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Barium distributions in teeth reveal early-life dietary transitions in primates

Nature volume 498, pages 216–219 (2013)Cite this article

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Abstract

Early-life dietary transitions reflect fundamental aspects of primate evolution and are important determinants of health in contemporary human populations1,2. Weaning is critical to developmental and reproductive rates; early weaning can have detrimental health effects but enables shorter inter-birth intervals, which influences population growth3. Uncovering early-life dietary history in fossils is hampered by the absence of prospectively validated biomarkers that are not modified during fossilization4. Here we show that large dietary shifts in early life manifest as compositional variations in dental tissues. Teeth from human children and captive macaques, with prospectively recorded diet histories, demonstrate that barium (Ba) distributions accurately reflect dietary transitions from the introduction of mother’s milk through the weaning process. We also document dietary transitions in a Middle Palaeolithic juvenile Neanderthal, which shows a pattern of exclusive breastfeeding for seven months, followed by seven months of supplementation. After this point, Ba levels in enamel returned to baseline prenatal levels, indicating an abrupt cessation of breastfeeding at 1.2 years of age. Integration of Ba spatial distributions and histological mapping of tooth formation enables novel studies of the evolution of human life history, dietary ontogeny in wild primates, and human health investigations through accurate reconstructions of breastfeeding history.

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Figure 1: Barium distribution in human deciduous teeth.
Figure 2: Barium distribution reveals natural and truncated weaning.
Figure 3: Dietary transitions in a Neanderthal permanent first molar.

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Acknowledgements

L. Reynard, N. Tuross and F. Bidlack provided comments on this project. C. Amarasiriwardena and N. Lupoli provided expertise in macaque milk analysis. Fossil samples were provided by M. Toussaint, R. Gruen and M.-H. Moncell. The CHAMACOS study is funded by the US Environmental Protection Agency (RD 83171001 and RD 82670901 to B.E.) and the US National Institutes of Environmental Health Sciences (PO1 ES009605 to B.E.). Support for macaque data collection was provided by NSF BCS-0921978 (K.H.); milk samples were made possible through the ARMMS program (Archive of Rhesus Macaque Milk Samples). Histological study of the Scladina Neanderthal was funded by the Max Planck Institute for Evolutionary Anthropology. R.J.-B. is supported by Australian Research Council Discovery Grant (DP120101752) and SCU postdoctoral Fellowship grant. P.D. was supported by Australian Research Council Project Grant (LP100200254) that draws collaborative funding from Agilent Technologies and Kennelec Scientific. M.A. is supported by a National Institute of Environmental Health Sciences grant 4R00ES019597-03. C.A. and M.A. are supported by NHMRC grant APP1028372.

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Author notes

  1. Christine Austin and Tanya M. Smith: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, 10029, New York, USA

    Christine Austin & Manish Arora

  2. Environmental and Occupational Medicine and Epidemiology, Harvard School of Public Health, Boston, 02115, Massachusetts, USA

    Christine Austin & Manish Arora

  3. Institute of Dental Research, Westmead Millennium Institute, Westmead Hospital, and Oral Pathology and Oral Medicine, Faculty of Dentistry, University of Sydney, Sydney, 2145, New South Wales, Australia

    Christine Austin & Manish Arora

  4. Department of Human Evolutionary Biology, Harvard University, Cambridge, 02138, Massachusetts, USA

    Tanya M. Smith & Katie Hinde

  5. Center for Environmental Research and Children’s Health, School of Public Health, University of California, Berkeley, 94720, California, USA

    Asa Bradman & Brenda Eskenazi

  6. California National Primate Research Center, Davis, 95616, California, USA

    Katie Hinde

  7. Southern Cross GeoScience, Southern Cross University, Lismore, 2480, New South Wales, Australia

    Renaud Joannes-Boyau

  8. Elemental Bio-imaging Facility, University of Technology Sydney, Sydney, 2007, New South Wales, Australia

    David Bishop, Dominic J. Hare & Philip Doble

  9. The Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, Victoria 3010, Australia,

    Dominic J. Hare

Authors
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Contributions

C.A., T.M.S. and M.A. designed the study, undertook the elemental and histological analysis, and wrote the manuscript. A.B. and B.E. designed and analysed the human study. K.H. designed the macaque lactation study and collected samples. R.J.-B. analysed the Payre Neanderthal tooth in the Supplementary Information and assessed diagenetic alteration. C.A., D.J.H., D.B. and P.D. undertook elemental imaging of tooth samples. All authors contributed to the interpretation of the results, in addition to editing the manuscript.

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Correspondence to Manish Arora.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures 1-10, Supplementary Tables 1-5, a Supplementary Discussion, Supplementary Methods and additional references. (PDF 2164 kb)

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Austin, C., Smith, T., Bradman, A. et al. Barium distributions in teeth reveal early-life dietary transitions in primates. Nature 498, 216–219 (2013). https://doi.org/10.1038/nature12169

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