Plant-soil feedbacks trigger tannin evolution by niche construction: a spatial stoichiometric model

Abstract

Among plant traits, plant secondary metabolites such as tannins mediate plant-herbivore interactions but also have after-life effects on litter decomposition and nutrient cycling, which could influence their evolution. By modeling the flow of nitrogen and carbon through plants and soil in a spatially explicit context, we explored the relative contribution of herbivory and plant-soil feedbacks as drivers of tannin evolution. We assumed soil nitrogen to be composed of labile and recalcitrant compartments, the latter made of tannin-protein complexes accessible by plants via associations with mycorrhizal fungi. In unproductive environments and for plants with low biomass turnover rates, we show that when tannins modify soil properties locally, plant-soil feedbacks alone can drive their evolution. We further predict the existence of positive coevolutionary feedbacks between associations with mycorrhizae and tannins, possibly triggered by the evolution of the latter as protection against herbivores. In line with our theoretical results, tannins are mostly present in conservative plants, associated with mycorrhizae and inhabiting unproductive environments. Our work suggests that plant-soil feedbacks can enable niche construction mechanisms which can be key to the evolution of plant traits.