Occupation of bare habitats, an evolutionary precursor to soil specialization in plants

Significance Integrating molecular phylogenies with clade-wide ecological data is expanding our ability to address classic ecological questions, such as the origins and maintenance of plant soil specialists, a global source of plant biodiversity. We reconstruct selective forces related to serpentine soil specialization using clade-wide microhabitat characterizations, soil physicochemical data, and phylogenetic hypotheses. Surprisingly, species’ occupation of bare environments, not of chemically similar soils, preceded shifts to serpentine soils. Additionally, inhabiting bare environments traded off with competitive ability in multispecies greenhouse experiments, a relationship potentially contributing to soil endemism. We find that combining in situ detailed field ecological data, greenhouse experiments, and phylogenetic hypotheses can reveal underappreciated selective pressures and provide powerful tools to deepen our understanding of evolutionary pathways underlying biodiversity. Plant soil specialists contribute greatly to global diversity; however, the ecoevolutionary forces responsible for generating this diversity are poorly understood. We integrate molecular phylogenies with descriptive and experimental ecological data, creating a powerful framework with which to elucidate forces driving soil specialization. Hypotheses explaining edaphic specialization have historically focused on costs of adaptation to elements (e.g., nickel, calcium/magnesium) and accompanying tradeoffs in competitive ability in benign soils. We combine in situ microhabitat data for 37 streptanthoid species (Brassicaceae), soil analyses, and competition experiments with their phylogeny to reconstruct selective forces generating serpentine soil endemism, which has four to five independent origins in this group. Coupling ancestral state reconstruction with phylogenetic independent contrasts, we examine the magnitude and timing of changes in soil and habitat attributes relative to inferred shifts to serpentine. We find large changes in soil chemistry at nodes associated with soil shifts, suggesting that elemental changes occurred concomitantly with soil transitions. In contrast, the amount of bare ground surrounding plants in the field (“bareness”), which is greater in serpentine environments, is conserved across soil-type shifts. Thus, occupation of bare environments preceded shifts to serpentine, and may serve as an evolutionary precursor to harsh elemental soils and environments.