Abstract
An evolutionary response to selection requires genetic variation; however, even if it exists, then the genetic details of the variation can constrain adaptation. In the simplest case, unlinked loci and uncorrelated phenotypes respond directly to multivariate selection and permit unrestricted paths to adaptive peaks. By contrast, ‘antagonistic’ pleiotropic loci may constrain adaptation by affecting variation of many traits and limiting the direction of trait correlations to vectors that are not favoured by selection. However, certain pleiotropic configurations may improve the conditions for adaptive evolution. Here, we present evidence that the Arabidopsis thaliana gene FRI (FRIGIDA) exhibits ‘adaptive’ pleiotropy, producing trait correlations along an axis that results in two adaptive strategies. Derived, low expression FRI alleles confer a ‘drought escape’ strategy owing to fast growth, low water use efficiency and early flowering. By contrast, a dehydration avoidance strategy is conferred by the ancestral phenotype of late flowering, slow growth and efficient water use during photosynthesis. The dehydration avoidant phenotype was recovered when genotypes with null FRI alleles were transformed with functional alleles. Our findings indicate that the well-documented effects of FRI on phenology result from differences in physiology, not only a simple developmental switch.
Highlights
Populations of a species are frequently distributed across climatic gradients, where natural selection can lead to adaptation to local conditions
To study the adaptive value of pleiotropic loci, it is necessary to assess the effects of genetic variation on the structure of many phenotypes which are subject to correlational selection in nature
Using genome-wide approaches, allelic variants and transgenic manipulation, we demonstrate that the ‘flowering time (FT)’ gene, FRIGIDA (FRI) pleiotropically affects phenotypic variation in growth rate, water use efficiency (WUE) and FT
Summary
Populations of a species are frequently distributed across climatic gradients, where natural selection can lead to adaptation to local conditions. The environmental conditions that cause local adaptation have been well documented through reciprocal transplants and studies of clines [1,2,3,4,5,6] These experiments show that divergent patterns of selection cause shifts in the mean values of many traits leading to a multivariate response. To study the adaptive value of pleiotropic loci, it is necessary to assess the effects of genetic variation on the structure of many phenotypes which are subject to correlational selection in nature. Null FRI alleles produce a drought escape phenotype (decreased WUE, increased growth rate, decreased FT) relative to the ancestral adaptive strategy This phenomenon, which we term ‘adaptive pleiotropy’, enhances the likelihood of adaptation by increasing adaptive responses to selection
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