Abstract
Tripartite interactions between plants, herbivores, and pollinators hold fitness consequences for most angiosperms. However, little is known on how plants evolve in response—and in particular what the net selective outcomes are for traits of shared relevance to pollinators and herbivores. In this study, we manipulated herbivory (“presence” and “absence” treatments) and pollination (“open” and “hand pollination” treatments) in a full factorial common‐garden experiment with woodland strawberry (Fragaria vesca L.). This design allowed us to quantify the relative importance and interactive effects of herbivore‐ and pollinator‐mediated selection on nine traits related to plant defence and attraction. Our results showed that pollinators imposed stronger selection than herbivores on traits related to both direct and indirect (i.e., tritrophic) defence. However, conflicting selection was imposed on inflorescence density: a trait that appears to be shared by herbivores and pollinators as a host plant signal. However, in all cases, selection imposed by one agent depended largely on the presence or ecological effect of the other, suggesting that dynamic patterns of selection could be a common outcome of these interactions in natural populations. As a whole, our findings highlight the significance of plant‐herbivore‐pollinator interactions as potential drivers of evolutionary change, and reveal that pollinators likely play an underappreciated role as selective agents on direct and in direct plant defence.
Highlights
Impact Summary This study advances understanding of plant-herbivorepollinator interactions in revealing how these interactions can influence the phenotypic evolution of plant defence and attractive traits
Herbivores have long been considered the primary drivers of defence trait evolution in plant populations
We offer a novel counter to this preconception, and provide the first empirical support demonstrating the importance of pollinators as selective agents on direct and indirect defence traits, which here even surpassed that of herbivores
Summary
Impact Summary This study advances understanding of plant-herbivorepollinator interactions in revealing how these interactions can influence the phenotypic evolution of plant defence and attractive traits. We offer a novel counter to this preconception, and provide the first empirical support demonstrating the importance of pollinators as selective agents on direct and indirect defence traits, which here even surpassed that of herbivores. We revealed that the net selective pressures arising from these interactions were highly dynamic, and depended largely on the presence or ecological effects of the other agent. These findings are important given there remains a lack of studies that simultaneously quantify pollinator- and herbivore-mediated selection on the same trait. Our study highlights the possible evolutionary trajectories of defence and attractive traits in natural populations, and how pollinator and herbivore selective pressures are expected to interactively shape this evolution
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