Locomotion in the earliest tetrapods: testing models of terrestriality

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

Abstract

The water - to - land transition made by vertebrates during the Devonian period, between 370 and 360 million years ago, was one of the most profound in evolutionary history, and ultimately allowed the appearance of all land vertebrates including humans. The changes involved fundamental modifications to skeletons - from supports for swimming musculature in water to robust weight-bearing struts and cantilevers for walking and running on land, as well as changes to physiological and sensory systems. These latter changes also had influences on the skeleton that in turn affected the locomotor patterns. Over the last few years we have a gained a much improved fossil record of the animals that represent this transition. It has vastly improved since the days when only two taxa were available (the fish Eusthenopteron and the tetrapod Ichthyostega): we now have the elpistostegids Panderichthys and Tiktaalik, and the tetrapod Acanthostega. These newly discovered skeletons are well enough known to permit hypotheses about relationships and sequences of character acquisition. However, this is only part of the story. It is now evident that the two Devonian tetrapods whose skeletons are adequately known (Acanthostega and Ichthyostega) differ radically not just from modern tetrapods, but from each other. They represent divergent answers to some of the problems of emerging from the water. Ichthyostega and Acanthostega are evolutionary icons of importance comparable to that of other critical 'transitional forms' such as Archaeopteryx (the first bird), Australopithecus (e.g., 'Lucy'), and Ambulocetus (an early 'walking whale'). Acanthostega though possessing limbs with digits was still basically aquatic. On the other hand, the popular image of Ichthyostega as a sturdy land-going quadruped has been shown to be quite erroneous: in fact it was highly aberrant skeletally, having morphological traits that suggest both aquatic and terrestrial specialisations. Its mode of locomotion appears to have been more like that of a seal than a salamander, and its skeleton, according to work by the PI and colleagues, seems to have allowed dorsoventral flexion using a regionalised vertebral column and differentiated musculature as in mammals. We want to test both these diverse models of early tetrapod morphology for their accuracy quantitatively and in three dimensions, which our earlier attempts were unable to do. This we will do by subjecting the specimens to recently developed high-tech methods including microCT, CT and laser scanning, 3D reconstruction and manipulation software that allow us to do this for the first time. Next, we will examine the range of movements of the skeletons to assess what they were capable of, and quantify key indices of biomechanical performance such as regional stiffness of the vertebral column as well as internal bone architecture. For this, we will compare particular parts of the skeleton - centra, neural arches, ribs, limbs and girdles - with modern tetrapods to try to understand, using modern quantitative techniques, how the Devonian tetrapods moved, to what conditions they were most suited, and thus to what environments and life styles they were best adapted. This will help to illuminate the earliest conditions of the transition from water to land and ultimately lead to greater understanding of how modern tetrapod skeletons evolved. This will not only enhance our understanding of the transition from water to land, but lay the foundations and establish the starting conditions for the eventual appearance of the truly terrestrial members of the tetrapod crown group, and thus our own remote ancestors.

Publications

10 25 50
 
Description Hypotheses: (1) Ichthyostega had vertebral and limb ranges of motion more similar in key respects to those of a seal, otter or crocodile than a salamander, with ranges of motion in the "lumbar" vertebrae restricted mainly to dorsoventral flexion.

This hypothesis has been refuted: Ichthyostega had very restricted ranges of motion in both fore and hind limbs, and could not place its hind feet flat on the ground. Thus its locomotion was unlike that of any modern tetrapod. Its hind limbs were more likely adapted for swimming than walking, whereas its fore limbs served to support the front part of the body off the ground during 'crutching-style' locomotion. (Pierce et al. 2012)

(2) Acanthostega's possible vertebral and limb ranges of motion do not differ appreciably from those of a giant salamander.

This hypothesis still remains to be tested. Synchrotron scanning results await analysis in terms of biomechanical potential.


Objectives: (1) Three-dimensionally image the key skeletal elements of the best-preserved specimens of Ichthyostega and Acanthostega as well as at least four potential extant analogs (1 individual each: giant salamander, ringed seal, Eurasian otter, and Australian freshwater crocodile) with microCT, CT and laser scanning. These have largely been achieved. Publications resulting include a study of pinniped vertebral construction (Pierce et al, 2011), and other publications on the extant taxa will follow. The data have been collected. We have, so far, been unable to source a suitable giant salamander for CT scanning; test scans of 2 specimens proved unsuitable due to poor preservative fluid/flesh vs. skeleton contrast. However, we did source several more salamanders and lizards for comparison.

