Knowledge about the origins and evolution of crop species represents an important prerequisite for efficient conservation and use of existing plant materials. This study was designed to solve the ongoing debate on the origins of the common bean by investigating the nucleotide diversity at five gene loci of a large sample that represents the entire geographical distribution of the wild forms of this species. Our data clearly indicate a Mesoamerican origin of the common bean. They also strongly support the occurrence of a bottleneck during the formation of the Andean gene pool that predates the domestication, which was suggested by recent studies based on multilocus molecular markers. Furthermore, a remarkable result was the genetic structure that was seen for the Mesoamerican accessions, with the identification of four different genetic groups that have different relationships with the sets of wild accessions from the Andes and northern Peru–Ecuador. This finding implies that both of the gene pools from South America originated through different migration events from the Mesoamerican populations that were characteristic of central Mexico.

Summary: We have studied the nucleotide diversity of common bean,Phaseolus vulgaris, which is characterized by two independent domestications in two geographically distinct areas: Mesoamerica and the Andes. This provides an important model, as domestication can be studied as a replicate experiment. We used nucleotide data from five gene fragments characterized by large introns to analyse 214 accessions (102 wild and 112 domesticated). The wild accessions represent a cross‐section of the entire geographical distribution ofP. vulgaris. A reduction in genetic diversity in both of these gene pools was found, which was three‐fold greater in Mesoamerica compared with the Andes. This appears to be a result of a bottleneck that occurred before domestication in the Andes, which strongly impoverished this wild germplasm, leading to the minor effect of the subsequent domestication bottleneck (i.e. sequential bottleneck). These findings show the importance of considering the evolutionary history of crop species as a major factor that influences their current level and structure of genetic diversity. Furthermore, these data highlight a single domestication event within each gene pool. Although the findings should be interpreted with caution, this evidence indicates the Oaxaca valley in Mesoamerica, and southern Bolivia and northern Argentina in South America, as the origins of common bean domestication.

Here, we aim to provide a comprehensive and up-to-date overview of the most significant outcomes in the literature regarding the origin of Phaseolus genus, the geographical distribution of the wild species, the domestication process, and the wide spread out of the centres of origin. Phaseolus can be considered as a unique model for the study of crop evolution, and in particular, for an understanding of the convergent phenotypic evolution that occurred under domestication. The almost unique situation that characterises the Phaseolus genus is that five of its ~70 species have been domesticated (i.e., Phaseolus vulgaris, P. coccineus, P. dumosus, P. acutifolius, P. lunatus), and in addition, for P. vulgaris and P. lunatus, the wild forms are distributed in both Mesoamerica and South America, where at least two independent and isolated episodes of domestication occurred. Thus, at least seven independent domestication events occurred, which provides the possibility to unravel the genetic basis of the domestication process not only among species of the same genus, but also between gene pools within the same species. Along with this, other interesting features makes Phaseolus crops very useful in the study of evolution, including: (i) their recent divergence, and the high level of collinearity and synteny among their genomes; (ii) their different breeding systems and life history traits, from annual and autogamous, to perennial and allogamous; and (iii) their adaptation to different environments, not only in their centres of origin, but also out of the Americas, following their introduction and wide spread through different countries. In particular for P. vulgaris this resulted in the breaking of the spatial isolation of the Mesoamerican and Andean gene pools, which allowed spontaneous hybridization, thus increasing of the possibility of novel genotypes and phenotypes. This knowledge that is associated to the genetic resources that have been conserved ex situ and in situ represents a crucial tool in the hands of researchers, to preserve and evaluate this diversity, and at the same time, to identify the genetic basis of adaptation and to develop new improved varieties to tackle the challenges of climate change, and food security and sustainability.

Together with the knowledge of the population structure, a critical aspect for the planning of association and/or population genomics studies is the level of linkage disequilibrium (LD) that characterizes the species and the population used for such an analysis. We have analyzed the population structure and LD in wild and domesticated populations of Phaseolus vulgaris L. using amplified fragment length polymorphism markers, most of which were genetically mapped in two recombinant inbred populations. Our results reflect the previous knowledge of the occurrence of two major wild gene pools of P. vulgaris, from which two independent domestication events originated, one in the Andes and one in Mesoamerica. The high level of LD in the whole sample was mostly due to the gene pool structure, with a much higher LD in domesticated compared to wild populations. In relation to association studies, our results also suggest that whole‐genome‐scan approaches are feasible in the common bean. Interestingly, an excess of inter‐chromosomal LD was found in the domesticated populations, which suggests an important role for epistatic selection during domestication. Moreover, our results indicate the occurrence of a strong bottleneck in the Andean wild population before domestication, suggesting a Mesoamerican origin of P. vulgaris. Finally, our data support the occurrence of a single domestication event in Mesoamerica, and the same scenario in the Andes.

Using RNA sequencing technology and de novo transcriptome assembly, we compared representative sets of wild and domesticated accessions of common bean (Phaseolus vulgaris) from Mesoamerica. RNA was extracted at the first true-leaf stage, and de novo assembly was used to develop a reference transcriptome; the final data set consists of ∼190,000 single nucleotide polymorphisms from 27,243 contigs in expressed genomic regions. A drastic reduction in nucleotide diversity (∼60%) is evident for the domesticated form, compared with the wild form, and almost 50% of the contigs that are polymorphic were brought to fixation by domestication. In parallel, the effects of domestication decreased the diversity of gene expression (18%). While the coexpression networks for the wild and domesticated accessions demonstrate similar seminal network properties, they show distinct community structures that are enriched for different molecular functions. After simulating the demographic dynamics during domestication, we found that 9% of the genes were actively selected during domestication. We also show that selection induced a further reduction in the diversity of gene expression (26%) and was associated with 5-fold enrichment of differentially expressed genes. While there is substantial evidence of positive selection associated with domestication, in a few cases, this selection has increased the nucleotide diversity in the domesticated pool at target loci associated with abiotic stress responses, flowering time, and morphology.