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Evolution of human tooth enamel: unlocking hidden cell mechanisms

Periodic Reporting for period 1 - DENTALkeys (Evolution of human tooth enamel: unlocking hidden cell mechanisms)

Periodo di rendicontazione: 2022-02-07 al 2024-02-06

The DENTALkeys project addressed questions about the evolution human dental enamel and where humans fit in the evolution of our fossil ancestors from the genus Homo. Understanding the ways in which we relate to our fossil ancestors is fundamental to elucidating how modern humans evolved. Yet, after a century of investigations, there is still no consensus about relationships among some members of the genus Homo. Studies of enamel thickness have been at the centre of these debates. Teeth preserve well in the fossil record and enamel thickness is a trait that can contribute to taxonomic classification. Yet, we know very little about the cell mechanisms that generate variation in enamel thickness. Several of our fossil ancestors have enamel that is of similar thickness, though it formed with very different underlying developmental processes.

The goal in this interdisciplinary project is to identify links between enamel growth and thickness to reveal novel traits in our fossil ancestors that will contribute new classification knowledge to our understanding of human evolution. I used modern dental samples and fossil samples spanning the past 18 million years, but focused on modern humans and fossils from the genus Homo dating to the last 2 million years. I was able to re-examine existing debates about which fossils are, or are not, ‘human-like’ to provide novel insights into their classification. I was also able to make significant headway regarding how the cells that create enamel (ameloblasts) move and secrete enamel during childhood.
I worked with researchers from the Centro Nacional de Investigaciónsobre la Evolución Humana (Burgos, Spain) to evaluate whether there was an evolutionary connection between pits on fossil molars and thinner enamel. Using micro-computed tomography scans (3D x-rays, in essence) of fossil teeth from East and South Africa, we were able to identify that a certain evolutionary cousin of humans, the genus Paranthropus, likely had a genetic disposition toward highly pitted molars that were very thick. A recently discovered fossil hominin from South Africa, Homo naledi, also has very thick enamel, but does not have a the same type of pitting found in Paranthropus. My supervisor at University of Kent, Patrick Mahoney, and I worked with a very large, international team to perform histological analysis of a few Homo naledi teeth. We discovered that although Homo naledi had a very short stature and thick dental enamel on teeth that are very different from those of humans, its teeth grew at a slow pace very similar to what we see in modern human children.

The evolution of the extended human childhood, as tracked in dental tissues, was a major part of my research. Patrick Mahoney and I have just submitted an article detailing how the rate at which enamel is generated during childhood seems to have slowed down from Medieval to modern times in England. I have likewise been working with bioarchaeologists from the University of Lodz (Lodz, Poland) and Keele University (Keele, UK) to track evolutionary changes in enamel thickness, enamel growth variables, and stress events across 4000 years of Polish history. I created micro-computed tomography scans for 231 teeth from 77 individuals (balanced by males and females). We have histologically sectioned all 231 teeth and analysis is proceeding. We hope be able to answer whether a slowing of enamel development like what we identified in England also occurred in Poland.

As part of this query, I also examined the relationship between internal enamel structures and final enamel thickness in deciduous teeth (baby teeth) from Medieval and Modern England and found several significant correlations. This research helped establish a baseline of relationships that I then used to build a computer model of enamel development. With enamel growth data from five modern human teeth, an Applied Mathematics colleague at the Flatiron Institute (New York City, USA) and I have been using Machine Learning and Artificial Intelligence to model the progression of ameloblasts across crown formation time and have been able to model the mechanisms and parameters needed for ameloblasts to produce enamel of different thicknesses. This Machine Learning/AI study allows for a preliminary look at whether relationships between incremental variables and enamel thickness follow the same trends as modern humans and will allow us to predict internal growth rates of teeth without cutting them open using histological sectioning.

Another exciting project that came out of this grant is a collaboration with a Physicist at Lawrence Berkeley National Laboratory (California, USA). Together, we examined the evolution of enamel crystallite ultrastructure across the last 18 million years of human history. We were able to perform state of the art phase image contrast x-ray microscopy at the Advanced Light Source synchrotron in Berkeley, California and on fossil specimens that are rarely allowed outside of their country of origin. We are working on a paper from the results of this study which will examine the relationship and evolution of enamel crystallite organization, diet, and enamel thickness across apes, with a particular emphasis on genus Homo.

Project results were disseminated at four international conferences: the 92nd and 93rd Annual Meetings of the American Association of Biological Anthropologists (2023 and 2024), International Society for Dental Morphology (2022), as well as the American Physical Society Meeting (2023). Results were shared with a Grade 4 class in Virginia, USA as part of the Skype a Scientist Program and the Tooth Talk Society for international dental researchers. Finally, a two-part seminar series titled “Using Enamel to Understand Human Evolution” was given to the University of Pittsburgh’s Department of Oral and Craniofacial Biology in the School of Dental Medicine. Two research articles resulting from this project have been published, three are in review, and five more are in preparation. During the project, I received training in histological methods of tooth preparation, new microCT systems, and polarization-dependent Imaging Contrast (PIC) imaging using photoemission electron microscopy (PEEM) at the Advanced Light Source synchrotron facility in Berkeley, California.
My study has the potential to transform the way enamel thickness and dental development is used in palaeoanthropology and dental biology. I have integrated multiple enamel developmental mechanisms with the study of enamel thickness variation across multiple species and methods. I have expanded the original plan of study to include machine learning application as well as synchrotron imaging of ultra-fine crystalline structures in enamel. The output of my research will show how a species’ growth and development can influence and/or constrain the ways that enamel of a particular thickness is produced. By incorporating multiple modern human groups, members of the genus Homo, new cutting-edge virtual-imaging technology, and methods of measurement, this research integrates dental development and enamel thickness in a way that has been hoped for, but never yet achieved. Together, this research will form the basis of new research into how the structure and development of baby teeth impact an individual later in life. Results will be of interest to anthropologists, human biologists, archaeologists, as well as the general public.
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