Spatial and Temporal Scales of Range Expansion in Wild Phaseolus vulgaris

Abstract

The wild progenitor of common-bean has an exceptionally large distribution from northern Mexico to northwestern Argentina, unusual among crop wild progenitors. This research sought to document major events of range expansion that led to this distribution and associated environmental changes. Through the use of genotyping-by-sequencing (∼20,000 SNPs) and geographic information systems applied to a sample of 246 accessions of wild Phaseolus vulgaris, including 157 genotypes of the Mesoamerican, 77 of the southern Andean, and 12 of the Northern Peru-Ecuador gene pools, we identified five geographically distinct subpopulations. Three of these subpopulations belong to the Mesoamerican gene pool (Northern and Central Mexico, Oaxaca, and Southern Mexico, Central America and northern South America) and one each to the Northern Peru-Ecuador (PhI) and the southern Andean gene pools. The five subpopulations were distributed in different floristic provinces of the Neotropical seasonally dry forest and showed distinct distributions for temperature and rainfall resulting in decreased local potential evapotranspiration (PhI and southern Andes groups) compared with the two Mexican groups. Three of these subpopulations represent long-distance dispersal events from Mesoamerica into Northern Peru-Ecuador, southern Andes, and Central America and Colombia, in chronological order. Of particular note is that the dispersal to Northern Peru-Ecuador markedly predates the dispersal to the southern Andes (∼400 vs. ∼100 ky), consistent with the ancestral nature of the phaseolin seed protein and chloroplast sequences observed in the PhI group. Seed dispersal in common bean can be, therefore, described at different spatial and temporal scales, from localized, annual seed shattering to long-distance, evolutionarily rare migration.

Keywords: climate adaptation; coalescent analysis; crop wild relatives; genotyping‐by‐sequencing; long‐distance dispersal.

Fig. 1.

(A) Molecular PCA analysis of genetic diversity in wild Phaseolus vulgaris. Inset: Geographical distribution of the genotypes analyzed. (B) Correlation between molecular PC1 and latitude of wild P. vulgaris. Black dashed line: linear correlation; red dotted line: local polynomial regression. Pearson’s correlation coefficient (r) is shown. MW, Mesoamerican wild; AW, Andean wild; PhI, Northern Peru–Ecuador.

Fig. 2.

Spatial population clustering and ancestry coefficients estimated with TESS3 using the best number of subpopulations (K = 5). The genotypes are sorted by latitude from Northern Mexico to Northwestern Argentina. MW, Mesoamerican wild; AW, Andean wild; PhI, Northern Peru-Ecuador.

Fig. 3.

Spatial interpolation of population ancestry coefficients across the geographic distribution of the genotypes analyzed. Populations are colored as in figure 2.

Fig. 4.

Phylogenetic tree of the wild Phaseolus vulgaris analyzed in the current study built using neutral variants. Populations are colored as in figure 2. Genotypes with a membership coefficient (Q) < 0.7, by population, analysis, were considered as admixed. Phaseolus coccineus PI430191 was used as outgroup for rooting the phylogenetic trees.

Fig. 5.

Climatic distribution of the different genetic groups identified by population clustering analysis. (A) Annual precipitation, (B) PET, and (C) Annual mean temperature. Only genotypes with a membership coefficient (Q) ≥ 0.7 were considered. The genetic groups are colored as in figure 2. Histograms represent the group mean, whereas error bars are the group standard deviation. Different letters were assigned based on Tukey–HSD multiple comparison post hoc test. MW, Mesoamerican wild; AW, Andean Wild; PhI, Northern Peru–Ecuador.

Fig. 6.

Graphical representation of the different demographic models compared in the current study. (A) Mesoamerican model where the Mesoamerican wild (MW) population did not experience any population bottleneck; (B) the Northern Peru–Ecuador model where the Northern Peru–Ecuador (PhI) gene pool did not experience any population bottleneck; and (C) the Protovulgaris model where the ancestral population went extinct after the Mesoamerican and Andean differentiation.