Intermediate degrees of synergistic pleiotropy drive adaptive evolution in ecological time

• Published in: Nature ecology & evolution Vol. 1; no. 10; pp. 1551 - 1561
• Main Authors: Frachon, Léa, Libourel, Cyril, Villoutreix, Romain, Carrère, Sébastien, Glorieux, Cédric, Huard-Chauveau, Carine, Navascués, Miguel, Gay, Laurène, Vitalis, Renaud, Baron, Etienne, Amsellem, Laurent, Bouchez, Olivier, Vidal, Marie, Le Corre, Valérie, Roby, Dominique, Bergelson, Joy, Roux, Fabrice
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.10.2017; Nature Publishing Group; Nature
• Subjects: 631/158/2464; 631/208/182; 631/208/729; 631/449/1870; Arabidopsis thaliana; Architecture; Biological and Physical Anthropology; Biomedical and Life Sciences; Ecology; Evolution; Evolution & development; Evolutionary Biology; Evolutionary genetics; Flowering; Gene mapping; Genes; Genetic diversity; Genetics; Habitats; Life Sciences; Local population; Mapping; Microhabitats; Nucleotides; Paleontology; Pleiotropy; Population genetics; Populations and Evolution; Quantitative trait loci; Regulators; Single-nucleotide polymorphism; Zoology
• ISSN: 2397-334X; 2397-334X
• DOI: 10.1038/s41559-017-0297-1

Rapid phenotypic evolution of quantitative traits can occur within years, but its underlying genetic architecture remains uncharacterized. Here we test the theoretical prediction that genes with intermediate pleiotropy drive adaptive evolution in nature. Through a resurrection experiment, we grew Arabidopsis thaliana accessions collected across an 8-year period in six micro-habitats representative of that local population. We then used genome-wide association mapping to identify the single-nucleotide polymorphisms (SNPs) associated with evolved and unevolved traits in each micro-habitat. Finally, we performed a selection scan by testing for temporal differentiation in these SNPs. Phenotypic evolution was consistent across micro-habitats, but its associated genetic bases were largely distinct. Adaptive evolutionary change was most strongly driven by a small number of quantitative trait loci (QTLs) with intermediate degrees of pleiotropy; this pleiotropy was synergistic with the per-trait effect size of the SNPs, increasing with the degree of pleiotropy. In addition, weak selection was detected for frequent micro-habitat-specific QTLs that shape single traits. In this population, A . thaliana probably responded to local warming and increased competition, in part mediated by central regulators of flowering time. This genetic architecture, which includes both synergistic pleiotropic QTLs and distinct QTLs within particular micro-habitats, enables rapid phenotypic evolution while still maintaining genetic variation in wild populations. The genetic architecture underlying rapid phenotypic changes remains largely unknown. Here, the authors show that genes with an intermediate degree of pleiotropy have the highest rate of adaptive evolution in Arabidopsis thaliana .