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Nature Ecology & Evolution
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The use and domestication ofTheobroma cacao during the mid-Holocene in the upper Amazon

Nature Ecology & Evolutionvolume 2, pages1879–1888 (2018)Cite this article

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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 thatT. 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 ofT. 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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Fig. 1: Locations of the four archaeological sites in Mexico, Central America and South America with the earliest evidence ofTheobroma use, as well as the species diversity distributions for the genusTheobroma17,19,58.
Fig. 2: Selected artefacts from SALF that tested positive forT. cacao andTheobroma spp. by aDNA, starch grains and theobromine analyses.
Fig. 3: Starch grains ofTheobroma spp. and other economically important plants.
Fig. 4: UPLC-MS/MS chromatograms, multiple reaction monitoring transitions and method parameters.
Fig. 5: Population structure of modern individuals and aDNA mixtures extracted from ceramic residues.

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Data availability

NCBI GenBank accession numbers of theTheobroma mitochondrial reference sequences areMF462389,MF462390 andMF462396 toMF462398. Examples of PCR amplified mitochondrial ancient DNA sequences identified asT. cacao sequences are reported in Supplementary Figs.2–4. All results on ancient DNA sequences obtained after DNA capture and containing SNPs are reported inSupplementary Information; corresponding SNPs from the collection of modern accessions, used as controls, are reported in the Tropgene database (http://tropgenedb.cirad.fr/tropgene/)52. Additional data that support the findings of this study are available from the corresponding author on reasonable request.

References

  1. Powis, T. G., Cyphers, A., Gaikwad, N. W., Grivetti, L. & Cheong, K. Cacao use and the San Lorenzo Olmec.Proc. Natl Acad. Sci. USA108, 8595–8600 (2011).

    Article PubMed PubMed Central  Google Scholar 

  2. Powis, T. G. et al. Oldest chocolate in the New World.Antiquity81 (2007);https://www.antiquity.ac.uk/projgall/powis314/

  3. 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. USA104, 18937–18940 (2007).

    Article PubMed PubMed Central  Google Scholar 

  4. Sheets, P. D.The Ceren Site: An Ancient Village Buried by Volcanic Ash in Central America 2nd edn (Wadsworth Publishing, Belmont, 2005).

  5. Coe, S. D. & Coe, M. D.The True History of Chocolate 3rd edn (Thames and Hudson, London, 2013).

  6. Stuart, D. inChocolate inMesoamerica: A Cultural History of Cacao (ed. McNeil, C. L.) 184–201 (Univ. Press of Florida, Gainesville, 2009).

  7. Crown, P. L. & Hurst, W. J. Evidence of cacao use in the Prehispanic American Southwest.Proc. Natl Acad. Sci. USA106, 2110–2113 (2009).

    Article PubMed PubMed Central  Google Scholar 

  8. 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).

    Article  Google Scholar 

  9. 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).

    Article CAS  Google Scholar 

  10. Grivetti, L. H. & Shapiro, H.-Y. (eds)Chocolate, History, Culture, and Heritage (John Wiley & Sons, Hoboken, 2009).

  11. Hurst, W. J., Tarka, S. M. Jr, Powis, T. G., Valdez, F.Jr & Hester, T. R. Cacao usage by the earliest Maya civilization.Nature418, 289–290 (2002).

    Article CAS PubMed  Google Scholar 

  12. 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).

    Article  Google Scholar 

  13. McNeil, C. L.Chocolate in Mesoamerica: A Cultural History of Cacao (Univ. Press of Florida, Gainesville, 2009).

  14. Motamayor, J. C. et al. Cacao domestication I: the origin of the cacao cultivated by the Mayas.Heredity89, 380–386 (2002).

    Article CAS PubMed  Google Scholar 

  15. Motamayor, J. C. et al. Geographic and genetic population differentiation of the Amazonian chocolate tree (Theobroma cacao L.).PLoS ONE3, e3311 (2008).

    Article CAS PubMed PubMed Central  Google Scholar 

  16. Loor Solorzano, R. G. et al. Insight into the wild origin, migration and domestication history of the fine flavour NacionalTheobroma cacao L. variety from Ecuador.PLoS ONE7, e48438 (2012).

