Collection of native Theobroma cacao L. accessions from the Ecuadorian Amazon highlights a hotspot of cocoa diversity

Societal Impact Statement "Fine flavor" cocoa, known for its superior flavor and aroma, commands a higher price for farmers than "bulk" cocoa produced for market. These fine flavor cocoa varieties make an important contribution to the agricultural sector in Ecuador. However, cocoa diversity is threatened by deforestation. The effective preservation, characterization, and use of cocoa tree diversity are therefore essential to the future development of this market. We carried out participatory collection surveys with local communities in the Ecuadorian Amazon Forest, to evaluate the genetic diversity of native cocoa trees and protect trees as a resource for local communities. Accessing this wealth of diversity will aid farmers to safeguard cocoa against climate change and develop new varieties for market. The aromatic Nacional variety of Theobroma cacao, emblematic of Ecuador, is highly sought after by the chocolate industry. The modern Nacional is a hybrid population resulting from genetic admixture that has lost the specificity of the ancestral variety. In the context of progressive forest disappearance, the objective of our study was to collect, safeguard, and evaluate native aromatic cocoa trees from Ecuadorian Amazon areas previously identified as areas of origin of the Nacional variety, as well as those that extend toward the northern Amazon. Four collection expeditions were organized in the Ecuadorian Amazon provinces of Zamora-Chinchipe, Morona-Santiago, and Pastaza in close collaboration with local communities. A total of 283 native accessions were collected and safeguarded at experimental stations and in local communities. The genetic diversity of the cocoa trees was analyzed by comparison to known genetic groups with a set of 48 simple sequence repeat (SSR) markers. This new collection clearly enriches the currently known diversity and improves knowledge of the global genetic structure of cocoa trees. Our results clarify the geographic origin of the Nacional variety in the vicinity of an archeological site that housed a Maya Chinchipe population that consumed cacao 5,000 years ago. In addition, our analyses revealed clues to the origin of Criollo, another ancient variety with a fine flavor. These new genetic resources will be used in breeding programs for the varietal improvement of new aromatic cocoa varieties and more globally for the selection of new varieties adapted to environmental changes.