Skull evolution and the terrestrialization and radiation of tetrapods

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

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.