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Teeth hold valuable clues for understanding ancient climates and evolutionary processes

Increasing climate variability has been implicated as a driving force for the origins of our species (Homo sapiens) over 300,000 years ago, our genus (Homo) several million years earlier, and our more ancient great ape ancestors. The variability selection hypothesis posits that the landmark evolutionary features of humans, such as upright bipedal walking, large brains, and refined cognitive ability, arose in response to complex environmental processes in Africa. This influential theory has received support from environmental indicators including sediment sequences and changes in the composition of ancient animal communities. Yet these methods yield information on the scale of thousands of years or more, making it difficult to understand how climate patterns directly impacted ancient humans and their evolutionary kin on the time scale of an individual’s life.

The fossil record consists predominantly of teeth, which contain unique information about childhood development and concurrent environmental and dietary chemistry. For example, when individuals drink water, naturally occurring oxygen variants (isotopes) are quickly incorporated into the minerals of growing teeth and bone. Oxygen isotope values (δ¹⁸O) in water vary with temperature, altitude, precipitation, and evaporation cycles. In seasonal environments surface water is enriched in the heavy isotope (¹⁸O) during periods of warm or dry weather, raising δ¹⁸O, while the opposite occurs during cool or wet periods. Because teeth do not remodel during life, and tooth enamel is rarely modified after burial, these faithful climate records can be recovered from fossil teeth thousands and even millions of years later—facilitating tests of whether ancient climate variation directly impacted our evolutionary history.

Australian innovations super-charge interdisciplinary collaboration

Tooth enamel is typically sampled with hand-held drills to recover the record of oxygen inputs from water and food preserved in the hard mineral composite. This coarse drilling method yields spatially-blurred powdered samples formed over a substantial and unknown period of time, precluding the identification of precise seasonal environmental patterns. To resolve this dilemma, an international team of researchers is leveraging the exceptional potential of the stable isotope sensitive high-resolution ion microprobe (SHRIMP SI) developed at the Australian National University (ANU). Led by Griffith University’s Professor Tanya Smith and ANU’s Professor Ian Williams, the team employs SHRIMP SI to measure δ¹⁸O microscopically from carefully-prepared thin slices of teeth.

Smith and Williams
Tanya Smith and Ian Williams developed a new method to analyse δ18O from thin sections of teeth. Here they are measuring a prehistoric human tooth in the ANU SHRIMP Laboratory, an experiment that was filmed for the Australian Academy of Science by Bohdee Media. Photo: Petra Vaiglova

In order to make these micro-measurements, a caesium ion beam under high vacuum is used to ablate tiny sequential spots from the enamel, and the ionised oxygen emitted from each spot is transferred to a sophisticated mass analyser. Each δ¹⁸O measurement takes seven minutes, and values are calibrated against a standard to correct for any analytical variance over the approximately 8- to 24-hour data collection period for each tooth. Smith’s team has shown that δ¹⁸O values of enamel measured by SHRIMP SI are nearly identical to those from the gold standard wet chemistry approach (silver phosphate microprecipitation), confirming the fidelity of this approach for oxygen isotope recovery. Excitingly, the ANU’s SHRIMP Laboratory is the best facility worldwide for this cutting-edge dental research.

Professor Smith was drawn to Australia, in part, by the potential of the SHRIMP for investigating human evolutionary biology. She completed her doctorate in Anthropological Sciences at Stony Brook University in New York, led a prolific research unit in the Max Planck Institute for Evolutionary Anthropology in Leipzig, and served on the Harvard University faculty prior to joining Griffith University in 2016. Emeritus Professor Williams, a pioneering scholar in the use of SHRIMP systems for Earth Science, has worked with SHRIMP since its first application in 1980—patiently assisting and training researchers at the ANU SHRIMP lab for over 40 years. Smith and Williams’ initial research partnership in 2017 has since led to their selection as finalists for the 2019 Eureka Award for Excellence in Interdisciplinary Research, and funding from the Australian Academy of Science’s Regional Collaboration Programme and the Australian Research Council’s Discovery Program.

