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Citation:
Austin*, C., Smith*, T.M., Bradman, A., Hinde, K., Joannes-Boyau, R., Bishop, D., Hare, D.J., Doble, P., Eskenazi, B., Arora, M.(in press) Barium distributions in teeth reveal early life dietary transitions in primates. Nature.
* These authors contributed equally to this work.


The Study in Brief

Early life dietary transitions reflect fundamental aspects of primate evolution and are important determinants of health in living human populations. Identifying these transitions in ancient hominins has been difficult due to the lack of accurate biomarkers that are not modified during fossilization. In this study we show that major dietary shifts during infancy are accurately recorded in mineralized dental tissues, which survive in fossil remains from thousands of years ago. Teeth from human children and captive macaques with known diet histories demonstrate that barium distributions reflect dietary transitions, beginning with the onset of breast feeding and continuing through the weaning process. Barium levels in dental tissues formed during nursing are higher than in tissues that mineralize before birth, during solid food supplementation, or after nursing ceases. Consumption of common Figure 1commercially-available infant formula results in higher barium values than those of exclusive human breastfeeding. This approach also allows insight into ancient breastfeeding practices, as we document the first early life diet transitions in a juvenile Neanderthal, which shows a pattern of exclusive mother’s milk for seven months, followed by seven months of supplementation. After this point, barium levels returned to baseline prenatal levels, suggesting an abrupt cessation of breastfeeding at 1.2 years of age. Integration of information on the spatial distribution of elements such as barium and the precise daily record of tooth formation (Figure 1) enables novel studies of the evolution of human life history, dietary patterns in wild primates, and human health investigations through accurate reconstructions and comparisons of breastfeeding history.



Background

One of the most remarkable features of human development is that human infants are weaned much earlier than our closest ape relatives, often by several years. Although there is some variation among human cultures, this accelerated transition to foods other than mother’s milk is thought to have emerged in our ancestral history due, in part, to more cooperative infant care and access to a more nutritious diet. Shorter lactation periods can translate into shorter inter-birth intervals and higher reproductive rates. This has likely played a part in the relatively high lifetime fertility of humans, even before the advent of modern industrial food production. However there is much debate about when accelerated weaning occurred in the hominin lineage. For the past few decades researchers have relied on tooth eruption age as a direct proxy for weaning age. Yet recent investigations of wild chimpanzees have revealed that first molar eruption occurs prior to the cessation of weaning, complicating the estimation of weaning from fossilized dentitions. Other methods are needed to understand the evolution of human weaning. In this study we show that the timing of breastfeeding and the weaning process can be uncovered in tooth crowns – down to nearly the day!



The Approach

Like the rings found in tree trunks, teeth form following a regular pattern that creates permanent daily lines in enamel and dentine, which can be viewed and counted under a microscope (see examples here). This faithful record of development also includes a marked “neonatal line” formed at birth in baby teeth and the first permanent molar of monkeys and apes (including humans) (Figure 2).

Figure 2

As teeth mineralize they incorporate elements derived from dietary and environmental sources, including calcium, oxygen and small amounts of metals such as barium and lead. Using sophisticated analytical chemistry and microscopy techniques at the University of Sydney’s Faculty of Dentistry,
the Elemental Bio-imaging Facility (University of Technology, Sydney) and the Dental Hard Tissue Laboratory (Harvard University, Cambridge, MA) we were able to track fine-scale changes in barium concentration in primate teeth throughout their development. We first investigated the relationship between tooth mineralization and dietary signals in humans and monkeys of known dietary histories. Human subjects enrolled in the University of California, Berkeley's Center for the Health Assessment of Mothers and Children of Salinas (CHAMACOS) study (Monterey County, USA) provided naturally shed baby teeth along with precise records of infant diet, including the duration of breastfeeding and timing of formula introduction. Macaque teeth, milk, and dietary histories were provided through a long term lactation study at the Comparative Lactation Lab (Harvard University, Cambridge, MA) and the California National Primate Research Center (Davis, CA). Finally, we also analysed the first molar tooth of a juvenile Neanderthal from Belgium to assess weaning patterns in a Middle Paleolithic hominin.

