Attracting pollinators vs escaping herbivores: eco-evolutionary dynamics of plants confronted with an ecological trade-off

Abstract Many plant traits are subject to an ecological trade-off between attracting pollinators and escaping herbivores. The interplay of both plant-animal interaction types determines their evolution. As most studies focus on either pollination or herbivory, how they jointly affect the eco-evolutionary dynamics of plant-animal communities is often left unknown. Within a plant-pollinator-herbivore community where interaction strengths depend on trait matching, we consider the evolution of a plant trait involved in both plant-animal interactions. Using adaptive dynamics, we uncover when stabilizing, runaway (i.e. directional) or disruptive selection emerges and its consequences for multispecies coexistence. We find that strong pollination relative to herbivory favors stabilizing selection and coexistence. Strong herbivory relative to pollination fosters runaway selection and threatens coexistence. Importantly, given balanced interactions, joint effects may lead to disruptive selection, allowing the emergence of plant dimorphism. The strength of the ecological trade-off largely explains the occurrence of these contrasting eco-evolutionary dynamics. In particular, plant diversification requires strong trade-offs, with the strongest trade-offs allowing long-term polymorphism. We discuss how our results relate to various empirical cases where the interplay of pollination and herbivory maintains plant polymorphism. Beyond maintenance, our work suggests that it might also have fueled the diversification process itself. Graphical Abstract Eco-evolutionary dynamics resulting from the evolution of plant phenotype under ecological trade-off A. Typical eco-evolutionary landscape . The type of selection and the ecological outcome depend on the dissimilarity between animal phenotypes (i.e. preferences for plant phenotype), which is a proxy for the strength of the ecological trade-off. B. The long-term community composition depends on the type of selection. (1) Runaway selection leads to the extinction of a first animal species as the plant phenotype is diverging. (a) Pollinators are lost first so that runway selection continues until herbivores are also lost. (b) Herbivores are lost first so that selection turns stabilizing over time, leading to a perfect plant-pollinator matching. (2) Stabilizing selection can enable the maintenance of coexistence. (3) Disruptive selection leads to the emergence of plant dimorphism.