Present Spatial Diversity Patterns of Theobroma cacao L. in the Neotropics Reflect Genetic Differentiation in Pleistocene Refugia Followed by Human-Influenced Dispersal

Abstract

Cacao (Theobroma cacao L.) is indigenous to the Amazon basin, but is generally believed to have been domesticated in Mesoamerica for the production of chocolate beverage. However, cacao’s distribution of genetic diversity in South America is also likely to reflect pre-Columbian human influences that were superimposed on natural processes of genetic differentiation. Here we present the results of a spatial analysis of the intra-specific diversity of cacao in Latin America, drawing on a dataset of 939 cacao trees genotypically characterized by means of 96 SSR markers. To assess continental diversity patterns we performed grid-based calculations of allelic richness, Shannon diversity and Nei gene diversity, and distinguished different spatially coherent genetic groups by means of cluster analysis. The highest levels of genetic diversity were observed in the Upper Amazon areas from southern Peru to the Ecuadorian Amazon and the border areas between Colombia, Peru and Brazil. On the assumption that the last glaciation (22,000–13,000 BP) had the greatest pre-human impact on the current distribution and diversity of cacao, we modeled the species’ Pleistocene niche suitability and overlaid this with present-day diversity maps. The results suggest that cacao was already widely distributed in the Western Amazon before the onset of glaciation. During glaciations, cacao populations were likely to have been restricted to several refugia where they probably underwent genetic differentiation, resulting in a number of genetic clusters which are representative for, or closest related to, the original wild cacao populations. The analyses also suggested that genetic differentiation and geographical distribution of a number of other clusters seem to have been significantly affected by processes of human management and accompanying genetic bottlenecks. We discuss the implications of these results for future germplasm collection and in situ, on farm and ex situ conservation of cacao.

Trade-offs between crop intensification and ecosystem services: the role of agroforestry in cocoa cultivation

“…Domestication of cocoa began around 8,000 years ago, in the foothills of the Andes, along the banks of major upper tributaries of the Amazon River in what is today Bolivia, Peru, Ecuador, and Colombia (Clement et al 2010;Miller and Nair 2006;Thomas et al 2012). Native Amazonians collected ripe cocoa pods from fruiting trees found in patches embedded within the forest matrix in the high terraces of the riverine system, and transported them back to their villages for home consumption.…”

“…Cocoa pods were consumed as fruit by sucking the pulp and spitting out the seed, or were fermented to produce an alcoholic drink (Henderson et al 2007). Early selection for desirable traits such as abundant and sweet pulp probably occurred (Thomas et al 2012).…”

Genetic diversity of Ceratoides arborescens, a species endemic to China, detected by inter-simple sequence repeat (ISSR)

“…First, the mode of pollen and seed dispersal, which determines the N m among populations (Li et al, 2009a;Bellucci et al, 2011;Nestmann et al, 2011;Wang and Li, 2011), can facilitate N m among populations, minimizing the population differentiation. Many studies have demonstrated that wind-pollinated and wind-dispersed species exhibit low levels of genetic differentiation (Li et al, 2009b;Adamski et al, 2012;Thomas et al, 2012), approaching the levels observed in C. arborescens. Second, genetic diversity may be influenced by geographic distances, especially longitudinal differences, as revealed by the Mantel test.…”

Conservation and Use of Genetic Resources of Underutilized Crops in the Americas—A Continental Analysis

“…An important step towards improving the on-farm conservation of any species is having data about its current (and potential) distribution and cultivation. In addition to individuals' knowledge on these aspects, publicly available georeferenced data is a powerful starting point for studies on a crop's agroecological potential and adaptive capacity which in turn are useful for planning in situ conservation initiatives [33][34][35]. Searches performed in the data portal of the GBIF resulted in retrieval of georeferenced data for almost all the species.…”