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Ancient proteins provide evidence of dairy consumption in eastern Africa

Bleasdale, Madeleine, Richter, Kristine K., Janzen, Anneke, Brown, Samantha, Scott, Ashley, Zech, Jana, Wilkin, Shevan, Wang, Ke, Schiffels, Stephan, Desideri, Jocelyne, Besse, Marie, Reinold, Jacques, Saad, Mohamed, Babiker, Hiba, Power, Robert C., Ndiema, Emmanuel, Ogola, Christine, Manthi, Fredrick K., Zahir, Muhammad, Petraglia, Michael, Trachsel, Christian, Nanni, Paolo, Grossmann, Jonas, Hendy, Jessica, Crowther, Alison, Roberts, Patrick, Goldstein, Steven T., Boivin, Nicole·2021·Nature Communications
DOI 10.1038/s41467-020-20682-3PMC PMC7841170
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Abstract

Consuming the milk of other species is a unique adaptation of Homo sapiens , with implications for health, birth spacing and evolution. Key questions nonetheless remain regarding the origins of dairying and its relationship to the genetically-determined ability to drink milk into adulthood through lactase persistence (LP). As a major centre of LP diversity, Africa is of significant interest to the evolution of dairying. Here we report proteomic evidence for milk consumption in ancient Africa. Using liquid chromatography tandem mass spectrometry (LC-MS/MS) we identify dairy proteins in human dental calculus from northeastern Africa, directly demonstrating milk consumption at least six millennia ago. Our findings indicate that pastoralist groups were drinking milk as soon as herding spread into eastern Africa, at a time when the genetic adaptation for milk digestion was absent or rare. Our study links LP status in specific ancient individuals with direct evidence for their consumption of dairy products.

