Natural variation on whole-plant form in the wild is influenced by multivariate soil nutrient characteristics: natural selection acts on root traits

Abstract

Premise: In the complex soil nutrient environments of wild populations of annual plants, in general, low nutrient availability restricts growth and alters root–shoot relationships. However, our knowledge of natural selection on roots in field settings is limited. We sought to determine whether selection acts directly on root traits and to identify which components of the soil environment were potential agents of selection. Methods: We studied wild native populations of Arabidopsis thaliana across 4 years, measuring aboveground and belowground traits and analyzing soil nutrients. Using multivariate methods, we examined patterns of natural selection and identified soil attributes that contributed to whole-plant form. In a common garden experiment at two field sites with contrasting soil texture, we examined patterns of selection on root and shoot traits. Results: In wild populations, we uncovered selection for above- and belowground size and architectural traits. We detected variation through time and identified soil components that influenced fruit production. In the garden experiment, we detected a distinct positive selection for total root length at the site with greater water-holding capacity and negative selection for measures of root architecture at the field site with reduced nutrient availability and water holding capacity. Conclusions: Patterns of natural selection on belowground traits varied through time, across field sites and experimental gardens. Simultaneous investigations of above- and belowground traits reveal trait functional relationships on which natural selection can act, highlighting the influence of edaphic features on evolutionary processes in wild annual plant populations.