Neanderthals did it tough in prehistoric Europe

Their initial research at the ANU SHRIMP yielded the most detailed study ever undertaken of ancient seasonality in two 250,000 year-old Neanderthals and a recent human child. They microsampled δ¹⁸O sequentially from enamel preserved in thin tooth slices, relating this to formation times, and in two instances, calendar ages. The teeth of humans and other primates start to develop prior to birth, forming incrementally through time, and precise developmental records can be quantified using a light microscope. Subtle developmental defects (accentuated lines) in the enamel can be mapped and aged from daily lines formed after birth, which are preserved in first molars (neonatal line). They confirmed that the region of France where the fossils were discovered was cooler and more seasonal 250,000 years ago than it was 5,000 years ago, when the unlucky modern human child lived and died. In a surprising twist⎯ both Neanderthal children were exposed to lead at least twice during cooler times of the year, likely through consumption of contaminated food and/or water.

Neanderthal Molar Cusp
Left: Magnified thin section of a 250,000 year-old Neanderthal molar cusp showing the progression of growth marked by successive accentuated lines (dotted lines, age in days). Right: oxygen isotope values (VSMOW scale) sampled at weekly intervals along the enamel-dentine junction of this tooth (diagonal boundary) from birth to 2.8 years of age (time scale is non-linear). Three prehistoric summers and two winters are evident, revealing that this Neanderthal was born in the spring. (Images: Smith et al. 2018.)

These findings raise intriguing questions about Neanderthal behaviour that require further study. For example, this approach could facilitate much-needed tests of theories about the impact of climate change on the disappearance of Neanderthals. Youngsters with unworn teeth are especially helpful. Although numerous Neanderthal fossils have been unearthed, coaxing teeth from the curators of collections for this kind of study is a tall order. But the more teeth scientists examine in such detail, the more information will be available about the lived experiences of ancient people. 

New views of an ancient African environment

Smith and William’s most recent collaborative study leverages these analytical breakthroughs to establish an oxygen isotope record from modern primates across equatorial Africa—covering 45 years of tooth formation sampled nearly every week. The project includes humans’ closest-living relative, chimpanzees, and contrasts δ¹⁸O values from primates with different dietary preferences within similar ecosystems (chimpanzees and monkeys in dense forests), and values from primates with similar diets in different ecosystems (baboons in forest-savannah mosaic, grassland, and highland environments). Remarkably, the modern African primate teeth show annual and semiannual seasonal rainfall patterns across a broad range of environments and diets.

The team then turned their attention to an enigmatic 17-17.5 million year-old large-bodied ape called Afropithecus turkanensis, which was first described by Richard and Meave Leakey in 1986. Afropithecus is found in a part of Kenya that is currently very arid and largely devoid of trees, but had been thought to be much like the dense tropic forests where most modern great apes live. It turns out that the δ¹⁸O fluctuations in two fossil apes’ teeth are intermediate between baboons living across a gradient of aridity, and modern forest-dwelling chimpanzees. It appears that this fossil ape consumed seasonally variable food and water sources, and its reliance on fallback foods during dry seasons may have led to novel dental features for hard-object feeding. Considered in the light of its unusually thick tooth enamel and slow dental development—the seasonal variation experienced by Afropithecus over geological time is consistent with the idea that environmental variation was an important driver in the early evolution of humanity’s closest living kin — the great apes.

Precipitation
Left: Average annual precipitation map of δ¹⁸O (‰, VSMOW scale) in Africa taken from www.waterisotopes.org. White numbers indicate locations of primate samples for this project. Right inset: high δ¹⁸O values are due to sustained dry periods, while low values represent approximately annual rainfall events of shorter duration.

Results from modern and fossil apes also permit more refined assessments of previous δ¹⁸O values for Plio-Pleistocene hominins from equatorial Africa. It turns out that the two 17-17.5 million year-old Afropithecus individuals show the same range of δ¹⁸O variation as the entire set of bulk values from 101 east African fossil hominins spanning 4 million years—a striking result that challenges existing models of ecological and evolutionary change. This is important because variations in rainfall patterns influence the fundamental structure of natural habitats. Dense tropical forests are sustained by fairly consistent rainfall and short dry seasons, while woodland communities in more arid environments have smaller trees, less dense canopies, and more deciduous trees. In regions with prolonged dry seasons and low annual rainfall, savannah landscapes abound. Models of early hominin evolution commonly postulate that upright bipedal walking became habitual once seasonal savannah-woodland environments began to predominate and our African ape ancestors ceased being able to rely on closely-spaced trees for routine arboreal locomotion. By revealing real-time historical and prehistoric environmental variation on a near-weekly basis, extraordinary behavioral and ecological variability can be recovered—permitting future tests of influential models of early human evolution.

