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The use and domestication of Theobroma cacao during the mid-Holocene in the upper Amazon

Zarrillo, Sonia, Gaikwad, Nilesh, Lanaud, Claire, Powis, Terry, Viot, Christopher, Lesur, Isabelle, Fouet, Olivier, Argout, Xavier, Guichoux, Erwan, Salin, Franck, Solorzano, Rey Loor, Bouchez, Olivier, Vignes, Hélène, Severts, Patrick, Hurtado, Julio, Yepez, Alexandra, Grivetti, Louis, Blake, Michael, Valdez, Francisco·2018·Nature Ecology & Evolution

Abstract

Cacao (Theobroma cacao L.) is an important economic crop, yet studies of its domestication history and early uses are limited. Traditionally, cacao is thought to have been first domesticated in Mesoamerica. However, genomic research shows that T. cacao's greatest diversity is in the upper Amazon region of northwest South America, pointing to this region as its centre of origin. Here, we report cacao use identified by three independent lines of archaeological evidence-cacao starch grains, absorbed theobromine residues and ancient DNA-dating from approximately 5,300 years ago recovered from the Santa Ana-La Florida (SALF) site in southeast Ecuador. To our knowledge, these findings constitute the earliest evidence of T. cacao use in the Americas and the first unequivocal archaeological example of its pre-Columbian use in South America. They also reveal the upper Amazon region as the oldest centre of cacao domestication yet identified.

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Research works printed but not linked: 51