The Results

Barium levels in the deciduous (baby) teeth of human children increase with the introduction of breast milk and/or formula following birth. Barium transfer is restricted by the placenta, resulting in low prenatal levels. Barium rises after birth from the consumption of breast milk and rises further with the introduction of formula, which has higher barium levels than breast milk (Figure 3).

figure 3Examination of molars in four captive macaques also revealed that barium is enriched in the enamel and dentine formed after birth, which peaked during periods of exclusive suckling, and declined during periods of supplementation. In one instance, it was possible to document the cessation of suckling in an individual who was abruptly separated from its mother for several weeks (leading to mammary involution and discontinuation of milk synthesis).
(Figure 4). The power of this approach is further confirmed by direct comparisons of barium levels in macaque teeth and their mother’s milk, which show similar changes through time.

Figure 4 Temporal and elemental mapping of a Neanderthal first molar (Figure 5) revealed a transition pattern similar to the macaque that weaned abruptly. Following approximately 13 days of prenatal enamel formation, barium levels near the enamel-dentine junction increase and remain elevated until approximately 227 days of age, after which they show intermediate values until 435 days of age (1.2 years). After this age barium rapidly returns to prenatal levels for the final 1.15 years of crown formation.

Figure 5

Significance

This is the first demonstration that major dietary shifts in early life are accurately recorded as elemental signals that remain apparent in primate fossil teeth. A primary aim of many tooth chemistry studies is to document dietary histories, including the evolution of human weaning, which has proven difficult due to the natural processes of decay and modification that occur after death and during fossilization. Reliable biomarkers of dietary patterns in both modern and fossil samples have been largely unavailable until now. This technique will enable the evaluation of theories regarding weaning patterns and life histories of hominin species, which have important implications for models of population growth and species replacement. Moreover, understanding exclusive breastfeeding and weaning transitions informs studies of human health. Breastfeeding is believed to reduce the risk of many illnesses in children including gastrointestinal infections, respiratory tract diseases, obesity and type 1 and 2 diabetes. Some studies have also suggested that breastfeeding can lower the risk of Sudden Infant Death Syndrome. Because maternal recall of breastfeeding after many years may be unreliable, objective biomarkers will substantially aid studies on the benefits of breastfeeding in contemporary Figure 6populations. Finally, we can now investigate the weaning process across primates with more confidence. Primatologists have relied on observations of infant suckling, nipple contact (Figure 6), and maternal rejection to investigate weaning, although these behavioral observations are not entirely accurate for assessing milk transfer. This may be especially true in late lactation when offspring sleep with their mother and likely gain nipple access at night. By applying these new techniques to primate teeth in museum collections, we can more precisely assess maternal investment across individuals within species, as well as life history evolution among species.



Contacts

Manish Arora
Department of Preventive Medicine
Icahn School of Medicine at Mt. Sinai
Box 1057
New York, NY 10029
Phone: +1 212 824 7046 (USA)/
+1 61 416 006 408 (Australia)
E-mail: manish.arora [at] mssm.edu

Tanya Smith
Department of Human Evolutionary Biology
Harvard University
Cambridge, MA 02138
Phone: +1 617 496 8259
E-mail: tsmith [at] fas.harvard.edu

Christine Austin
Institute of Dental Research
Westmead Centre for Oral Health
Westmead Hospital
Westmead, NSW 2145
Phone: +61 2 9845 8767
E-mail: christine.austin [at] sydney.edu.au

Katie Hinde
Department of Human Evolutionary Biology
Harvard University
Cambridge, MA 02138
Phone: +1 617 496 4551
E-mail: khinde [at] fas.harvard.edu

Funding Information

Funded by the US Environmental Protection Agency, US National Institutes of Environmental Health Sciences, US National Science Foundation, Australian National Health and Medical Research Council, Australian Research Council and Harvard University.

Related Online Resources

Mammals Suck Science Blog
Video/Lecture on Tooth Growth and Human Evolution