A genome-wide scan shows evidence for local adaptation in a widespread keystone Neotropical forest tree

Abstract

The role of natural selection in shaping patterns of diversity is still poorly understood in the Neotropics. We carried out the first genome-wide population genomics study in a Neotropical tree, Handroanthus impetiginosus (Bignoniaceae), sampling 75,838 SNPs by sequence capture in 128 individuals across 13 populations. We found evidences for local adaptation using Bayesian correlations of allele frequency and environmental variables (32 loci in 27 genes) complemented by an analysis of selective sweeps and genetic hitchhiking events using SweepFinder2 (81 loci in 47 genes). Fifteen genes were identified by both approaches. By accounting for population genetic structure, we also found 14 loci with selection signal in a STRUCTURE-defined lineage comprising individuals from five populations, using Outflank. All approaches pinpointed highly diverse and structurally conserved genes affecting plant development and primary metabolic processes. Spatial interpolation forecasted differences in the expected allele frequencies at loci under selection over time, suggesting that H. impetiginosus may track its habitat during climate changes. However, local adaptation through natural selection may also take place, allowing species persistence due to niche evolution. A high genetic differentiation was seen among the H. impetiginosus populations, which, together with the limited power of the experiment, constrains the improved detection of other types of soft selective forces, such as background, balanced, and purifying selection. Small differences in allele frequency distribution among widespread populations and the low number of loci with detectable adaptive sweeps advocate for a polygenic model of adaptation involving a potentially large number of small genome-wide effects.