The evolution of terrestrial locomotor performance in early tetrapod vertebrates

Lead Research Organisation: Royal Veterinary College
Department Name: Comparative Biomedical Sciences CBS

Abstract

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.

Planned Impact

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.

Publications

10 25 50
 
Description We have measured the muscle activity, muscle physiology, 3D motions and forces of gait, and 3D anatomy of 5 adult fire salamanders, completing experimental data collection for the project, and analysis of those data is now finished. Publications are in preparation for (1) muscle physiology data (showing that our salamanders fit expectations for vertebrate muscle properties such as force output and contraction speed; which will build confidence in our simulation analyses); (2) muscle anatomy data (showing for the first time the complete, 3D anatomy and quantitative measurements of the limb musculature of salamanders); and (3) muscle electromyography data (showing that our salamanders use their limb muscles similarly to those in other salamanders and reptiles (either mainly active during foot-ground contact or during limb-swinging); again reinforcing that our models should be maximally strong); all three papers are expected to be submitted in 2018-9. Simulations of the salamanders and fossil animals using these data are in progress. The PI (JRH) has been working to get all old data processed and there has been substantial progress in 2017-8, continuing into 2018-9+2019-20; we have had to develop some new techniques to complete our simulations. Meanwhile, we have published some new insights into the morphology of Crassigyrinus (rare, aquatic fossil tetrapod) and its importance for the evolution of bone repair as an unexpected benefit of this project (2 papers); and likewise a paper in Nature on an early tetrapod's locomotion that stems directly from the ideas developed in this project.
Exploitation Route We plan to share all scan data from this study openly so that the 3D image data can be used widely. This will enhance accessibility of the rare fossil tetrapod data, in particular. We have now uploaded a large database of all our crocodile scans (citing NERC's support) on the Open Science Framework: https://osf.io/x38nh/wiki/home/ and https://osf.io/6zamj/. These have earned 25,742 activity points so far, indicating extensive usage by other researchers and members of the public. We will be uploading further data as the publication of our work proceeds.
Sectors Creative Economy,Digital/Communication/Information Technologies (including Software),Education,Culture, Heritage, Museums and Collections

URL http://whatsinjohnsfreezer.com/2013/09/14/scampering-salamanders/
 
Description Outreach/Media by Stephanie Pierce (postdoc): "Fascinating Fossils" ¬(radio broadcast/podcast) The Naked Scientist 2014 "Your Inner Fish" ¬(Episode 1) PBS America 2014 "How did the earliest land animals move?" - public talk Cambridge Science Festival 2013
First Year Of Impact 2014
Sector Digital/Communication/Information Technologies (including Software),Education,Culture, Heritage, Museums and Collections
Impact Types Cultural

 
Description Marie Sklodowska-Curie International Fellowship
Amount € 183,455 (EUR)
Organisation European Commission 
Department Horizon 2020
Sector Public
Country European Union (EU)
Start 08/2016 
End 08/2018
 
Description Marie Sklodowska-Curie International Fellowship
Amount € 251,857 (EUR)
Funding ID 654155 
Organisation European Commission 
Department Horizon 2020
Sector Public
Country European Union (EU)
Start 08/2015 
End 08/2018
 
Title Crocodile CT scan data 
Description Publically accessible database of whole-body CT and MRI scans of multiple crocodile specimens from ancillary research in the NERC-funded projects (acknowledged support). 
Type Of Material Database/Collection of data 
Year Produced 2016 
Provided To Others? Yes  
Impact Notification from multiple colleagues that they are using these open data in their own research and will be citing it. 
URL https://osf.io/x38nh/wiki/home/
 
Title Dynamic simulation code for OpenSim software 
Description New simulation algorithms for estimating maximal speed, energetic cost, and gait dynamics in legged land animals, for open source OpenSim software. 
Type Of Material Computer model/algorithm 
Provided To Others? No  
Impact Still in development, but operational. 
URL https://simtk.org/home/opensim
 
Description City of London Academy school collaboration 
Organisation City of London
Country United Kingdom 
Sector Public 
PI Contribution Expertise on palaeontology and anatomy, staff time to instruct students in these areas
Collaborator Contribution Expertise in art and how to combine this with scientific insight to intensity students' interest in science/STEM subjects.
Impact Students were taught by the RVC team about biomechanics and palaeontology and then used this information and our guidance to build their own baby Tyrannosaurus rex sculptures, to illustrate what a ~5kg infant T. rex might have looked like (no fossils exist!) and then to share them with their peers for comparison and discusssion. This will be featured at the RVC's Night at the Vet College event on 17 March 2016 as a public showcase event to display what the students came up with, and then we plan to expand this 2015-6 event into a new, broader art-science collaboration between RVC (PI Hutchinson & team) and City of London Academy (art teacher Ben Frimet + students) in 2016-7 onwards. To date over 50 students have taken part.
Start Year 2015
 
