Neutral and Adaptive Drivers of Microgeographic Genetic Divergence within Continuous Populations: The Case of the Neotropical Tree Eperua falcata (Aubl.)

Background: In wild plant populations, genetic divergence within continuous stands is common, sometimes at very short geographical scales. While restrictions to gene flow combined with local inbreeding and genetic drift may cause neutral differentiation among subpopulations, microgeographical variations in environmental conditions can drive adaptive divergence through natural selection at some targeted loci. Such phenomena have recurrently been observed in plant populations occurring across sharp environmental boundaries, but the interplay between selective processes and neutral genetic divergence has seldom been studied. Methods: We assessed the extent of within-stand neutral and environmentally-driven divergence in the Neotropical tree Eperua falcate Aubl. (Fabaceae) through a genome-scan approach. Populations of this species grow in dense stands that cross the boundaries between starkly contrasting habitats. Within-stand phenotypic and candidate-gene divergence have already been proven, making this species a suitable model for the study of genome-wide microgeographic divergence. Thirty trees from each of two habitats (seasonally flooded swamps and well-drained plateaus) in two separate populations were genotyped using thousands of AFLPs markers. To avoid genotyping errors and increase marker reliability, each sample was genotyped twice and submitted to a rigorous procedure for data cleaning, which resulted in 1196 reliable and reproducible markers. Results: Despite the short spatial distances, we detected within-populations genetic divergence, probably caused by neutral processes, such as restrictions in gene flow. Moreover, habitat-structured subpopulations belonging to otherwise continuous stands also diverge in relation to environmental variability and habitat patchiness: we detected convincing evidence of divergent selection at the genome-wide level and for a fraction of the analyzed loci (comprised between 0.25% and 1.6%). Simulations showed that the levels of differentiation for these outliers are compatible with scenarios of strong divergent selection.