Large-effect flowering time mutations reveal conditionally adaptive paths through fitness landscapes inArabidopsis thaliana

Abstract

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.

Natural variation in autumn expression is the major adaptive determinant distinguishing Arabidopsis FLC haplotypes

“…In the field, silique production is closely linked to branch production ( Fig. 7; Taylor et al, 2019). In Arabidopsis, saturation of vernalization requirement is known to increase flowering branch production, particularly rosette branch production, and this effect is linked to FLC (Figure 1 there was little variation in branch production.…”

“…Recent work has shown the importance of analysing flowering in natural field conditions ( Figure 1A ), ‘in natura’ ( Kudoh, 2016 ). Such studies have highlighted how the influence of genes of major effect, including FLC , changes depending on the field environment ( Wilczek et al, 2009 ; Fournier-Level et al, 2011 ; Duncan et al, 2015 ; Ågren et al, 2017 ; Taylor et al, 2019 ). In particular, the investigation of RNA levels in natura has identified genetic mechanisms in the field that were previously unknown from laboratory observations ( Antoniou-Kourounioti et al, 2018 ; Song et al, 2018 ; Nagano et al, 2019 ).…”

Pleiotropy facilitates local adaptation to distant optima in common ragweed (Ambrosia artemisiifolia)

“…By contrast, when phenotypes are nearing their optimal values, large-effect loci become less beneficial because they can overshoot the optimum [6]. Experimental data indicates that the effect-sizes of loci increase with increasing level of pleiotropy [7][8][9], suggesting that highly pleiotropic loci may escape the "cost of complexity" [2] and be selectively advantageous if phenotypes are distant from their selective optima.…”

Plant adaptation to climate change—Where are we?

“…Furthermore, we have a very limited understanding of whether common genes and pathways underlie climatic adaptation across plant species and families. A more complete understanding of plant responses to climate change will only emerge through integrative studies and international collaboration that include field fitness tests across diverse environments and countries (Losos et al, 2013;Taylor et al, 2019).…”