The evolution of terrestrial locomotor performance in early tetrapod vertebrates

Tetrapods, or bony animals with limbs instead of fins, evolved the ability to support their body weight and move on land sometime in the Middle to Late Devonian period - around 350-400 million years ago. However, the ability to stand on all four legs seems to have evolved after the appearance of fully developed limbs with digits and other skeletal features which are now thought to have arisen in aquatic animals. Our prior NERC-funded work focused on the locomotor behaviours of two key Devonian animals, Ichthyostega and Acanthostega, to reconstruct how early tetrapods transitioned from swimming in water to walking on land. Through the use of 3D modelling and simple static biomechanics, we found these evolutionary pioneers had limited capacity to move their limbs in certain directions which hindered their ability to walk like a modern land animal. This raises the question: when and how did modern walking styles evolve? Furthermore, were all tetrapods similarly sedate or could some forms move more quickly than others? The technology and biological understanding now exists to answer such fundamental evolutionary questions. To answer them, we need to determine what kinds of forces and speeds that different tetrapods could generate.

We aim to reconstruct dynamic motions in a series of early tetrapods bracketing the water-to-land transition using the latest computer simulation techniques. These animals include the mainly aquatic Ichthyostega and Acanthostega and two more recent Carboniferous forms that seem to have been more terrestrial, Pederpes and Proterogyrinus. To validate the simulation technique, cutting-edge 3D experimental data will be collected on walking/trotting modern salamanders for the first time. We will also measure how land-adapted salamanders change their speed capacity as they grow, which by analogy should give insights into the evolutionary progression of walking capabilities in progressively more terrestrially adapted early tetrapods. These experimental studies will test (1) how important the limbs and backbone are in supporting movements on land and (2) whether maximal speed capacity is constant or changes during growth.

The experimental data from salamanders will be fed into a computer model in which a novel, high-fidelity dynamic simulation of how muscles drive locomotion will be created. In addition, whole body 3D models of the early tetrapods will be constructed with simplified, abstract representations of the major limb/backbone muscles. The salamander data will then be used as a template to simulate locomotion in the extinct animals; how each species of tetrapod moved and how quickly they could do it will be estimated. Locomotor abilities of each animal will then be compared to determine the sequence of evolutionary events that ultimately gave rise to walking capabilities, made possible because each species is successively more closely related to living tetrapods. The evolutionary changes will also be compared to the walking aptitude of growing salamanders to see if the two are mutually informative -- i.e. broadly speaking, does 'ontogeny recapitulate phylogeny' in tetrapod locomotion?

This project will uncover how evolutionary changes in anatomy impacted the ways in which early tetrapods could move, ultimately illuminating how vertebrates eventually conquered the terrestrial realm. It is curiosity-driven science that aims to tackle one of the most awe-inspiring and pivotal evolutionary events in Earth's history. As such, it will engender a great deal of public interest (as demonstrated by our previous NERC grant), which we will vigorously capitalize upon by creating interactive public/scientific fora to communicate and disseminate our research. Further, it will advance the field of evolutionary biomechanics by creating a novel simulation approach, firmly grounded in empirical data, which will be distributed to scientists studying locomotion in living and extinct organisms.

The major NERC Science Theme that our project fits is "understanding the role of biodiversity in key ecosystem processes." Accessible, exciting science about extant (our study of salamander growth) and extinct (early tetrapod morphology and simulated motions; and evolution thereof) organisms is a vital part of the raw fuel of public enthusiasm that powers sustained public engagement with such priorities and progress in pursuing major societal goals such as protecting biodiversity.

The key impact of this study would be public engagement with, and communication of, science including biodiversity. The tetrapod water-to-land transition was a crucial evolutionary breakthrough, with wide-ranging consequences for all later tetrapods - including humans. As such, early tetrapod research has attracted a vast interest, from frequent high profile publications in Nature/Science and related media interest to documentaries and museum exhibits and even numerous popular books including Project Partner Prof. Clack's critically acclaimed "Gaining Ground". We will continue to feed new discoveries into the public domain, both in the UK and worldwide, e.g. through maintained websites and blogs as per our Impact Plan. Our prior NERC project demonstrates this commitment with our latest publication in Nature - on 3D limb joint mobility in Ichthyostega - being featured on Planet Earth Online, the BBC, National Geographic, Reuters TV, and many other media outlets. As part of this publication we also developed an informative website for the general public and scientists alike, with videos on YouTube (http://www.rvc.ac.uk/SML/Research/Stories/TetrapodLimbMotion.cfm).

To deliver this impact, several distinct groups of beneficiaries/audiences are involved:

For natural history museums, the programme will provide resources for their work in education and dissemination of research findings relating to the natural world, especially the Palaeozoic era and its inhabitants, and how changes that transpired then influenced all future events on land. Ongoing contact with museum staff has helped inform this proposal, including two interactive museum exhibits that JRH has advised on and frequent contact with curators of museums worldwide. The models - both computer-simulated and physical rapid-prototypes - generated from the research will be valuable tools to support this activity. The presentation of the relationships between extinct and extant animals and the evolutionary processes revealed in their study is a mission of many museums and universities and helps a general audience grasp a deeper understanding of the many related areas of biology.

The latter role is also applicable to zoo staff, and here the evolutionary message may be embedded within an appreciation of how animals adapt to different environments (including across ontogeny in salamanders), in many cases alongside an ecological mission to appreciate and conserve natural habitats. The exploration of movement from early tetrapods linked through to modern salamanders will aid in a lucid delivery of these messages.

Science communicators - particularly those involved in documentary production, whom our team targets for dissemination of our research - comprise a third group with a similar requirement for engaging, especially visual, materials to support their presentation of new findings in biology and palaeontology.

Biology teachers at primary and secondary levels, together with their students, are further groups of beneficiaries. A relatively small number in the UK (>200 over 3 years) will benefit through direct interaction with JRH and the research team through their outreach activities - both 'live' during school visits and RVC open days. A greater number (thousands or more worldwide) will be reached online, but still interactively, via the project blog, Twitter account and Facebook page; together with the opportunity to use the digital materials which will be made available.