Population genomic analyses of the chocolate tree, Theobroma cacao L., provide insights into its domestication process

Abstract

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).

Inferring the Demographic History of Inbred Species From Genome-Wide SNP Frequency Data

“…2016; Koenig et al . 2019) or masking rare variants (e.g., Cornejo et al . 2018), which are disproportionately affected at lower levels of inbreeding (Figure 1).…”

Chromosome Engineering in Tropical Cash Crops

“…About 24% of the genome consists of transposable elements such as the Gaucho long-terminal repeat (LTR) retrotransposon [12]. In cacao, the improvement of and selection for desirable traits is believed to have also caused accelerated accumulation of deleterious mutations because of population bottlenecks that started 3600 years ago [12,13]. Some of the mutations are suspected to be due to the process of fertilization itself [13].…”

“…In cacao, the improvement of and selection for desirable traits is believed to have also caused accelerated accumulation of deleterious mutations because of population bottlenecks that started 3600 years ago [12,13]. Some of the mutations are suspected to be due to the process of fertilization itself [13]. However, as compared with non-domesticated Theobroma cacao varieties such as Marañón (1.68 × 10 −5 ) and Purús (1.23 × 10 −4 ), in the varieties Amelonado, Contamana, Criollo and Guianna, the same domestication process may account for differentially high recombination rates (expressed in centiMorgans per megabase pairs [cM/Mb], 4.04 × 10 −6 to 3.91 × 10 −3 ) [14].…”

Chromosome Engineering in Tropical Cash Crops

“…Genes that contribute to stress tolerance/resistance or other traits can be obtained from local germplasm resources or via introduced landraces or breeding lines from other breeding programs, wild species, or genera 10 . In T. cacao (2n=2=20 chromosomes, 430-445 Mbp) 11 , the improvement of and selection for desirable traits has also caused accelerated accumulation of deleterious mutations because of population bottlenecks that started 3600 years ago 12,13 . Some of the mutations are suspected to be due to the process of fertilization itself 12 .…”

“…In T. cacao (2n=2=20 chromosomes, 430-445 Mbp) 11 , the improvement of and selection for desirable traits has also caused accelerated accumulation of deleterious mutations because of population bottlenecks that started 3600 years ago 12,13 . Some of the mutations are suspected to be due to the process of fertilization itself 12 . However, as compared with non-domesticated T. cacao varieties such as Marañón (1.68x10 -5 ) and Purús (1.…”