Contrasting and fluctuating selection from direct and indirect herbivory drives transient plant evolution

Predicting evolution in nature requires separating the forces acting directly on traits from those indirectly acting through ecological pathways. In a two-year outdoor mesocosm with Spirodela polyrhiza and its herbivore, we experimentally partitioned direct from indirect herbivory effects and tracked their evolutionary consequences. In the first year, herbivory reduced duckweed abundance but indirectly promoted growth by reducing algal competition and increasing phosphate availability, shifting plant traits and genotype frequencies. In the second year, a macroalgal bloom co-occurred with severe phosphate depletion, eliminating these effects and reversing the direction of selection on defence metabolites. Across years and metabolites, selection from direct effects was strong but fluctuated, whereas selection from indirect effects was weaker yet more consistent and frequently antagonistic with direct effects, buffering net evolutionary change. A macroalgal bloom with phosphate depletion erased earlier signals and reversed selection, identifying a community-level factor that constrains the predictability of evolution in natural ecosystems.