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

Abstract

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.

Fig. 1.

Percentages of membership (q) for each of the clusters identified (B1–B6; color-coded as indicated). Each accession is represented by a vertical line divided into colored segments, the lengths of which indicate the proportions of the genome that are attributed to the specific clusters. The accessions are ordered according to latitude from northern Mexico to northern Argentina. The country of origin is indicated by the horizontal line. AW, Andean wild; ar, Argentina; bl, Bolivia; C_mx, central Mexico; col, Colombia; ec, Ecuador; es, El Salvador; gt, Guatemala; MW, Mesoamerican wild; N_mx, north Mexico; N_pr, northern Peru; PhI, type I phaseolin (northern Peru–Ecuador); S_mx, south Mexico; S_pr, southern Peru.

Fig. 2.

Spatial interpolation of membership coefficients (q) for the four Mesoamerican clusters identified by the Bayesian clustering analysis. (A) B1_blue. (B) B2_light-blue. (C) B3_green. (D) B4_orange. Latitude and longitude are expressed in the Universal Transverse Mercator system.

Fig. 3.

Unrooted NJ tree showing the phylogenetic relationships of genetic clusters identified by cluster analysis.

Fig. 4.

Unrooted NJ bootstrap tree inferred from the concatenate sequence data. Each set of accessions (as indicated) is represented by a colored circle, and each color indicates the membership to the BAPS groups. Small gray and violet circles represent the nodes for which bootstrap values are higher that 50% and 80%, respectively (the 80% threshold highlights the relationships with very strong support). AW, Andean wild; MW, Mesoamerican wild; PhI, type I phaseolin (northern Peru–Ecuador).

Fig. 5.

Haplotype networks of the five nuclear loci. Each circle represents a single different haplotype, and the circle sizes are proportional to the number of individuals that carry the same haplotype. Black circles indicate missing intermediate haplotypes. The lengths of the lines of the haplotype networks are proportional to the number of mutational steps, which are indicated when more than one. Colors show the genotypes belonging to the different BAPS clusters (as indicated). AW, Andean wild; MW, Mesoamerican wild; PhI, type I phaseolin (northern Peru–Ecuador).

Fig. P1.

(A) Percentages of membership (q) for each genetic cluster (B1, B2, B3, B4, B5, and B6; color coded). Each genotype ( “accession” refers to a member of a plant collection) is represented by a vertical line divided into colored segments, with the lengths representing their proportion of the genome. The accessions are ordered according to latitude: N_mx, Northern Mexico; C_mx, Central Mexico; S_mx, Southern Mexico; gt, Guatemala; es, El Salvador; col, Colombia; ec, Ecuador; N_pr, Northern Peru; S_pr, Southern Peru; bl, Bolivia; ar, Argentina. The country of origin is indicated by the horizontal line. (B) Unrooted NJ bootstrap tree. Each set of accessions is represented by a colored circle, and each color indicates the membership in the clusters. Gray and violet circles represent the nodes for which values are higher than 50% and 80%, respectively (indicating strength of support). AW, Andean wild; MW, Mesoamerican wild; PhI, type I phaseolin (northern Peru–Ecuador).