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

Omar E Cornejo; Muh-Ching Yee; Victor Dominguez; Mary Andrews; Alexandra Sockell; Erika Strandberg; Donald Livingstone 3rd; Conrad Stack; Alberto Romero; Pathmanathan Umaharan; Stefan Royaert; Nilesh R Tawari; Pauline Ng; Osman Gutierrez; Wilbert Phillips; Keithanne Mockaitis; Carlos D Bustamante; Juan C Motamayor

doi:10.1038/s42003-018-0168-6

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

Commun Biol. 2018 Oct 16:1:167. doi: 10.1038/s42003-018-0168-6. eCollection 2018.

Authors

Omar E Cornejo^{1

2}, Muh-Ching Yee^{2

3}, Victor Dominguez⁴, Mary Andrews⁴, Alexandra Sockell², Erika Strandberg^{2

5}, Donald Livingstone 3rd^{6

7}, Conrad Stack⁶, Alberto Romero⁶, Pathmanathan Umaharan⁸, Stefan Royaert⁶, Nilesh R Tawari⁹, Pauline Ng⁹, Osman Gutierrez¹⁰, Wilbert Phillips¹¹, Keithanne Mockaitis^{4

12}, Carlos D Bustamante², Juan C Motamayor¹³

Affiliations

¹ School of Biological Sciences, Washington State University, PO Box 644236, Heald Hall 429B, Pullman, Washington, 99164, USA.
² Department of Genetics, School of Medicine, Stanford University, 300 Pasteur Dr. Lane Bldg Room L331, Stanford, CA, 94305, USA.
³ Stanford Functional Genomics Facility, Stanford, CA, 94305, USA.
⁴ Department of Biology, Indiana University, 915 E. Third St, Bloomington, IN, 47405, USA.
⁵ Biomedical Informatics Training Program, 1265 Welch Road, MSOB, X-215, MC 5479, Stanford, CA, 94305-5479, USA.
⁶ Mars, Incorporated, 6885 Elm Street, McLean, VA, 22101, USA.
⁷ United States Department of Agriculture-Agriculture Research Service, Subtropical Horticulture Research Station, 13601 Old Cutler Rd, Miami, FL, 33158, USA.
⁸ Cocoa Research Centre, The University of the West Indies, St. Augustine, Trinidad and Tobago.
⁹ Computational and Systems Biology, Genome Institute of Singapore, 60 Biopolis Street, Genome, #02-01, Singapore, 138672, Singapore.
¹⁰ SHRS, USDS-ARS, 13601 Old Cutler Road, Miami, FL, 33158, USA.
¹¹ Programa de Mejoramiento de Cacao, CATIE, 7170, Turrialba, Costa Rica.
¹² Pervasive Technology Institute, Indiana University, 2709 E. 10th St., Bloomington, IN, 47408, USA.
¹³ Mars, Incorporated, 6885 Elm Street, McLean, VA, 22101, USA. juancarlos.motamayor@gmail.com.

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).