Description New collaboration with Brown University 
Organisation Brown University
Country United States 
Sector Academic/University 
PI Contribution New collaboration with fellow (now at RVC ) on dinosaur foot pressures/mechanics, as per EU Marie Curie fellowship.
Start Year 2011
 
Description New collaboration with John Nyakatura (Humboldt University) 
Organisation Humboldt University of Berlin
Country Germany 
Sector Academic/University 
PI Contribution New collaboration on evolution of land animal locomotion, focusing on amniotes (advanced land animals). We contribute expertise on evolutionary biomechanics. JR Hutchinson involved.
Collaborator Contribution New data and analysis tools for studying amniote locomotion and reconstructing gait in fossil taxa.
Impact still pending
Start Year 2013
 
Description "Anatomy to You" social media 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact New blog, Twitter and Facebook feeds called "Anatomy to You" to disseminate anatomical research to the general public, media and scientists. Since launching at the start of 2016, the ATY blog site has had 9,315 views from a total of 123 countries across the world, with 23 subscribed followers. We also have 486 Twitter followers, generating more than 4,500 profile views and more than 135,000 Tweet impressions. Our Facebook page has 420 'likes' and a total reach of 25,500 since launch in January. In addition to general coverage of anatomical research, we are using it to promote our NERC-funded research on early tetrapod locomotor evolution and other RCUK-funded projects throughout our lab, so this social media presence is already having strong impacts in terms of public engagement as well as new invitations to participate in other engagement activities worldwide.
Year(s) Of Engagement Activity 2015,2016
URL http://anatomytoyou.com/
 
Description #SalamandraScience Twitter hashtag- documenting experiments 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Ongoing reporting of our in vivo experiments with fire salamanders for our NERC-funded studies, to show the excitement of (non-invasive) research with these fascinating animals in Oviedo, Spain, and what we learn from them as we process the data. "#SalamandraScience" hashtag on Twitter
Year(s) Of Engagement Activity 2015,2016
URL https://twitter.com/search?q=%23salamandrascience&src=typd
 
Description BBC TV appearance 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact PI Hutchinson was a featured consultant on this BBC TV documentary, shown studying how elephants move (BBSRC funded research work) and how this relates to interpreting fossil organisms (NERC funded research work). The programme was a massive success internationally (reportedly breaking BBC documentary records), with millions of viewers (8.5M in the UK on the first night alone) and ongoing discussions as well as likely lead-ins to future documentary programme involvement by Hutchinson's team.
Year(s) Of Engagement Activity 2016
URL http://www.bbc.co.uk/programmes/p03dwy5z
 
Description Cambridge University Biological Society lecture 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Undergraduate students
Results and Impact Public seminar entitled "The evolutionary struggles of giant land animals against gravity" to local zoological society, which stimulated discussion of my team's BBSRC- and NERC-funded research projects afterwards, and subsequent emails thanking me for my stimulating presentation as well as an invitation to do future events.
Year(s) Of Engagement Activity 2015
 
Description Careers Day at local school 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Presentation to 5th year at Greneway School, Royston, Herts, UK: 30 minutes providing information about what it is like to be a scientist and study extinct and living (especially large) animals and be a university professor, and then 30 minutes of discussion answering questions about animals, careers and related topics. Teachers reported that students had rave reviews of the event and it increased their interest in STEM subjects and careers. Featured BBSRC funded work on chickens and NERC funded work on tetrapod fossils.
Year(s) Of Engagement Activity 2016
 
Description Cheltenham Science Festival exhibit on fossil tetrapod research 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Free public stand exhibited in 2016 at Cheltenham Science Festival (UK) featuring 3D-printed skeletal material of our study fossils. Discussions with approximately 300 students, teachers and families of the NERC-funded research project activities, which initiated further questions. Feedback from the festival and public was that there was strong interest in palaeontology stimulated by this exhibit and requests for further information, plus invitations for future exhibitions and presentations.

Report available from Anatomical Society (funded costs of event): http://www.anatsoc.org.uk/docs/default-source/default-document-library/hutchinson_as_award_report.doc?sfvrsn=0
Year(s) Of Engagement Activity 2016
URL https://whatsinjohnsfreezer.com/2016/06/07/the-freezers-hit-the-road/
 
Description City of London Academy school visits 
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 Arranged six hour-long events with City of London Academy school to discuss palaeontology research associated with these NERC-funded projects. Students in art and science classes watched presentations about palaeontological field work, dinosaur/tetrapod palaeobiology, and then engaged with the scientific staff to create their own extinct animals in art projects (sculptures). This has led to an established collaboration with art teacher Ben Frimet that will continue in 2017 with more similar events planned at the school.
Year(s) Of Engagement Activity 2008,2015,2016
URL https://whatsinjohnsfreezer.com/2015/04/26/giant-dinosaurs-london/
 
Description Misc. TV documentary involvement 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Prof. Hutchinson's research was featured in the 2011 "Dino Gangs" documentary on the Discovery Channel, which aired worldwide, with the work on theropod growth and speed also referenced in the accompanying book. Other programmes covering the team's work include "Evolutions" (National Geographic, 2008), "Raw Anatomy" (National Geographic Channel, 2009) and 'How to build a Dinosaur" (BBC4, 2011), featuring our NERC-funded research.

