Global range expansion history of pepper (Capsicum spp.) revealed by over 10,000 genebank accessions

Significance This study provides a deep population genomic analysis of 10,000 Capsicum accessions held in genebanks and representing a frame of the global diversity of the genus. By combining single nucleotide polymorphisms (SNPs) based data and passport information, we investigated the genomic diversity and population structure of wild and domesticated peppers, tracing back to routes of evolution and providing a model of Capsicum annuum distribution, which reflects human trade and historical/cultural influences. Our results highlight west–east routes of expansion, shedding light on the links between South and Mesoamerica, Africa, and East/South Asia, the latter two constituting important diversification centers of pepper diversity. Finally, we outline a roadmap for genebank management and future direction for better exploitation of germplasm resources.
Genebanks collect and preserve vast collections of plants and detailed passport information, with the aim of preserving genetic diversity for conservation and breeding. Genetic characterization of such collections has the potential to elucidate the genetic histories of important crops, use marker–trait associations to identify loci controlling traits of interest, search for loci undergoing selection, and contribute to genebank management by identifying taxonomic misassignments and duplicates. We conducted a genomic scan with genotyping by sequencing (GBS) derived single nucleotide polymorphisms (SNPs) of 10,038 pepper (Capsicum spp.) accessions from worldwide genebanks and investigated the recent history of this iconic staple. Genomic data detected up to 1,618 duplicate accessions within and between genebanks and showed that taxonomic ambiguity and misclassification often involve interspecific hybrids that are difficult to classify morphologically. We deeply interrogated the genetic diversity of the commonly consumed Capsicum annuum to investigate its history, finding that the kinds of peppers collected in broad regions across the globe overlap considerably. The method ReMIXTURE—using genetic data to quantify the similarity between the complement of peppers from a focal region and those from other regions—was developed to supplement traditional population genetic analyses. The results reflect a vision of pepper as a highly desirable and tradable cultural commodity, spreading rapidly throughout the globe along major maritime and terrestrial trade routes. Marker associations and possible selective sweeps affecting traits such as pungency were observed, and these traits were shown to be distributed nonuniformly across the globe, suggesting that human preferences exerted a primary influence over domesticated pepper genetic structure.