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Contrary to previous assumptions that most mutations are deleterious, there is increasing evidence for persistence of large-effect mutations in natural populations. A possible explanation for these observations is that mutant phenotypes and fitness may depend upon the specific environmental conditions to which a mutant is exposed. Here, we tested this hypothesis by growing large-effect flowering time mutants of Arabidopsis thaliana in multiple field sites and seasons to quantify their fitness effects in realistic natural conditions. By constructing environment-specific fitness landscapes based on flowering time and branching architecture, we observed that a subset of mutations increased fitness, but only in specific environments. These mutations increased fitness via different paths: through shifting flowering time, branching, or both. Branching was under stronger selection, but flowering time was more genetically variable, pointing to the importance of indirect selection on mutations through their pleiotropic effects on multiple phenotypes. Finally, mutations in hub genes with greater connectedness in their regulatory networks had greater effects on both phenotypes and fitness. Together, these findings indicate that large-effect mutations may persist in populations because they influence traits that are adaptive only under specific environmental conditions. Understanding their evolutionary dynamics therefore requires measuring their effects in multiple natural environments.more » « less
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Fournier‐Level, Alexandre ; Taylor, Mark A. ; Paril, Jefferson F. ; Martínez‐Berdeja, Alejandra ; Stitzer, Michelle C. ; Cooper, Martha D. ; Roe, Judith L. ; Wilczek, Amity M. ; Schmitt, Johanna ( , New Phytologist)
Summary The relevance of flowering time variation and plasticity to climate adaptation requires a comprehensive empirical assessment. We investigated natural selection and the genetic architecture of flowering time in Arabidopsis through field experiments in Europe across multiple sites and seasons.
We estimated selection for flowering time, plasticity and canalization. Loci associated with flowering time, plasticity and canalization by genome‐wide association studies were tested for a geographic signature of climate adaptation.
Selection favored early flowering and increased canalization, except at the northernmost site, but was rarely detected for plasticity. Genome‐wide association studies revealed significant associations with flowering traits and supported a substantial polygenic inheritance. Alleles associated with late flowering, including functional
FRIGIDA variants, were more common in regions experiencing high annual temperature variation. Flowering time plasticity to fall vs spring and summer environments was associated withGIGANTEA SUPPRESSOR 5 , which promotes early flowering under decreasing day length and temperature.The finding that late flowering genotypes and alleles are associated with climate is evidence for past adaptation. Real‐time phenotypic selection analysis, however, reveals pervasive contemporary selection for rapid flowering in agricultural settings across most of the species range. The response to this selection may involve genetic shifts in environmental cuing compared to the ancestral state.