  1. Powis, T. G., Cyphers, A., Gaikwad, N. W., Grivetti, L. & Cheong, K. Cacao use and the San Lorenzo Olmec. Proc. Natl Acad. Sci. USA 108, 8595–8600 (2011). · DOI
  2. Henderson, J. S., Joyce, R. A., Hall, G. R., Hurst, W. J. & McGovern, P. E. Chemical and archaeological evidence for the earliest cacao beverages. Proc. Natl Acad. Sci. USA 104, 18937–18940 (2007). · DOI
  3. Stuart, D. in Chocolate in Mesoamerica: A Cultural History of Cacao (ed. McNeil, C. L.) 184–201 (Univ. Press of Florida, Gainesville, 2009). · DOI
  4. Crown, P. L. & Hurst, W. J. Evidence of cacao use in the Prehispanic American Southwest. Proc. Natl Acad. Sci. USA 106, 2110–2113 (2009). · DOI
  5. Washburn, D. K., Washburn, W. N. & Shipkova, P. A. Cacao consumption during the 8th century at Alkali Ridge, southeastern Utah. J. Arch. Sci. 40, 2007–2013 (2013). · DOI
  6. Washburn, D. K., Washburn, W. N., Shipkova, P. A. & Pelleymounter, M. A. Chemical analysis of cacao residues in archaeological ceramics from North America: considerations of contamination, sample size and systematic controls. J. Arch. Sci. 50, 191–207 (2014). · DOI
  7. Grivetti, L. H. & Shapiro, H.-Y. (eds) Chocolate, History, Culture, and Heritage (John Wiley & Sons, Hoboken, 2009). · DOI
  8. Hurst, W. J., Tarka, S. M. Jr, Powis, T. G., Valdez, F.Jr & Hester, T. R. Cacao usage by the earliest Maya civilization. Nature 418, 289–290 (2002). · DOI
  9. Powis, T. G., Valdez, F., Hester, T. R., Hurst, W. J. & Tarka, S. M. Spouted vessels and cacao use among the Preclassic Maya. Lat. Am. Antiq. 13, 85–106 (2002). · DOI
  10. McNeil, C. L. Chocolate in Mesoamerica: A Cultural History of Cacao (Univ. Press of Florida, Gainesville, 2009). · DOI
  11. Motamayor, J. C. et al. Cacao domestication I: the origin of the cacao cultivated by the Mayas. Heredity 89, 380–386 (2002). · DOI
  12. Motamayor, J. C. et al. Geographic and genetic population differentiation of the Amazonian chocolate tree (Theobroma cacao L.). PLoS ONE 3, e3311 (2008). · DOI
  13. Loor Solorzano, R. G. et al. Insight into the wild origin, migration and domestication history of the fine flavour Nacional Theobroma cacao L. variety from Ecuador. PLoS ONE 7, e48438 (2012). · DOI
  14. Thomas, E. et al. Present spatial diversity patterns of Theobroma cacao L. in the neotropics reflect genetic differentiation in Pleistocene refugia followed by human-influenced dispersal. PLoS ONE 7, e47676 (2012). · DOI
  15. Valdez, F. in The Handbook of South American Archaeology (eds Silverman, H. & Isbell, W. H.) 865–888 (Springer, New York, 2008). · DOI
  16. Cuatrecasas, J. Cacao and its allies, a taxonomic revision of the genus.Theobroma. Contr. US Natl Herb. 35, 379–614 (1964).
  17. Walker, T. in Chocolate: History, Culture, and Heritage (eds Grivetti, L. E. & Shapiro, H.-Y.) 543–558 (John Wiley & Sons, Hoboken, 2009).
  18. Bletter, N. & Daly, D. C. in Chocolate in Mesoamerica: A Cultural History of Cacao (ed. McNeil, C. L.) 31–68 (Univ. Press of Florida, Gainesville, 2009). · DOI
  19. Valdez, F., Guffroy, J., de Saulieu, G., Hurtado, J. & Yepes, A. Découverte d’un site cérémoniel formatif sur le versant oriental des Andes. C. R. Palevol. 4, 369–374 (2005). · DOI
  20. Zarrillo, S. Human Adaptation, Food Production, and Cultural Interaction During the Formative Period in Highland Ecuador. PhD dissertation, Univ. Calgary (2012).
  21. Lanaud, C., Loor, R. G., Zarrilo, S. & Valdez, F. Origen de la domesticacion del cacao y su uso temprano en el Ecuador. Nuestro Patrimonio 12, 12–14 (2012).
  22. Reichert, E. T. The Differentiation and Specificity of Starches in Relation to Genera, Species, Etc. (Carnegie Institution of Washington, Washington DC, 1913).
  23. Schmieder, R. L. & Keeney, G. Characterization and quantification of starch in cocoa beans and chocolate products. J. Food. Sci. 45, 555–557 (1980). · DOI
  24. Hammerstone, J. F., Romanczyk, L. J. & Martin Aitken, W. Purine alkaloid distribution with Herrania and Theobroma. Phytochemistry 35, 1237–1240 (1994). · DOI
  25. Pääbo, S. et al. Genetic analyses from ancient DNA. Annu. Rev. Genet. 38, 645–679 (2004). · DOI · Paper page
  26. Parducci, L. et al. Molecular- and pollen-based vegetation analysis in lake sediments from central Scandinavia. Mol. Ecol. 22, 3511–3524 (2013). · DOI
  27. Willerslev, E. et al. Fifty thousand years of Arctic vegetation and megafaunal diet. Nature 506, 47–51 (2014). · DOI · Paper page
  28. Carpenter, M. L. et al. Pulling out the 1%: whole-genome capture for the targeted enrichment of ancient DNA sequencing libraries. Am. J. Hum. Genet. 93, 852–864 (2013). · DOI
  29. Argout, X. et al. The genome of Theobroma cacao. Nat. Genet. 43, 101–108 (2011). · DOI
  30. Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000). · DOI
  31. Hansen, A., Willerslev, E., Wiuf, C., Mourier, T. & Arctander, P. Statistical evidence for miscoding lesions in ancient DNA templates. Mol. Biol. Evol. 18, 262–265 (2001). · DOI
  32. Silva, P. & Oliveira-Cardoso, A. Historico das introduçoes de cacaueiro (Theobroma cacao L.) no Reconcavo da Bahia, Brasil. Revista Theobroma 10, 135–140 (1980).
  33. Mackensen, A. K., Brey, T., Bock, C. & Luna, S. Spondylus crassisquama Lamarck, 1819 as a microecosystem and the effects of associated macrofauna on its shell integrity: isles of biodiversity or sleeping with the enemy? Mar. Biodivers. 42, 443–451 (2012). · DOI
  34. Piperno, D. R. & Pearsall, D. M. The Origins of Agriculture in the Lowland Neotropics (Academic Press, New York, 1998).
  35. Hilbert, L. et al. Evidence for mid-Holocene rice domestication in the Americas. Nat. Ecol. Evol. 1, 1693–1698 (2017). · DOI
  36. Biehl, B. Veränderungen der subcellulären struktur in keimblättern von kakaosamen (Theobroma cacao L.) während der fermentation und troeknung. Z. Lebensm. Unters. Forch. 153, 137–150 (1973). · DOI
  37. Redgwell, R. J. & Hansen, C. E. Isolation and characterisation of cell wall polysaccharides from cocoa (Theobroma cacao L.) beans. Planta 210, 823–830 (2000). · DOI
  38. King, A., Powis, T. G., Cheong, K. & Gaikwad, N. Cautionary tales on the identification of caffeinated beverages in North America. J. Archaeol. Sci. 85, 30–40 (2017). · DOI
  39. Kufer, J. & McNeil, C. L. in Chocolate in Mesoamerica: A Cultural History of Cacao (ed. McNeil, C. L.) 384–407 (Univ. Press of Florida, Gainesville, 2009). · DOI
  40. Cieslak, M. et al. Origin and history of mitochondrial DNA lineages in domestic horses. PLoS ONE 5, e15311 (2010). · DOI
  41. Pääbo, S. Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification. Proc. Natl Acad. Sci. USA 86, 1939–1943 (1989). · DOI
  42. Dabney, J., Meyer, M. & Pääbo, S. in DNA Repair, Mutagenesis, and Other Responses to DNA Damage (eds Friedberg, E. C., Elledge, S. J., Lehmann, A. R., Lindahl, T. & Muzi-Falconi, M.) 19–26 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 2013). · DOI · Paper page
  43. Argout, X. et al. Towards the understanding of the cocoa transcriptome: production and analysis of an exhaustive dataset of ESTs of Theobroma cacao L. generated from various tissues and under various conditions. BMC Genomics 9, 512 (2008). · DOI
  44. Ye, J. et al. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform. 13, 134 (2012). · DOI
  45. Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. & Barton, G .J. Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009). · DOI
  46. Ewing, B., Hillier, L., Wendl, M. C. & Green, P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8, 175–185 (1998). · DOI
  47. Hamelin, C., Sempere, G., Jouffe, V. & Ruiz, M. TropGeneDB, the multi-tropical crop information system updated and extended. Nucleic Acids Res. 41, D1172–D1175 (2013). · DOI
  48. Argout, X. et al. The cacao Criollo genomev2.0: an improved version of the genome for genetic and functional genomic studies. BMC Genomics 18, 730 (2017). · DOI
  49. Cruz-Dávalos, D. I. et al. Experimental conditions improving in-solution target enrichment for ancient DNA. Mol. Ecol. Resour. 17, 508–522 (2017). · DOI · Paper page
  50. Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26, 589–595 (2010). · DOI · Paper page
  51. GBIF Backbone Taxonomy (GBIF Secretariat, 2017); https://doi.org/10.15468/39omei · DOI