For their latest project, Professors Smith and Williams recruited Dr. Daniel Green—an expert in the interpretation of oxygen isotopic data for palaeoenvironmental reconstruction, who obtained his PhD from Harvard University under Smith’s supervision. Not coincidentally, two decades prior to the Afropithecus analysis at the ANU, Smith had been invited to study these same teeth by her doctoral supervisor Professor Lawrence Martin. This formative experience led to her long-standing curiosity about this fossil ape, especially with its particularly thick tooth enamel and slow dental development that is strikingly similar to modern African apes. In this case, a multigenerational transfer of knowledge has helped to advance our understanding of ancient African landscapes.

A new approach to a significant problem
Scientists
Left: Tanya Smith with her former doctoral supervisor Lawrence Martin and Meave Leakey, co-discoverer of Afropithecus—not far from the Kenyan fossil site (Kalodirr) where it was recovered. Smith published the first study of the fossil ape’s enamel thickness and molar development while she was still a graduate student at Stony Brook University. Right: Tanya Smith with her former doctoral student Daniel Green, who led the recent paleoenvironmental reconstruction of Kalodirr published with Smith, Williams, and an international collaborative team.

Climate variation also has profound effects on food abundance, and primates show diverse anatomical and behavioural adaptations to survive when preferred foods are unavailable. A lack of precise palaeoclimate proxies has made it nearly impossible to test whether climate variation was a driving force for human origins, or what the current period of climatic instability might mean for the future of humanity. Several fine-scaled climate proxies have been developed for the environmental sciences, including isotopic studies of ancient otoliths (fish ear bones), mollusc shells, fossil corals, and tree rings, yet these items are rarely recovered from African hominin localities—the region where our genus and species originated. Extracting precipitation records from tooth enamel ensures that this environmental snapshot was experienced directly by the individual in question, not just sometime within the broad standard error of most geochronological age estimates for archaeological layers.

Dr. Green and Professors Smith and Williams are now teaming up with Dr. Kyalo Manthi of the National Museums of Kenya, and Dr. Kevin Uno at Columbia University, aiming to apply this cutting-edge approach to additional fossils in order to determine whether ancient climate change can be related to key transitions in great ape and human evolution. Teeth from several hominins and ancient apes will be analysed with the ANU’s SHRIMP SI and financed by Stony Brook University’s Turkana Basin Institute. This will contextualise previous ‘fossil-first’ studies that have not delivered on their full potential due to the lack of both sound comparative data and crucial experimental studies needed to resolve potential complications. The team’s approach could be extended to faunal remains from rural Australia for insight into undocumented historic climate conditions, as well as prehistoric environmental changes that have shaped Australia’s unique modern landscapes. These interdisciplinary methods will push the boundaries of research and open up new opportunities for scientists worldwide who specialise in understanding ancient life forms, reconstructing past environments, studying endangered animals, and investigating life history in prehistoric humans. With the help of Australia’s flagship SHRIMP—the future looks bright for such novel research partnerships!

Author

Professor Tanya SmithTanya Smith is a Professor in the Australian Research Centre for Human Evolution (ARCHE) and the Griffith Centre for Social and Cultural Research (GCSCR) at Griffith University. She has previously held a professorship at Harvard University, and fellowships at the Radcliffe Institute for Advanced Study and the Max Planck Institute for Evolutionary Anthropology.

Professor Smith’s area of expertise is the study of tooth growth and structure, as detailed in The Tales Teeth Tell – her popular science book published by MIT Press. Her research has been funded by the Australian Academy of Science, the US National Science Foundation, the Leakey Foundation, and the Wenner-Gren Foundation for Anthropological Research. She has published in Nature, Science Advances, and Proceedings of the National Academy of Sciences, and these works have been featured in The New York Times, National Geographic, Nature, Science, Smithsonian, and Discovery magazines, as well as through American, Australian, British, Canadian, French, Irish, German, New Zealand, and Singaporean broadcast media.

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