Extremely fine-scale soil heterogeneity in a rare serpentine endemic plant shapes patterns of genetic diversity

Studies of population genetic structure are typically conducted at the scale of species distributions and encompass large distances and substantial environmental variation. However, population genetic structure could also be present in species with highly restricted global distributions, such as habitat specialists with threatened or vulnerable conservation status. For these organisms, low dispersal distances coupled with fine-scale environmental heterogeneity could influence population genetic composition, potentially creating spatial genetic structure and genotype by environment associations. Here we use the serpentine endemic plant Calochortus tiburonensis, with a global distribution of 160 ha, to evaluate whether fine-scale structure in soil composition and low seed dispersal distances result in the development of population genetic structure. We paired soil elemental analysis with a RAD-seq SNP dataset for 24 C. tiburonensis individuals. Although no population structure was detected between C. tiburonensis sampling locations, multiple analyses identified associations between soil composition and genetic distance between individuals. This included associations with nickel and magnesium, two elements that were expected a priori to impact plant fitness in serpentine landscapes. However, redundancy analyses and a generalized dissimilarity model both suggest that total soil variation better explains differences in genetic composition between individuals, implying that selection from the holistic soil environment has a role in matching plant genotypes to the microenvironment. Our results indicate that fine-scale environmental heterogeneity could influence genetic differences between individuals in plant populations, even in the absence of population genetic structure. Additionally, these associations between genetic composition and fine-scale environmental heterogeneity implicate extremely fine-scale environmental heterogeneity as an essential mechanism for preserving genetic variation, particularly within range-limited species.