Unraveling the polyacetylene paradox: Reciprocal impacts of multitrophic interactions and chemical defense evolution in tall goldenrod (Solidago altissima)

Multitrophic interactions involving insect herbivores and microbially-mediated plant-soil feedbacks play pivotal roles in shaping plant communities. The community of herbivores and microbes interacting with a plant exert selective pressure on the plant traits mediating these ecological relationships. However, it is poorly understood how herbivores and microbial communities interact to jointly shape selection on plant phenotypes. We investigated how microbial plant-soil feedbacks and herbivory interact to shape root chemical defenses in tall goldenrod (Solidago altissima). Prior research has shown that herbivory exerts strong selection on competitive ability and root chemical defenses in tall goldenrod. Notably, release from natural herbivory was found to lead to strong positive selection on polyacetylene production in goldenrod roots. Polyacetylenes, a highly bioactive class of plant secondary metabolites, are thought to enhance goldenrod's competitive ability through allelopathic effects on neighboring plants.

Through a series of common garden experiments, we explored an alternative hypothesis that polyacetylenes may also increase plant fitness by beneficially influencing rhizosphere microbial communities. We found that the effects of polyacetylenes on plant performance are strongly dependent on the microbial context, suggesting that the performance-enhancing effects of polyacetylenes are microbially-mediated. These polyacetylene-mediated effects on the soil microbiome may, in turn, feedback to affect herbivore performance. Our findings suggest that herbivores and soil microbial communities may be strongly linked through selection on the same plant traits, enhancing our understanding of the complex interplay between plants, herbivores and soil microbial communities.