Spatiotemporal dynamics of genetic variation at the quantitative and molecular levels within a natural Arabidopsis thaliana population

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.