The demographic and ecological factors shaping diversification among rare Astragalus species

Abstract

Aim: Evolutionary radiations are central to the origin and maintenance of biodiversity, yet we rarely understand how they are jointly shaped by demography and ecological opportunity. Astragalus is the largest plant genus in the world and is disproportionately comprised of rare species restricted to narrow geographic and ecological regions. Here, we explored the demographic and ecological mechanisms underlying patterns of diversification in a threatened Astragalus species complex endemic to a small desert region in the western United States. Location: Southeast Utah, USA. Methods: We used high-throughput DNA sequencing to infer genetic structure, genetic diversity, and demographic history (i.e., the timing of population divergence, effective population sizes and gene flow) among Astragalus taxa. We performed landscape genetic analyses to quantify the relationships between genetic differentiation, geographic distance, and ecological distance based on bioclimatic and soil variables. Finally, we identified putative adaptive loci that show higher genetic differentiation between taxa than expected based on our inferred neutral demographic model. Results: We found evidence of low gene flow between three highly differentiated taxa (currently delineated as A. iselyi, A. sabulosus var. sabulosus and A. sabulosus var. vehiculus) that rapidly diverged from a small ancestral population near the beginning of the last glacial period. Genomic signatures revealed long-term effective population sizes are 2–10× larger than recent census sizes, perhaps due to the maintenance of standing genetic variation through seed banks. Consistent with limited dispersal and local adaptation, genome-wide patterns of differentiation are shaped by geographic distance (isolation-by-distance) and climate and soil variation (isolation-by-environment). Taxon-specific adaptation is further supported by uncovering putative adaptive loci. Main Conclusions: Our findings suggest that interactions between demography (i.e., dispersal limitations and seeds banks) and ecological opportunity (i.e., spatial and temporal environmental heterogeneity) may promote diversification, endemism, and rarity among closely related Astragalus species and similar plant clades distributed across complex landscapes.