Signatures of Environmental Adaptation During Range Expansion of Wild Common Bean (Phaseolus vulgaris)

Abstract

Landscape genomics integrates population genetics with landscape ecology, allowing the identification of putative molecular determinants involved in environmental adaptation across the natural geographic and ecological range of populations. Wild Phaseolus vulgaris, the progenitor of common bean (P. vulgaris), has a remarkably extended distribution over 10,000 km from northern Mexico to northwestern Argentina. Earlier research has shown that this distribution represents a range expansion from Mesoamerica to the southern Andes through several discrete migration events and that the species colonized areas with different temperature and rainfall compared to its core area of origin. Thus, this species provides an opportunity to examine to what extent adaptation of a species can be broadened or, conversely, ecological or geographical distribution can be limited by inherent adaptedness. In the current study, we applied a landscape genomics approach to a collection of 246 wild common bean accessions representative of its broad geographical and climatic distribution and genotyped for [~]20K SNPs. We applied two different but complementary approaches for identifying loci putatively involved in environmental adaptation: i) an outlier-detection method that identifies loci showing strong differentiation between sub-populations; ii) an association method based on the identification of loci associated with bio-climatic variables. This integrated approach allowed the identification of several genes showing signature of selection across the different natural sub-populations of this species, as well as genes associated with specific bio-climatic variables related to temperature and precipitation. The current study demonstrates the feasibility of landscape genomics approach for a preliminary identification of specific populations and novel candidate genes involved in environmental adaptation in P. vulgaris. As a resource for broadening the genetic diversity of the domesticated gene pool of this species, the genes identified constitute potential molecular markers and introgression targets for the breeding improvement of domesticated common bean.\n\nAuthor SummaryThe ancestral form of common bean has an unusually large distribution in the Americas, extending over 10,000 km from [~]35{degrees} N. Lat. to [~]35{degrees} S. Lat. This wide distribution results from discrete long-range dissemination events to the Andes region from the original environments in Mesoamerica. It also suggests adaptation to new environments that are distinct from those encountered in Mesoamerica. In this research, we identified genes that may be involved in adaptation to climate variables in these new environments using two methods. A first method - outlier detection - was used to identify genome regions that differentiated the wild bean groups in the Andes resulting from discrete dissemination events among themselves and the different groups in Mesoamerica. The second method - genome-wide association - was used to identify candidate genome regions correlated with these same variables across the entire distribution from Mesoamerica to the southern Andes. The two methods identified two sets of candidate genes, several of which were related to the water status of plants, and illustrate how the genetic architecture of adaptation following long-range dissemination. This study provides sets of candidate genes as well as candidate wild bean populations that need to be corroborated for their use in increasing the water use efficiency of domesticated beans.