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Abstract Evolutionary change begins at the population scale. Therefore, understanding adaptive variation requires the identification of the factors maintaining and shaping standing genetic variation at the within‐population level. Spatial and temporal environmental heterogeneity represent ecological drivers of within‐population genetic variation, determining the evolutionary trajectory of populations along with random processes. Here, we focused on the effects of spatiotemporal heterogeneity on quantitative and molecular variation in a natural population of the annual plant Arabidopsis thaliana . We sampled 1093 individuals from a Spanish A. thaliana population across an area of 7.4 ha for 10 years (2012–2021). Based on a sample of 279 maternal lines, we estimated spatiotemporal variation in life‐history traits and fitness from a common garden experiment. We genotyped 884 individuals with nuclear microsatellites to estimate spatiotemporal variation in genetic diversity. We assessed spatial patterns by estimating spatial autocorrelation of traits and fine‐scale genetic structure. We analysed the relationships between phenotypic variation, geographical location and genetic relatedness, as well as the effects of environmental suitability and genetic rarity on phenotypic variation. The common garden experiment indicated that there was more temporal than spatial variation in life‐history traits and fitness. Despite the differences among years, genetic distance in ecologically relevant traits (e.g. flowering time) tended to be positively correlated to genetic distance among maternal lines, while isolation by distance was less important. Genetic diversity exhibited significant spatial structure at short distances, which were consistent among years. Finally, genetic rarity, and not environmental suitability, accounted for genetic variation in life‐history traits. Synthesis . Our study highlighted the importance of repeated sampling to detect the large amount of genetic diversity at the quantitative and molecular levels that a single A. thaliana population can harbour. Overall, population genetic attributes estimated from our long‐term monitoring scheme (genetic relatedness and genetic rarity), rather than biological (dispersal) or ecological (vegetation types and environmental suitability) factors, emerged as the most important drivers of within‐population structure of phenotypic variation in A. thaliana . 

Abstract Background Disentangling the drivers of genetic differentiation is one of the cornerstones in evolution. This is because genetic diversity, and the way in which it is partitioned within and among populations across space, is an important asset for the ability of populations to adapt and persist in changing environments. We tested three major hypotheses accounting for genetic differentiation—isolation-by-distance (IBD), isolation-by-environment (IBE) and isolation-by-resistance (IBR)—in the annual plant Arabidopsis thaliana across the Iberian Peninsula, the region with the largest genomic diversity. To that end, we sampled, genotyped with genome-wide SNPs, and analyzed 1772 individuals from 278 populations distributed across the Iberian Peninsula. Results IBD, and to a lesser extent IBE, were the most important drivers of genetic differentiation in A. thaliana . In other words, dispersal limitation, genetic drift, and to a lesser extent local adaptation to environmental gradients, accounted for the within- and among-population distribution of genetic diversity. Analyses applied to the four Iberian genetic clusters, which represent the joint outcome of the long demographic and adaptive history of the species in the region, showed similar results except for one cluster, in which IBR (a function of landscape heterogeneity) was the most important driver of genetic differentiation. Using spatial hierarchical Bayesian models, we found that precipitation seasonality and topsoil pH chiefly accounted for the geographic distribution of genetic diversity in Iberian A. thaliana . Conclusions Overall, the interplay between the influence of precipitation seasonality on genetic diversity and the effect of restricted dispersal and genetic drift on genetic differentiation emerges as the major forces underlying the evolutionary trajectory of Iberian A. thaliana .