(2) Digitally reconstruct the skeletons of our study taxa in 3D using modern graphics software.

This has been achieved for Ichthyostega and has been published in Nature (Pierce et al. 2012). Scan data have been acquired for Acanthostega and for the related taxon Pederpes. Acanthostega material proved much more problematic. However we have been able to model its vertebral construction, which has corroborated our new view of tetrapod vertebral architecture.

(3) Articulate the 3D digital skeletons of our study taxa in DinoMorph software and quantify their 3D ranges of joint motion in the key vertebral and limb joints.

This has been achieved and published as in (2), although software other than DinoMorph was used because we were not granted access to that proprietary software; this did not impede our success on the project.

(4) Quantitatively compare and contrast possible vertebral and limb joint ranges of motion in Ichthyostega and Acanthostega with those of our potential extant analogs.

This has been achieved for limb joint ranges of Ichthyostega, as above.
Exploitation Route Our 2012 paper on vertebral morphology is already stimulating others to take a new, fresh look at tetrapod(omorph) vertebral evolution, and the earlier paper on limb motion in Ichthyostega has stimulated a lot more biomechanical research in this area (32 citations; e.g. report by Hutchinson in Nature News&Views in 2014: http://whatsinjohnsfreezer.com/2014/08/28/plastic-fishapods/).
Sectors Digital/Communication/Information Technologies (including Software),Education,Culture, Heritage, Museums and Collections,Other

URL http://whatsinjohnsfreezer.com/2012/05/23/ichthyostega-party-time/
 
Description Mainly scientific/academic uses, e.g. citations. But also public engagement: Outreach/Media by Stephanie Pierce: "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 2013
Sector Digital/Communication/Information Technologies (including Software),Education,Culture, Heritage, Museums and Collections,Other
Impact Types Cultural

 
Description EU Marie Curie FP7 Outgoing-Incoming Fellowship (Coordinator)
Amount £188,000 (GBP)
Organisation European Commission 
Sector Public
Country European Union (EU)
Start 02/2012 
End 02/2015
 
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
 
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 The evolution of terrestrial locomotor performance in early tetrapod vertebrates
Amount £420,413 (GBP)
Funding ID NE/K004751/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 07/2013 
End 07/2016
 
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 Linking the evolution of body shape and locomotor biomechanics in bird-line archosaurs: 3D models of dinosaurs 
Description 3D models of dinosaur bodies and code to run analyses published in Nature by Allen et al. in 2013 
Type Of Material Computer model/algorithm 
Year Produced 2013 
Provided To Others? Yes  
Impact too soon to be sure. 
URL http://datadryad.org/resource/doi:10.5061/dryad.hh74n
 
Title Micro-CT and synchrotron-CT scanning datasets 
Description Large datasets from micro-CT and synchrotron-CT scanning have been generated. The latter will be stored at the ESRF facility on completion of the research programme. The former will be stored by the RVC and UMZC. Virtual reconstruction will be placed on open access sites such as Digimorph, as appropriate. As agreed in our data sharing plan, we will also offer these data to be stored at a NERC data centre and we were previously in touch with them about this. All such data will be made available after the current NERC project completes in 2016. 
Type Of Material Database/Collection of data 
Provided To Others? No  
Impact Only public engagement with science impact so far. 
URL http://dx.doi.org/10.5061/dryad.0003s
 
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 Charles Darwin BSF award lecture 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact The lecture theatre was fully booked (250 attendees) for the highly interactive presentation (incorporating the Be The Dinosaur simulation), with many visitors staying on to ask questions and examine specimens, plus subsequent discussion via Twitter.

