Evolutionary relationships, hybridization and diversification under domestication of the locoto chile (Capsicum pubescens) and its wild relatives.

Patterns of genetic variation in crops are the result of multiple processes that have occurred during their domestication and improvement, and are influenced by their wild progenitors that often remain understudied. The locoto chile, Capsicum pubescens, is a crop grown mainly in mid-highlands of South-Central America. This species is not known from the wild and exists only as a cultigen. The evolutionary affinities and exact origin of C. pubescens have still not been elucidated, with hypotheses suggesting its genetic relatedness and origin to two wild putative ancestral Capsicum species from the Central Andes, C. eximium and C. cardenasii. In the current study, RAD-sequencing was applied to obtain genome-wide data for 48 individuals of C. pubescens and its wild allies representing different geographical areas. Bayesian, Maximum Likelihood and coalescent-based analytical approaches were used to reconstruct population genetic patterns and phylogenetic relationships of the studied species. The results revealed that C. pubescens forms a well-defined monotypic lineage closely related to wild C. cardenasii and C. eximium, and also to C. eshbaughii. The primary lineages associated with the diversification under domestication of C. pubescens were also identified. Although direct ancestor-descendant relationship could not be inferred within this group of taxa, hybridization events were detected between C. pubescens and both C. cardenasii and C. eximium. Therefore, although hybrid origin of C. pubescens could not be inferred, gene flow involving its wild siblings was shown to be an important factor contributing to its contemporary genetic diversity. The data allowed for the inference of the center of origin of C. pubescens in central-western Bolivia highlands and for better understanding of the dynamics of its gene pool. The results of this study are essential for germplasm conservation and breeding purposes, and provide excellent basis for further research of the locoto chile and its wild relatives.

Geographical Patterns of Genetic Variation in Locoto Chile (Capsicum pubescens) in the Americas Inferred by Genome-Wide Data Analysis.

The locoto chile (Capsicum pubescens) is a regionally important food crop grown and marketed throughout the mid-highlands of South andCentral America, but little is known about its evolution and the diversity it harbours. An initial scan of genetic diversity and structure across its cultivation range was conducted, the first one using a genomic approach. The RAD-sequencing methodology was applied to a sampling of C. pubescens germplasm consisting of 67 accessions from different American countries, covering its range of distribution/cultivation on the continent. The RAD-seq SNP data obtained clustered the accessions into three major groups, with a high degree of admixture/reticulation among them. Moderate but significant differentiation and geographic structuration were found, depicting a south-north pattern in the distribution of genetic variation. The highest levels of diversity were found among central-western Bolivian individuals, while the lowest was found across Central America-Mexican germplasm. This study provides new genome-wide supported insights into the diversity and differentiation of C. pubescens, as well as a starting point for more efficient use of its genetic variation and germplasm conservation efforts. The findings also contribute to understanding the evolutionary history of C. pubescens, but further investigation is needed to disentangle its origin and diversification under domestication.

Diversification of chiles (Capsicum, Solanaceae) through time and space: New insights from genome-wide RAD-seq data.

Capsicum L. encompasses 43 American species, including the five domesticated worldwide consumed sweet and hot chiles. This study presents new, updated and age-calibrated phylogenetic hypothesis on the genus evolution incorporating nearly all currently accepted Capsicum species. A new model of spatial diversification of Capsicum is proposed based on analyses of several thousands of genome-wide RAD-seq derived SNPs. Maximum likelihood approaches were used to reconstruct phylogenies and to estimate dates of all major splits. Ancestral ranges were inferred and diversification events were modeled in a time frame using a Bayesian approach. Nine clades corresponding to genetically and (mostly) geographically well-defined lineages, which diversified starting around mid-upper Miocene, were recovered with strong support. The Northern and Central Andes were inferred to represent the most likely ancestral range of the genus Capsicum. A few early vicariant and dispersal events were estimated to have driven the geographic divergence of the main Capsicum clades. Each lineage was inferred to have diversified within a distinct region of South America and expanded geographically to different extent. Extant species diversification was inferred to have begun at the beginning of Pliocene and continued through the Pleistocene. The Central Andes, represented mainly by the territory of present-day Bolivia, were proposed to play a central role in the diversification of lineages comprising domesticated capsicums and their wild allies. The genome-wide approach allowed for high resolution and support of deep phylogenetic nodes providing novel insights into the affinities of major lineages and clades as well as on the geographic expansion of Capsicum. This study provides the first dated evolutionary history of the genus encompassing most of the chile species diversity.