Repeated global adaptation across plant species

Abstract Global adaptation occurs when all populations of a species undergo selection toward a common optimum. This can occur by a hard selective sweep with the emergence of a new globally advantageous allele that spreads throughout a species’ natural range until reaching fixation. This evolutionary process leaves a temporary trace in the region affected, which is detectable using population genomic methods. While selective sweeps have been identified in many species, there have been few comparative and systematic studies of the genes involved in global adaptation. Building upon recent findings showing repeated genetic basis of local adaptation across independent populations and species, we asked whether certain genes play a more significant role in driving global adaptation across plant species. To address this question, we scanned the genomes of 17 plant species to identify signals of repeated global selective sweeps. Despite the substantial evolutionary distance between the species analysed, we identified several gene families with strong evidence of repeated positive selection. These gene families tend to be enriched for reduced pleiotropy, consistent with predictions from Fisher’s evolutionary model and the cost of complexity hypothesis. We also found that genes with repeated sweeps exhibit elevated levels of gene duplication. Our findings contrast with recent observations of increased pleiotropy in genes driving local adaptation, consistent with predictions based on the theory of migration-selection balance. Significance Global adaptation occurs when a species undergoes selection toward a common optimum throughout its natural range. While instances of global adaptation are widespread in the literature, there is a shortage of comparative studies aimed at understanding its genetic architecture and how it contrasts with that of local adaptation. This research compares global selective sweeps across 17 plant species to uncover the attributes of the genetic loci repeatedly involved in adaptation. We show that global adaptation tends to rely on genes with reduced pleiotropy and is characterized by increased levels of gene duplication. This finding contrasts with recent observations of increased pleiotropy in genes driving local adaptation, reflecting the opposing dynamics underlying these two evolutionary processes.