Population genomic analyses of the chocolate tree, Theobroma cacao L., provide insights into its domestication process
Omar E. Cornejo et al.
Domestication has had a strong impact on the development of modern societies. We sequenced 200 genomes of the chocolate plant Theobroma cacao L. to show for the first time to our knowledge that a single population, the Criollo population, underwent strong domestication ~3600 years ago (95% CI: 2481–13,806 years ago). We also show that during the process of domestication, there was strong selection for genes involved in the metabolism of the colored protectants anthocyanins and the stimulant theobromine, as well as disease resistance genes. Our analyses show that domesticated populations of T. cacao (Criollo) maintain a higher proportion of high-frequency deleterious mutations. We also show for the first time the negative consequences of the increased accumulation of deleterious mutations during domestication on the fitness of individuals (significant reduction in kilograms of beans per hectare per year as Criollo ancestry increases, as estimated from a GLM, P = 0.000425).
Population genetic structure in T. cacao. a The ten main genetic clusters can be recovered (A.1), although further structure (11 clusters) seems to be meaningful given that a considerable number of admixed individuals present the ancestry from a subset of Amelonado ancestry (A. 2). Color bars on top of the admixed individuals show our suggested grouping for the hybrids. b Map of Central and South America showing the median coordinate locations for the origin of samples from each population sampled in this work (with the exception of Admixed). c MDS showing a gradient of differentiation form the West to the East side of the Amazon (PC2) and a major separation of the Criollo group that corresponds to the Mesoamerican domesticated group (PC1). d Significant decay of genetic diversity (π) for the species along PC2 is supportive of the origin of the species being in the western side of the Amazon Basin (Criollo is excluded, model: π ∼ group + ε, p < 2E-16, r2 = 0.19). e All ten population genetic groups that have been described for the species are highly differentiated, with Criollo presenting a larger average FST when compared against all the other groups
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