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Metadata

Authors
Zarrillo, S., Gaikwad, N., Lanaud, C., Powis, T., Viot, C., Lesur, I., Fouet, O., Argout, X., Guichoux, E., Salin, F., Solorzano, R. L., Bouchez, O., Vignes, H., Severts, P., Hurtado, J., Yepez, A., Grivetti, L., Blake, M., & Valdez, F.
Venue
Nature Ecology & Evolution
Published
2018-10-29
Volume
2
Issue
12
Pages
1879-1888
ISSN
2397-334X
Cited by
173
References
2
Language
en

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CoChat. (2026). Citation check: The use and domestication of Theobroma cacao during the mid-Holocene in the upper Amazon. https://app.cochat.ai/papers/10.1038/s41559-018-0697-x
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Zarrillo, S., Gaikwad, N., Lanaud, C., Powis, T., Viot, C., Lesur, I., Fouet, O., Argout, X., Guichoux, E., Salin, F., Solorzano, R. L., Bouchez, O., Vignes, H., Severts, P., Hurtado, J., Yepez, A., Grivetti, L., Blake, M., & Valdez, F. (2018). The use and domestication of Theobroma cacao during the mid-Holocene in the upper Amazon. Nature Ecology & Evolution. https://doi.org/10.1038/s41559-018-0697-x