The role of skull flexibility in feeding - an investigation using advanced computer modelling techniques

The project examines the role of skull flexibility in lizard feeding, using an advanced computer modelling approach. In a newborn human baby, areas of soft tissue remain between skull bones, allowing flexibility and continued growth. In an adult, the sutures close and the brain is enclosed in a rigid bony shell to which the facial bones are immovably attached. Gape is limited. However, in the skulls of adult lizards, snakes and birds some sutures remain open, allowing movement of the skull parts on one another. This flexibility (=kinesis) can be spectacular, e.g. in a large snake swallowing prey with a body diameter several times that of its own head. Such skulls clearly operate in a very different way to the rigid skulls of mammals, and reflect major differences in biology and lifestyle. Comparative studies between skull types are important in shedding light on normal, pathological and aging skull functions generally. Mammals need a regular supply of food to maintain a constant high body temperature. Their skulls have evolved to maximise the efficiency of oral food processing (chewing) (e.g. differentiated teeth, precise occlusion, hard palate, precise muscle control). Lizards and snakes, in contrast, warm themselves from external sources and can feed opportunistically. A large meal can last a snake for months), and there is usually little oral food processing. Instead, the skull of advanced snakes allows increased gape and aids both food transport through the mouth and swallowing. In lizards, from which snakes evolved, the situation is less clear-cut. Skull movements are more subtle and many of the joints through which they act, or potentially act, are not well understood. Many questions remain unanswered, notably: a) which lizards are really kinetic and to what degree? b) how do the different skull parts move in relation to one another, and by how much (passive adjustments or active linked movements)? c) what is the role of the membrane-cartilage braincase in the adult? Does it aid or limit kinesis? Does observed anatomical variation match the pattern of kinesis? d) what are the consequences of kinesis for skull function and stability, and how does this relate to diet? e) can kinetic ability be predicted by skull shape? To date, most discussion of lizard kinesis has been based on dissection, manipulation of dead or anaesthetised animals, theoretical analyses, and a few experimental studies. As a result, there is a lack of agreement on many points. Advanced computer modelling offers an alternative approach. Our research group is cross-disciplinary (reptile anatomy/evolution; biomechanical engineering; analysis of shape in relation to function). We have a strong track-record and have pioneered an approach that combines the use of 3-D computer simulations (multibody dynamics analysis) and stress analysis (finite element analysis). This yields detailed, anatomically accurate working computer models of animal skulls, including joints and muscles (jaw, neck). Sophisticated software then allows us to relate changing skull shape to skull performance during feeding. Comparisons with living animals (bite force data, records of muscle action and feeding) have shown our models to be biologically realistic, but our U.S collaborators (Ross, Lappin) will collect further comparative data in the new project. Beneficiaries of our work include the academic community (evolutionary biologists, palaeontologists, functional anatomists - data and new methodological approaches), the UK science base in general (through training of young scientists in an interdisciplinary framework, attraction of overseas students and collaborators, engaging young people in science), the wider public (public engagement, media interest) and, potentially, clinicians (perspectives on normal, aging and pathological skull, jaw and tooth function).

Lizard, snake and bird skulls differ from the rigid skulls of mammals in possessing intracranial flexibility (cranial kinesis). Such skulls offer an alternative perspective on the general factors controlling skull form and function in normal and, potentially, pathological conditions. Kinesis is most spectacular in higher snakes where it contributes to prey capture and increased gape. In lizards, from which snakes arose, the role and distribution of kinesis is more equivocal. Our broad aim in this project is to explore the relationship between skull flexibility and feeding performance, notably: how skull components move relative to one another; the distribution of active kinesis amongst lizards; the effect of kinesis on skull shape and function during feeding; and the role of the cartilage-membrane braincase. These questions have remained largely intractable due to the difficulty of recording subtle, complex movements in small skulls. Advanced computer-based modelling offers a novel approach. Our cross-disciplinary research group has pioneered an approach that combines the use of rigid-body modelling (MDA, multibody dynamics analysis), stress analysis (FEA, finite element analysis), and geometric morphometrics (GMM). Using this methodology, anatomically accurate working 3-D skull models (MDA) are used to predict joint and muscle forces, that are applied to FE models to predict the skull stress/strain under different feeding conditions. Sophisticated shape comparison software (GMM) then allows us to relate changing skull shape to skull performance. Comparisons with living animals have shown our models to be biologically realistic, but our U.S collaborators (Ross, Lappin) will aid validation in the new project (bite force, strain gauge, muscle recording). Ongoing BBSRC funded projects focus mainly on rigid skulls. The new project builds on their success to examine to the more complex skulls of kinetic lizards.

Who are the beneficiaries of this research; how will they benefit? UK life sciences: The BBSRC stresses the need for interdisciplinary approaches to the 'big' questions in biology. As an interdisciplinary team we promote this between colleagues and in the training environment provided for young scientists. Academic community: Our work is of interest to many disciplines including functional and evolutionary anatomy, palaeontology, systematics, and developmental biology, here and overseas (e.g.China, USA, Japan, Germany). It offers new insights on skull structure, function, and evolution. We have introduced novel methodologies (combined MDA/FEA; new GMM techniques/software; iterative modelling; DGO) that have significantly advanced the field and the new project will further refine these approaches. University UGs/MSc: We are all active university teachers - of science and medical undergraduates and postgraduates - as well as researchers, and our research informs what we teach. We will continue to involve UG and Master's students in research projects. The wider community: Animal structure and function interests the public and media and, as such, is a good mechanism for Public Engagement with Science and for fostering interest in science amongst young people. Ultimately this benefits the UK in the development of scientific literacy. Clinical research: Our results to date have implications for craniofacial medicine (e.g. Fagan and O'Higgins will shortly start a new project investigating craniosynostosis) and dentistry (jaw and tooth function), and our modelling approaches have wider application (e.g. iterative modelling, examining growth changes and aging using GMM regression, use of computer models to examine oral food handling). Fagan is a Royal Society Industry Fellow, working with Smith and Nephew's Research Centre on the modelling of bone, and has many other clinical and industry partnerships. What will be done to ensure that they have the opportunity to benefit from this research? Dissemination of results - academic: we publish in high impact journals (PNAS, Proc. Roy. Soc. [see publications/track record]) and speak at international conferences/ seminars/ workshops in the UK and overseas (palaeontology, vertebrate morphology, herpetology, developmental biology, anatomy). We also maintain web pages and are seeking to extend these to include a database of computer models and other useful data. Dissemination of results - wider participation: we will continue to engage in public-academic dialogue with schools, open days, festivals, museum talks, and by working with the media offices of our relevant institutions and funding bodies (e.g. BBSRC Business October 2008, pg 24). Each of our institutions has Public Engagement programmes in place (UCL is a Beacon) and Evans is participating in the web-based Q&A for BBC's new science programme, 'Bang Goes the Theory'). We are also applying to exhibit in the Royal Society's Summer Exhibition in 2010. We have lab web pages but are requesting funds to develop a comprehensive interactive site for the use of colleagues (see above) and the wider public. Fostering a cross-disciplinary approach: we hold bimonthly meetings of the whole team, to which visitors and research students are also invited, and which provide a forum for discussion and development of interdisciplinary thinking. Our research requires that individual researchers develop a broad knowledge base, are able to network across a range of disciplines, and are not afraid of 'thinking outside the box'. These young scientists will develop interdisciplinary teams of their own as well as bringing this approach to their undergraduate students. By making novel techniques and software available to interested parties: e.g. O'Higgins has made his GMM programme Morphologika freely available, and we plan an interactive web site from which existing models (ours and hopefully others) may be accessed.