitally separate each individual skull bone from matrix. Digital methods were used to repair and retrodeform the bones and produce the first complete three-dimensional skull reconstruction of Whatcheeria. We provide a revised description of the cranial and lower jaw anatomy of Whatcheeria based on CT data, focusing on sutural morphology and previously unknown anatomical details. Our findings suggest that Whatcheeria had one of the narrowest skulls of any known early tetrapod, a gap between the nasals, and significant overlap of the lacrimal onto the nasal and prefrontal. Sutural morphology is used to infer loading regime in the skull during feeding and suggests the skull of Whatcheeria was well adapted to resist stresses induced by biting large prey with its enlarged anterior fangs. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL https://tandf.figshare.com/articles/dataset/Osteology_and_digital_reconstruction_of_the_skull_of_the...
 
Title Rawson et al Early tetrapod skull network 
Description Supporting data for a forthcoming publication. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://data.bris.ac.uk/data/dataset/e0ea0wn9tby12sxvckwxlcefj/
 
Description Featured in museum display in a video discussing my research and career. 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact I am one of four regional female geoscientists who were filmed and whose videos are on permanent display in the Bristol City Museum and Art Gallery exhibit, Making Waves: Mary Anning and her astonishing ichthyosaur. The videos are also being shown as part of outreach events in local schools with low participation in HE.
Year(s) Of Engagement Activity 2023,2024
URL https://www.bristolmuseums.org.uk/bristol-museum-and-art-gallery/whats-on/making-waves-mary-anning-a...
 
Description Radio4 In Our Time with Melvyn Bragg, specialist guest on The Fish-Tetrapod Transition 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact In Our Time with Melvin Bragg (BBC Radio 4). Expert panel guest for popular radio show. This episode was entitled The Fish-Tetrapod Transition. First broadcast 20 October 2022. Available on BBC Sounds.
Year(s) Of Engagement Activity 2022
URL https://www.bbc.co.uk/programmes/m001d56q#:~:text=At%20the%20swampy%20margins%20between,with%20backb...
 
Description Scientific consultant and featured on documentary in conversation with Sir David Attenborough: Attenborough and the Sea Dragon 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I was scientific consultant and oversaw research funded by the BBC that later featured in this documentary. I was also filmed for the documentary in conversation with Sir David Attenborough about my research.
Year(s) Of Engagement Activity 2017,2018
URL https://www.bbc.co.uk/programmes/b09m2kgl
 
Description Scientific consultant and featured on documentary in conversation with Sir David Attenborough: Attenborough and the Sea Monster 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I was scientific consultant and then featured in conversation with Sir David Attenborough describing my research in the BBC documentary Attenborough and the Sea Monster. The documentary was first broadcast in the UK on New Year's Day 2024 and later in PBS in the USA.
Year(s) Of Engagement Activity 2023,2024
URL https://www.bbc.co.uk/programmes/m001txg2