Understanding the functional evolution of the mammalian middle ear and jaw joint across the cynodont-mammaliaform transition

Lead Research Organisation: University of Bristol
Department Name: Earth Sciences

Abstract

The origin and evolution of mammals is a key event in vertebrate evolutionary history, and a textbook example of an evolutionary transition. From around 230 million years ago, the fossil record documents an uncharacteristically well-preserved sequence of transitional fossils evolving key mammalian features such as deciduous and permanent teeth, a large brain, strong skull and the unique mammalian middle ear. Rather than a single middle ear bone, mammals have a more finely tuned middle ear comprising three small bones, or ossicles, the malleus, incus and the stapes. Along with a coiled cochlea, this structure enables high frequency sound detection. Combined evidence from the fossil record, embryology and development reveal a remarkable example of transformation in structure and function: bones forming the jaw joint of mammalian ancestors transform into the minute middle ear structures of mammals. We know that as the tooth-bearing bone, the dentary, increases in size, the jaw joint bones become smaller and loosely attached. Eventually the dentary contacts the squamosal part of the skull forming a true mammalian 'dentary-squamosal' (temperomandibular) hinge. We even know that at one point in mammalian evolution, animals existed with two jaw hinges with a dual feeding and auditory function. A long-standing point of debate is how the bones of the ancestral jaw hinge were able to reduce in size, whilst at the same time still functioning as a viable jaw joint. Additionally puzzling, is that during this transition, the skull is supposed to be strengthening, as the jaw-closing musculature reorganises to become a more efficient force generating system. The jaw joint should become stronger, not weaker and degenerate. Perhaps most startling, is that this transition has happened more than once.

Theoretical models proposed in the 1970s and 80s suggested that reorganization of the jaw musculature lead to reduced loading at the jaw joint in the ancestors of mammals, allowing the ancestral hinge to become smaller and detect sound whilst the new mammalian hinge took over. These predictions are central to how the mammalian jaw and ear evolved, yet they have never been tested. This is largely because we have not had the means, until recently, to go beyond theory. We are now able to bring new computational biomechanical techniques, that we as a team have pioneered, to address the question of how the definitive mammalian middle ear and jaw joint were able to evolve yet remain functionally viable.

We have obtained CT scans of five key transitional taxa. Through detailed study of fossil specimens we will reconstruct the patterns of musculoskeletal evolution across the origin of mammals, particularly in light of new fossil discoveries and suggestions of reversal back to ancestral forms. Using 3D muscle reconstructions and multibody dynamics analysis, we will determine how the ancestral, dual jaw joint and true mammalian jaw joint function during feeding behaviour. We will test if there is a transfer of function from ancestral to modern mammals with the evolution of the dual jaw joint as predicted. For example, do the component parts of the dual joint bear load, and can they function without joint disarticulation; and how is load transferred from the ancestral to modern hinge during this transition. Using finite element models we will test how the bones of the jaw hinge withstand load and strains during feeding. We will test if skulls do become stronger across the transition, as predicted, and how this relates to predicted bite forces.

Comparative anatomists, biomechanists, evolutionary and developmental biologists, palaeontologists and biomedical engineers will benefit from this work. Benefits to UK science include multidisciplinary training of a young scientist and overseas collaboration. The visual aspect of this work and the focus on mammals is likely to appeal to the general public, offering engagement opportunities and media interest.

Planned Impact

Who will benefit from this research?
The main beneficiaries of this research will be the general public, including adults (general public and amateur scientists) and school children. Museums and galleries, public section institutions, will also benefit. It is possible that other beneficiaries may come from the commercial sector and include companies such as Tarmac, Hanson Aggregates and Minimix Ltd that work the quarry sites in South Wales where early mammal fossils have been recovered from fissure fill deposits. We have excellent relations with the quarry companies, and have assisted in identifying new fissure deposits and also consulted with them concerning the SSSI status for some of the quarry localities. It is therefore also possible that policy makers responsible for assigning SSSI status to some of the quarry sites may also benefit from these results.

How will they benefit?
Our research will provide new, novel insights into the evolution of early mammals. This topic is of lasting interest to the general public as it represents the beginnings of our own lineage. Also the origin of mammals is documented by a sequence of well-preserved transitional fossils. This goes against the traditional view many people have of an incomplete fossil record and the origin of new groups represented by gaps or jumps from one type of body plan to another. Mammals therefore represent a good case study to teach school children and adults about evolution and natural selection. Our proposed research will help people understand the adaptive potential of transitional modifications as new groups evolve. The rapid prototype actual models of fossil skulls (at 2-3x actual size), that we shall produce at modest cost, are ideal for these outreach activities, and in some cases for museum display. These models are robust and can be handled by children and adults. We will work with the excellent outreach team in the School of Earth Sciences and encourage further training of our students and postdocs as STEM ambassadors to ensure we reach as many beneficiaries as possible.