    Article CAS PubMed PubMed Central  Google Scholar 

  17. Thomas, E. et al. Present spatial diversity patterns ofTheobroma cacao L. in the neotropics reflect genetic differentiation in Pleistocene refugia followed by human-influenced dispersal.PLoS ONE7, e47676 (2012).

    Article CAS PubMed PubMed Central  Google Scholar 

  18. Valdez, F. inThe Handbook of South American Archaeology (eds Silverman, H. & Isbell, W. H.) 865–888 (Springer, New York, 2008).

  19. Cuatrecasas, J. Cacao and its allies, a taxonomic revision of the genus.Theobroma. Contr. US Natl Herb.35, 379–614 (1964).

    Google Scholar 

  20. Walker, T. inChocolate: History, Culture, and Heritage (eds Grivetti, L. E. & Shapiro, H.-Y.) 543–558 (John Wiley & Sons, Hoboken, 2009).

  21. Bletter, N. & Daly, D. C. inChocolate in Mesoamerica: A Cultural History of Cacao (ed. McNeil, C. L.) 31–68 (Univ. Press of Florida, Gainesville, 2009).

  22. 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).

    Article  Google Scholar 

  23. Zarrillo, S.Human Adaptation, Food Production, and Cultural Interaction During the Formative Period in Highland Ecuador. PhD dissertation, Univ. Calgary (2012).

  24. Lanaud, C., Loor, R. G., Zarrilo, S. & Valdez, F. Origen de la domesticacion del cacao y su uso temprano en el Ecuador.Nuestro Patrimonio12, 12–14 (2012).

    Google Scholar 

  25. Zarrillo, S. & Valdez, F. inArqueologia Amazonica: las Civilizaciones Ocultas del Bosque Tropical (ed. Valdez, F.) 147–171 (Abya-Yala, Ecuador, 2013).

  26. Reichert, E. T.The Differentiation and Specificity of Starches in Relation to Genera, Species, Etc. (Carnegie Institution of Washington, Washington DC, 1913).

    Google Scholar 

  27. Schmieder, R. L. & Keeney, G. Characterization and quantification of starch in cocoa beans and chocolate products.J. Food. Sci.45, 555–557 (1980).

    Article  Google Scholar 

  28. Pagán Jiménez, J. R.Almidones: Guía de Material Comparativo Moderno del Ecuador Para los Estudios Paleoetnobotánicos en el Neotrópico (Aspha, Buenos Aires, 2015).

  29. Hammerstone, J. F., Romanczyk, L. J. & Martin Aitken, W. Purine alkaloid distribution withHerrania andTheobroma.Phytochemistry35, 1237–1240 (1994).

    Article CAS  Google Scholar 

  30. Pääbo, S. et al. Genetic analyses from ancient DNA.Annu. Rev. Genet.38, 645–679 (2004).

    Article CAS PubMed  Google Scholar 

  31. Parducci, L. et al. Molecular- and pollen-based vegetation analysis in lake sediments from central Scandinavia.Mol. Ecol.22, 3511–3524 (2013).

    Article PubMed  Google Scholar 

  32. Willerslev, E. et al. Fifty thousand years of Arctic vegetation and megafaunal diet.Nature506, 47–51 (2014).

    Article CAS PubMed  Google Scholar 

  33. 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).

    Article CAS PubMed PubMed Central  Google Scholar 

  34. Argout, X. et al. The genome ofTheobroma cacao.Nat. Genet.43, 101–108 (2011).

    Article CAS PubMed  Google Scholar 

  35. Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data.Genetics155, 945–959 (2000).

    CAS PubMed PubMed Central  Google Scholar 

  36. 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).

    Article CAS PubMed  Google Scholar 

  37. Silva, P. & Oliveira-Cardoso, A. Historico das introduçoes de cacaueiro (Theobroma cacao L.) no Reconcavo da Bahia, Brasil.Revista Theobroma10, 135–140 (1980).

    Google Scholar 

  38. 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).

    Article  Google Scholar 

  39. Piperno, D. R. & Pearsall, D. M.The Origins of Agriculture in the Lowland Neotropics (Academic Press, New York, 1998).

    Google Scholar 

  40. Hilbert, L. et al. Evidence for mid-Holocene rice domestication in the Americas.Nat. Ecol. Evol.1, 1693–1698 (2017).

    Article PubMed  Google Scholar 

  41. 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).