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Fig. 1 Locations of sampled archaeological sites in Kenya and Sudan in relation to the distribution of main lactase persistence alleles found in modern populations in Africa. A 13907*G, B 13915*G, C 14009*G, and D 14010*C. Filled circles represent sites where milk proteins were identified in dental calculus samples, and empty circles are sites where samples did not yield milk proteins. The map was created for this study by Michelle O’Reilly (Graphic Designer for the Max Planck Institute for the Science of Human History, Jena, Germany) using QGIS 3.12 [https://qgis.org/en/site/] and the Natural Earth Database from [https://www.naturalearthdata.com/downloads/] and Adobe Illustrator CC. Heat maps were generated using published LP distribution frequencies6.
Fig. 1 Locations of sampled archaeological sites in Kenya and Sudan in relation to the distribution of main lactase persistence alleles found in modern populations in Africa. A 13907*G, B 13915*G, C 14009*G, and D 14010*C. Filled circles represent sites where milk proteins were identified in dental calculus samples, and empty circles are sites where samples did not yield milk proteins. The map was created for this study by Michelle O’Reilly (Graphic Designer for the Max Planck Institute for the Science of Human History, Jena, Germany) using QGIS 3.12 [https://qgis.org/en/site/] and the Natural Earth Database from [https://www.naturalearthdata.com/downloads/] and Adobe Illustrator CC. Heat maps were generated using published LP distribution frequencies6.CC BY · PubMed Central
Fig. 2 Map of sites with calculus containing milk proteins. A Area of study in relation to the spread of cattle-based pastoralism across Africa (after Marshall and Hildebrand35). B Pie charts showing the number of individuals per site with milk proteins (shaded) proportionate to the total number of individuals that passed screening with Oral Signature Screening Database (see “Methods” and Supplementary Note 3 for full details). Neolithic: ~8000–5500 cal. bp; Kerma: ~4450–3450 cal. bp; Pastoral Neolithic: ~3500–1200 cal. bp; Meroitic: ~2300–1600 cal. bp. The maps were created for this study by Michelle O’Reilly (Graphic Designer for the Max Planck Institute for the Science of Human History, Jena, Germany) using QGIS 3.12 [https://qgis.org/en/site/] and the Natural Earth Database from [https://www.naturalearthdata.com/downloads/]. Additional edits were made using Adobe Illustrator CC.
Fig. 2 Map of sites with calculus containing milk proteins. A Area of study in relation to the spread of cattle-based pastoralism across Africa (after Marshall and Hildebrand35). B Pie charts showing the number of individuals per site with milk proteins (shaded) proportionate to the total number of individuals that passed screening with Oral Signature Screening Database (see “Methods” and Supplementary Note 3 for full details). Neolithic: ~8000–5500 cal. bp; Kerma: ~4450–3450 cal. bp; Pastoral Neolithic: ~3500–1200 cal. bp; Meroitic: ~2300–1600 cal. bp. The maps were created for this study by Michelle O’Reilly (Graphic Designer for the Max Planck Institute for the Science of Human History, Jena, Germany) using QGIS 3.12 [https://qgis.org/en/site/] and the Natural Earth Database from [https://www.naturalearthdata.com/downloads/]. Additional edits were made using Adobe Illustrator CC.CC BY · PubMed Central
Fig. 3 Milk β-lactoglobulin proteins identified from ancient dental calculus of individuals from Sudan and Kenya. A 3D model of β-lactoglobulin showing location of species variant sites. B Variations in the amino acid sequence at position 71 and 148 can be used to distinguish between Bos, Ovis and Capra. C Spectrum for TPEVDKEALEK specific to Capra from individual Z708. D Spectrum for TPEVDDEALEKFDK from individual DA323. The deamidation of asparagine results in its conversion to aspartic acid so an unmodified (D) is indistinguishable from (de.N); therefore, this milk peptide is identified as Bovinae/Ovis. The 3D image of β-lactoglobulin is from SwissModel [https://swissmodel.expasy.org/repository/uniprot/P02754].
Fig. 3 Milk β-lactoglobulin proteins identified from ancient dental calculus of individuals from Sudan and Kenya. A 3D model of β-lactoglobulin showing location of species variant sites. B Variations in the amino acid sequence at position 71 and 148 can be used to distinguish between Bos, Ovis and Capra. C Spectrum for TPEVDKEALEK specific to Capra from individual Z708. D Spectrum for TPEVDDEALEKFDK from individual DA323. The deamidation of asparagine results in its conversion to aspartic acid so an unmodified (D) is indistinguishable from (de.N); therefore, this milk peptide is identified as Bovinae/Ovis. The 3D image of β-lactoglobulin is from SwissModel [https://swissmodel.expasy.org/repository/uniprot/P02754].CC BY · PubMed Central
Fig. 4 Stable isotope results for humans and fauna. A Bone collagen stable carbon and nitrogen isotope values for Lukenya Hill and Molo Cave. *Values previously published for Lukenya Hill53. B Tooth enamel stable carbon and oxygen isotope values for Lukenya Hill, Cole’s Burial and Molo Cave. The Cephalophus, Dendrohyrax, and Heterohyrax were sampled from Lukenya Hill.
Fig. 4 Stable isotope results for humans and fauna. A Bone collagen stable carbon and nitrogen isotope values for Lukenya Hill and Molo Cave. *Values previously published for Lukenya Hill53. B Tooth enamel stable carbon and oxygen isotope values for Lukenya Hill, Cole’s Burial and Molo Cave. The Cephalophus, Dendrohyrax, and Heterohyrax were sampled from Lukenya Hill.CC BY · PubMed Central

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Authors
Bleasdale, M., Richter, K. K., Janzen, A., Brown, S., Scott, A., Zech, J., Wilkin, S., Wang, K., Schiffels, S., Desideri, J., Besse, M., Reinold, J., Saad, M., Babiker, H., Power, R. C., Ndiema, E., Ogola, C., Manthi, F. K., Zahir, M., Petraglia, M., Trachsel, C., Nanni, P., Grossmann, J., Hendy, J., Crowther, A., Roberts, P., Goldstein, S. T., & Boivin, N.
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2021-01-27
Volume
12
Issue
1
ISSN
2041-1723
DOI
10.1038/s41467-020-20682-3
PMC
PMC7841170
Cited by
87
References
7
Language
en
Licence
Funders
Max-Planck-Gesellschaft

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