Ancient genomes reveal early Andean farmers selected common beans while preserving diversity.

All crops are the product of a domestication process that started less than 12,000 years ago from one or more wild populations1,2. Farmers selected desirable phenotypic traits (such as improved energy accumulation, palatability of seeds and reduced natural shattering3) while leading domesticated populations through several more or less gradual demographic contractions2,4. As a consequence, the erosion of wild genetic variation5 is typical of modern cultivars, making them highly susceptible to pathogens, pests and environmental change6,7. The loss of genetic diversity hampers further crop improvement programmes to increase food production in a changing world, posing serious threats to food security8,9. Using both ancient and modern seeds, we analysed the temporal dynamics of genetic variation and selection during the domestication process of the common bean (Phaseolus vulgaris) in the southern Andes. Here, we show that most domestic traits were selected for before 2,500 years ago, with no or only minor loss of whole-genome heterozygosity. In fact, most of the changes at coding genes and linked regions that differentiate wild and domestic genomes are already present in the ancient genomes analysed here, and all ancient domestic genomes dated between 600 and 2,500 years ago are highly variable (at least as variable as modern genomes from the wild). Single seeds from modern cultivars show reduced variation when compared with ancient seeds, indicating that intensive selection within cultivars in the past few centuries probably partitioned ancestral variation within different genetically homogenous cultivars. When cultivars from different Andean regions are pooled, the genomic variation of the pool is higher than that observed in the pool of ancient seeds from north and central western Argentina. Considering that most desirable phenotypic traits are probably controlled by multiple polymorphic genes10, a plausible explanation of this decoupling of selection and genetic erosion is that early farmers applied a relatively weak selection pressure2 by using many phenotypically similar but genetically diverse individuals as parents. Our results imply that selection strategies during the past few centuries, as compared with earlier times, more intensively reduced genetic variation within cultivars and produced further improvements by focusing on a few plants carrying the traits of interest, at the cost of marked genetic erosion within Andean landraces.

Molecular analysis of the parallel domestication of the common bean (Phaseolus vulgaris) in Mesoamerica and the Andes.

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 of P. 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.

Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data.

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.

Tagging the signatures of domestication in common bean (Phaseolus vulgaris) by means of pooled DNA samples.

BACKGROUND AND AIMS: The main aim of this study was to use an amplified fragment length polymorphism (AFLP)-based, large-scale screening of the whole genome of Phaseolus vulgaris to determine the effects of selection on the structure of the genetic diversity in wild and domesticated populations. METHODS: Using pooled DNA samples, seven each of wild and domesticated populations of P. vulgaris were studied using 2506 AFLP markers (on average, one every 250 kb). About 10 % of the markers were also analysed on individual genotypes and were used to infer allelic frequencies empirically from bulk data. In both data sets, tests were made to determine the departure from neutral expectation for each marker using an F(ST)-based method. KEY RESULTS: The most important outcome is that a large fraction of the genome of the common bean (16 %; P < 0.01) appears to have been subjected to effects of selection during domestication. Markers obtained in individual genotypes were also mapped and classified according to their proximities to known genes and quantitative trait loci (QTLs) of the domestication syndrome. Most of the markers that were found to be potentially under the effects of selection were located in the proximity of previously mapped genes and QTLs related to the domestication syndrome. CONCLUSIONS: Overall, the results indicate that in P. vulgaris a large portion of the genome appears to have been subjected to the effects of selection, probably because of linkage to the loci selected during domestication. As most of the markers that are under the effects of selection are linked to known loci related to the domestication syndrome, it is concluded that population genomics approaches are very efficient in detecting QTLs. A method based on bulk DNA samples is presented that is effective in pre-screening for a large number of markers to determine selection signatures.