    Article  Google Scholar 

  42. Redgwell, R. J. & Hansen, C. E. Isolation and characterisation of cell wall polysaccharides from cocoa(Theobroma cacao L.) beans.Planta210, 823–830 (2000).

    Article CAS PubMed  Google Scholar 

  43. 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).

    Article CAS  Google Scholar 

  44. Kufer, J. & McNeil, C. L. inChocolate in Mesoamerica: A Cultural History of Cacao (ed. McNeil, C. L.) 384–407 (Univ. Press of Florida, Gainesville, 2009).

  45. Cieslak, M. et al. Origin and history of mitochondrial DNA lineages in domestic horses.PLoS ONE5, e15311 (2010).

    Article CAS PubMed PubMed Central  Google Scholar 

  46. Pääbo, S. Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification.Proc. Natl Acad. Sci. USA86, 1939–1943 (1989).

    Article PubMed PubMed Central  Google Scholar 

  47. Dabney, J., Meyer, M. & Pääbo, S. inDNA 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).

  48. Argout, X. et al. Towards the understanding of the cocoa transcriptome: production and analysis of an exhaustive dataset of ESTs ofTheobroma cacao L. generated from various tissues and under various conditions.BMC Genomics9, 512 (2008).

    Article CAS PubMed PubMed Central  Google Scholar 

  49. Ye, J. et al. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction.BMC Bioinform.13, 134 (2012).

    Article CAS  Google Scholar 

  50. 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.Bioinformatics25, 1189–1191 (2009).

    Article CAS PubMed PubMed Central  Google Scholar 

  51. 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).

    Article CAS PubMed  Google Scholar 

  52. 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).

    Article CAS PubMed  Google Scholar 

  53. Argout, X. et al. The cacao Criollo genomev2.0: an improved version of the genome for genetic and functional genomic studies.BMC Genomics18, 730 (2017).

    Article CAS PubMed PubMed Central  Google Scholar 

  54. Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe.Nature522, 207–211 (2015).

    Article CAS PubMed PubMed Central  Google Scholar 

  55. Cruz-Dávalos, D. I. et al. Experimental conditions improving in-solution target enrichment for ancient DNA.Mol. Ecol. Resour.17, 508–522 (2017).

    Article CAS PubMed  Google Scholar 

  56. Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows–Wheeler transform.Bioinformatics26, 589–595 (2010).

    Article CAS PubMed PubMed Central  Google Scholar 

  57. Jónsson, H., Ginolhac, A., Schubert, M., Johnson, P. L. F. & Orlando, L. mapDamage 2.0: fast approximate Bayesian estimates of ancient DNA damage parameters.Bioinformatics29, 1682–1684 (2013).

    Article CAS PubMed PubMed Central  Google Scholar 

  58. GBIF Backbone Taxonomy (GBIF Secretariat, 2017);https://doi.org/10.15468/39omei

Download references

Acknowledgements

S.Z.’s research was funded by a Social Sciences and Humanities Research Council of Canada Doctoral Fellowship and an Honorary Isaak Walton Killam Memorial Scholarship, as well as the Martha Biggar Anders Memorial Award (2008, 2009, 2011), a Graduate Research Scholarship, a Faculty of Graduate Studies Travel Award, a Graduate Studies Scholarship and a Graduate Student Association Professional Development Grant from the University of Calgary. We thank the Universidad San Francisco de Quito, Riobamba and the University of British Columbia, Okanagan for use of laboratory facilities for some of S.Z.’s research. Funding for this project was provided by a Hampton Research Grant (no. F11-00878) from the University of British Columbia. Funding for archaeological excavations at SALF was provided by IRD. This project is supported by Agropolis Fondation under the reference ID 1202-029 through the Investissements d’avenir programme (Labex Agro: no. ANR-10-LABX-0001-01). The Hiseq sequencing activities were made in collaboration with the GeT platform, a partner of the National Infrastructure France Génomique, with thanks for support by the Commissariat aux Grands Investissements (no. ANR-10-INBS-0009). We are grateful to P. Lachenaud for providing genotyping by sequencing data on Guina group, to H. Kucera for assisting with Biochemical analyses, to N. Waber for preparing Fig.1 and M. Berard for assistance in preparing Figs.2 and3. We also thank The United States Department of Agriculture, Agricultural Research Services, Plant Genetic Resources Conservation Unit for generously supplyingTheobroma andHerrania pods and the Centro Agronómico Tropical de Investigación y Enseñanza (CATIE—Costa Rica) and the Cocoa Research Center, University of West Indies (CRC, Trinidad and Tobago) for providingTheobroma andHerrania leaves for modern DNA analyses.