All feedback responses rated the event 'good' or 'excellent, with a good level of understanding regarding overall research results
Year(s) Of Engagement Activity 2012
URL http://www.britishscienceassociation.org/sites/default/files/root/festival/BSFprog12%20lr%202.pdf
 
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 Inside Nature's Giants Documentary 
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 The "Inside Nature's Giants" documentary series, first screened on Channel 4 in 2009, had 1.2-2 million viewers per episode in the UK, and won the 2010 BAFTA award in the Specialist Factual category. The National Geographic channel also bought the series, increasing the potential reach to 160 million homes in 143 countries. Prof. Hutchinson was a consultant for the programme, editing scripts and providing 60 hours of paid scientific/technical expertise as well as appearing onscreen in 2 episodes and giving acknowledged input on the website content. BBSRC-funded elephant research was featured in 1 episode, and NERC-funded crocodile research in another (Nat. Geo.); both by Prof. Hutchinson. His invitation to act as a consultant on this production was a direct result of the scientific publications on elephant locomotion and his personal interactions with zoos and elephant keepers during the research. Three further series have followed, with episodes broadcast on PBS in the USA in 2012. Since 2011, a book, DVDs and iPad App have been sold based on the programmes.

Very broad viewership, awards and general acclaim. Led to many future media requests with Prof. Hutchinson (more documentaries) and interest in his science communication blog http://whatsinjohnsfreezer.com/.
Year(s) Of Engagement Activity 2009,2010
 
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
 
Description Museum exhibit featuring research output 
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 Geomuseum Faxe in Denmark: exhibited 3D image of fossil tetrapod from our research outputs, crediting our team and funding.
Year(s) Of Engagement Activity 2014
 
Description Museum exhibits 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Public lectures have stimulted discussions after them (roughly 1 lecture/2 years) and the museum exhibits themselves have generated countless discussions.

Regular visits from school groups to museum exhibits.

Hutchinson's expertise and publications in the field of dinosaur locomotion have led to contributions to the design of interactive exhibits produced for extensive museum tours. He was the Chief Palaeontology Advisor, providing the main quality control on scientific evidence, for the 'Be The Dinosaur' travelling museum exhibit, which includes an immersive multi-player video experience, and which has toured 25 museums in the USA and Canada since 2008. Curators have reported increased attendance ("We had a 9% increase in attendance over the previous summer while many other Museums in our State experienced a drop in attendance over the same timeframe." Executive Director, Mid-America Science Museum), together with visitor enthusiasm ("...this exhibit was a huge hit with both kids and adults, resulting in a noticeable increase in attendance." Vice-President of Exhibits and Operations, The Children's Museum of the Upstate). They have also commented on quality content ("... engaging interactive technology, a wealth of scientific information collected by experts in the field of Paleontology, and an unforgettable learning experience." Marketing and Exhibits Manager, ETSU/Gen) and positive educational value ("The educational content was superb and the best part was that young and old alike learned about science in a hands-on way." Director of Education, "Queen of Discovery", GWIZ - The Science Museum).

The RVC research on giant animals was explained and featured prominently as part of a second travelling museum exhibit, "Dinosaurs: Ancient Fossils, New Discoveries", which has attracted approximately 1.5 million visitors spread across 10 museums on two continents since 2008. The writer/producer from the American Museum of Natural History, who produced the 'Walking with T. rex' video within the exhibition, commented: "The exhibition demonstrates to visitors that scientists are still debating and arguing about evidence ... Theropod Biomechanics, utilizing Professor Hutchinson's research findings, is an integral section of the exhibition... YouTube video of the 'walking' mechanical T. rex from the exhibition has been posted by a member of the public, receiving 8,700 views [9,500 by 7/13], with written commentary and comments indicating real engagement with the science."
Year(s) Of Engagement Activity Pre-2006,2006,2007,2008,
URL http://www.bethedinosaur.com/
 
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 Royal College of Veterinary Surgeons, Share Jones Lecture in Veterinary Anatomy 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach Local
Primary Audience Professional Practitioners
Results and Impact An audience of about 100 listened to the latest research results from Dr. Hutchinson's team, which stimulated questions and discussion afterwards.

Further invitations for speaking engagements by Prof. Hutchinson have stemmed from this.
Year(s) Of Engagement Activity 2011
URL http://www.rcvs.org.uk/news-and-events/news/share-jones-lecture-2011-big-and-nimble/
 
Description School visit RVC 
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 Thirty 15 year old school students visited the RVC in August 2011 for a "science summer school" day and Prof. Hutchinson, Dr. Pierce and technician Julia Molnar spent 2 hours explaining their research to them, including anatomical dissections of crocodiles and birds to explain form/function/evolution in these animals.

The students commented afterwards that the day had made them all very likely to want to attend university, and they found our exercise to be one of the highlights. 100% said they aimed to attend university and that this Summer School session had strengthened this attitude
Year(s) Of Engagement Activity 2011
 
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 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