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

Omar E Cornejo,Carlos D Bustamante,Nilesh R Tawari,Mary Andrews,Victor Dominguez,Alexandra Sockell,Conrad Stack,Juan C Motamayor,Muh-Ching Yee,Donald Livingstone,Alberto Romero,Wilbert Phillips,Stefan Royaert,Pauline Ng,Keithanne Mockaitis,Pathmanathan Umaharan,Erika Strandberg,Osman Gutierrez

doi:10.1038/s42003-018-0168-6

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).

Highlights

Domestication has had a strong impact on the development of modern societies
We explore the extent of whole-genome variation in T. cacao L. and investigate the evolutionary origin of Criollo, the cacao tree domesticated in Mesoamerica
After aligning the reads to the cacao reference (Matina-v1.121), we identified 7,412,507 singlenucleotide polymorphisms (SNPs)

Summary

Introduction

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). Current dogma suggests that cacao was introduced to Mesoamerica in Olmec times from the cacao varieties present in the Upper Amazon (Northern South America), the hotbed of diversity for the species[6,8] Another line of evidence suggests that the route of domestication of the chocolate tree could have dispersed throughout the Amazon Basin along two routes: one leading north and another leading west[13]. The continuous intermixing of farmed and wild cacao trees has likely continued to shape both gene pools in recent times[11,15,16] Both the impact of ancient domestication processes and modern hybridization on the genetic variation in the species are largely unknown in T. cacao. We show that there is an increase in the higher-frequency deleterious variants, and show that this increase is associated with a reduction of individual fitness in domesticated cacao

Methods

Results

Conclusion