Author information

Author notes

  1. These authors contributed equally: Sonia Zarrillo, Nilesh Gaikwad, Claire Lanaud.

Authors and Affiliations

  1. Department of Anthropology and Archaeology, University of Calgary, Calgary, Alberta, Canada

    Sonia Zarrillo

  2. Department of Anthropology, University of British Columbia, Vancouver, British Columbia, Canada

    Sonia Zarrillo & Michael Blake

  3. Department of Nutrition and Department of Environmental Toxicology, West Coast Metabolomics Center, University of California, Davis, CA, USA

    Nilesh Gaikwad

  4. Gaikwad Steroidomics Laboratory, Davis, CA, USA

    Nilesh Gaikwad

  5. CIRAD, UMR AGAP, Montpellier, France

    Claire Lanaud, Christopher Viot, Olivier Fouet, Xavier Argout & Hélène Vignes

  6. AGAP, University Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France

    Claire Lanaud, Christopher Viot, Olivier Fouet, Xavier Argout & Hélène Vignes

  7. Department of Geography and Anthropology, Kennesaw State University, Kennesaw, GA, USA

    Terry Powis

  8. INRA-UMR BIOGECO, Cestas, France

    Isabelle Lesur, Erwan Guichoux & Franck Salin

  9. HelixVenture, Mérignac, France

    Isabelle Lesur

  10. Instituto Nacional de Investigación Agropecuaria Estación Experimental Tropical Pichilingue, Quevedo, Provincia de Los Ríos, Ecuador

    Rey Loor Solorzano

  11. INRA, GeT-PlaGe, Genotoul, Castanet-Tolosan, France

    Olivier Bouchez

  12. New South Associates Inc., Stone Mountain, GA, USA

    Patrick Severts

  13. Ministerio de Cultura y Patrimonio, Ecuador/IRD, Quito, Ecuador

    Julio Hurtado & Alexandra Yepez

  14. Department of Nutrition, University of California, Davis, CA, USA

    Louis Grivetti

  15. Institut de Recherche pour le Développement, UMR 208 PALOC, MNHN-IRD, Marseille, France

    Francisco Valdez

Authors
  1. Sonia Zarrillo

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  2. Nilesh Gaikwad

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  3. Claire Lanaud

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  4. Terry Powis

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  8. Xavier Argout

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Contributions

F.V., M.B., S.Z., T.P., N.G. and C.L. designed the research. F.V., J.H., A.Y. and S.Z. performed excavations at Santa Ana-La Florida. S.Z. designed starch investigation methods and performed starch granule analysis. T.P. and P.S. sampled artefacts for theobromine analysis. N.G. designed mass spectrometry analysis, performed UPLC-MS/MS analyses and processed and analysed mass spectrometry data. L.G. provided general input to the overall project. C.L., C.V., I.L., O.F., X.A., E.G., F.S. and R.L.S., performed aDNA experiments and analyses. H.V. and O.B. performed NGS aDNA sequencing. S.Z., C.L., N.G., T.P., M.B. and F.V. led the writing of the paper with inputs from all other authors.

Corresponding author

Correspondence toMichael Blake.

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Supplementary information

Supplementary Information

Supplementary Notes; Supplementary Figures 1–8; Supplementary Tables 3–9 and 11–16

Supplementary Table 1

Radiocarbon dates from the Santa Ana-La Florida site, Palanda (Zamora-Chinchipe, Ecuador)

Supplementary Table 2

Total SALF samples analysed for starch grains, theobromine and aDNA

Supplementary Table 10

List of aDNA sequences specific to Theobroma and containing SNPs identified by GBS

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Zarrillo, S., Gaikwad, N., Lanaud, C.et al. The use and domestication ofTheobroma cacao during the mid-Holocene in the upper Amazon.Nat Ecol Evol2, 1879–1888 (2018). https://doi.org/10.1038/s41559-018-0697-x

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