Very few people will realise that the origin of mammals, and therefore the origin of our own lineage, can be traced back to 200 million year old fossils from South Wales and Gloucestershire. We have therefore chosen to work with the National Museum of Wales (NMW) in Cardiff to help promote this national heritage and in doing so showcase some of the exciting new research being performed in the UK. The main focus of our impact plan is to produce a professional museum display on early mammal evolution. Our research will also create a good deal of visual data, from digital 3D models of fossil skulls, to movies of muscle and jaw movement and function, and colour-coded stress and strain plots of jaw mechanics. Modern visual museum displays provide a dynamic way to portray this information. The displays will travel from the NMW to at least three other institutions in Wales and South West England, and will be translated into Welsh, to ensure that the maximum number of users are reached. These museums will benefit in terms of fulfilling a remit to the general public to preserve and showcase regional and national heritage, and by increased visitor numbers associated with novel displays. The general public will benefit from an enhanced understanding of how fossils from Wales and the UK have played a central role in understanding the origin of mammals, our own lineage, and how research from the UK is providing important new insights into this major event in evolutionary history.

Publications

10 25 50
 
Description We have overturned current view on the evolutionary assembly of mammalian jaw musculature. We have shown that 'reptilian-like' muscles are lost and mammalian muscle organisation developed prior to the appearance of true mammalian characters, such as a single bone forming the lower jaw, only two sets of teeth and three sophisticated sound detecting middle ear bones (objective 1). We have shown that the load is not reduced at the jaw hinge, overturning to the standard model of jaw joint and middle ear evolution (objective 2) and that there is no change in the strength of the skull across the origin of mammals (objective 3). Papers describing our results for objectives 1 and 2 are published. Paper describing the results of objective 3 is in review.
Exploitation Route The methods we are developing will be of interest to the field. Our finding on musculoskeletal anatomy and jaw function are of interest to developmental biologists and anatomists.
Sectors Education,Culture, Heritage, Museums and Collections,Other

 
Description We have completed our impact plan. This comprises a museum exhibit at the National Museums of Wales in Cardiff featuring how our new methods deduce new information from the fossil mammals of Wales. This will be a touring exhibition; these specimens and our work are culturally and scientifically important parts of Welsh heritage. For more information see: https://museum.wales/blog/2018-01-26/Meet-Morgie/
First Year Of Impact 2018
Sector Culture, Heritage, Museums and Collections
Impact Types Cultural,Societal

 
Description University of Bristol capital expenditure - equipment
Amount £350,000 (GBP)
Organisation University of Bristol 
Sector Academic/University
Country United Kingdom
Start 08/2015 
End 01/2016
 
Description Collaboration with Agustin Martinelli (Buenos Aires), Marina Soares, Cesar Schultz (Federal University of Rio Grande do Sul: UFRGS) 
Organisation Federal University of Rio Grande do Sul
Country Brazil 
Sector Academic/University 
PI Contribution We are providing in kind support for CT scanning fossils and use of our tomography and computational facility to our Brazilian collaborators.
Collaborator Contribution Firstly researcher Dr Agustin Martinelli visited the University of Bristol via a Benjamin Meaker visiting professorship award in 2018. More recently, Agustin Martinelli, Professors Cesar Schultz and Marina Soares and PhD student Pedro Fonseca are visiting the University of Bristol via Brazilian government funding. They are providing collaboration and funds for CT scanning fossils and establishing and building future collaborations.
Impact Publication: https://doi.org/10.1080/08912963.2018.1427742
Start Year 2016
 
Description Collaboration with Vera Weisbecker (U. Queensland) & Stephen Wroe 
Organisation University of Queensland
Country Australia 
Sector Academic/University 
PI Contribution Visit to Australia - gave a series of workshops and seminars about our current project. Started collaboration with Dr Weisbecker.
Collaborator Contribution Dr Weisbecker shared knowledge and data on her work on marsupial embryology and how this relates to the series of character changes during the origin of mammals.
Impact Two invited departmental talks by postdoc Stephan Lautenschlager: 05/2015: School of Biological Sciences, University of Queensland, Brisbane, Australia 04/2015: Function, Evolution & Anatomy Research Lab, Zoology Division, University of New England, Armidale, Australia Four days of workshops: 05/2015: Introduction to Finite Element Analysis, School of Biological Sciences, University of Queensland, Brisbane, Australia (3-day lecture and workshop teaching Strand7) 04/2015: Blender workshop, Function, Evolution & Anatomy Research Lab, Zoology Division, University of New England, Armidale, Australia (1 day workshop)
Start Year 2015
 
Description Cafe Scientifique 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact CoI Gill presented a Cafe Scientifique on the Isle of Wight, focusing on how new scanning technologies can shed light on mammalian evolution.
Year(s) Of Engagement Activity 2017
 
Description Public lecture Birmingham 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Postgraduate students
Results and Impact Presented a public lecture on the research conducted; engaged student and general public attendees. Sparked future collaboration and raised awareness of the work we are doing.
Year(s) Of Engagement Activity 2016