Very broad viewership and more informed, entertained public. More requests for documentary involvement- Prof. Hutchinson is now contacted several times a month with TV documentary requests/advice.
Year(s) Of Engagement Activity 2008,2009,2010,2011,2012,2013,2014
 
Description NatGeo TV appearance: giant rhinoceroses 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact Featured appearance in "Top 10 Biggest Beasts Ever" documentary on NatGeo TV, focusing on interpreting the anatomy and behaviour of giant extinct rhinoceroses (relevant to NERC and BBSRC grant research).
Year(s) Of Engagement Activity 2015
URL http://natgeotv.com/uk/top-10-biggest-beasts-ever
 
Description Night at the RVC public event 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Evening event including an exhibit/stand promoting our NERC-funded tetrapod research project, including fossils and posters for the public to read/handle/discuss. Visited by about 200 people and generated numerous questions, leading to very positive feedback that the visitors departed with new knowledge of and interest in palaeontology.
Year(s) Of Engagement Activity 2016
URL http://www.rvc.ac.uk/news-and-events/events/night-at-the-vet-college-animal-athletes
 
Description Palaeocast podcast interview 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact 48-minute online podcast interview with PI Hutchinson about his research in palaeontology, anatomy and biomechanics, including NERC and BBSRC funded research, which led to numerous online discussions and interactions about careers in science especially my general subject area.
Year(s) Of Engagement Activity 2016
URL http://www.palaeocast.com/episode-58-animal-biomechanics/
 
Description Public event at RVC 
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 "Giant land animals versus gravity: performance at an extreme" public talk and also NERC tetrapod research-focused stand (interactive, hosted w/members of research team), at RVC's "Night at the Vet College" evening event, which provoked numerous discussions, hands-on demonstrations, extensive conversations and new interactions and collaborations that are persisting beyond the event.
Year(s) Of Engagement Activity 2016
URL http://www.knowledgequarter.london/night-at-the-vet-college-animal-athletes/
 
Description RVC Open Day bones demonstration 
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 RVC Hawkshead campus open day event, where our research team presented a publically accessible stand showing different kinds of animal bones and how these relate to biomechanics, behaviour, welfare, evolution and other topics of general interest as well as direct connection to our BBSRC- and NERC-funded research. Visitors were streaming through the stand (hosted by 5 postgrad researchers) for >6 hours and had many interactions with those hosting the stands to answer their questions about relevant topics and about our research.
Year(s) Of Engagement Activity 2015
 
Description Science Blog 
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 Anatomy blog: sharing the latest scientific research and insights from Prof. Hutchinson's team, with a strong focus on RCUK-funded research. Highly visual and stimulating discussion. As of submission in 2016, total 354,000 views, 3239 followers, 1855 comments, 161 posts.

255,944 all-time views (average 250/day) as of 14/10/2014; 1,529 comments, 750 Subscribers, 642 shares; with additional viewers (53,412) and subscribers (92) at associated Youtube Channel: https://www.youtube.com/user/Whatsinjohnsfreezer
Year(s) Of Engagement Activity 2012,2013,2014,2015,2016
URL http://whatsinjohnsfreezer.com/
 
Description T. rex Autopsy NatGeo TV consultancy 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact Major consultant role and featured appearance in "T. rex Autopsy" NatGeo/Channel4(UK) documentary, aired worldwide in 2015, featuring PI Hutchinson's explanations of how we infer the behaviours and anatomy of extinct organisms (NERC-funded grant research).
Year(s) Of Engagement Activity 2015
URL http://whatsinjohnsfreezer.com/2015/05/20/t-rex-autopsy-my-backstory/
 
Description Twitter: Science Communication 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Persistent, daily public engagement by Prof. Hutchinson on his personal account, which regularly addresses scientific research that his team is conducting, including RCUK-funded research. Averages ~250,000 impressions/month; as of submission in 2016 is 27,500 tweets total, 4778 followers, 1652 photos and videos.

>19,000 tweets, >3,000 followers, Klout score ~63 as of 14 October 2014-- indicates strong engagement in science communication. Twitter Analytics indicate 224.9K impressions (views) and thousands of engagements (clicks, favourites, retweets, replies etc.) during a representative month.
Year(s) Of Engagement Activity 2012,2013,2014,2015,2016
URL https://twitter.com/JohnRHutchinson