Identifying synergies and antagonisms between plant defense traits in Asclepias syriaca

Abstract

AbstractAs a general rule, plants defend against herbivores with multiple traits. The defense synergy hypothesis posits that some traits are more potent when co-expressed with others, compared to their independent potency. However, this hypothesis has rarely been tested outside of synergies within a class of particular phytochemicals, and seldom under field conditions. We tested for synergies between multiple defense traits of common milkweed (Asclepias syriaca) by assaying the performance of two specialist herbivores on plants in natural populations. We employed both standard regression and exploratory analysis using a novel application of Random Forests that allowed us to detect synergies between defense traits. In hypothesis testing, we found the first empirical evidence for a previously hypothesized synergy between one pair of co-expressed defense traits (latex and cardenolides), but not another (latex and trichomes). When exploring all potential interactions between pairs of traits we found eight synergies and five antagonisms in predicting herbivore performance. Half of the identified synergies involved carbon, which is the basis of several defenses including chemical and physical barriers to feeding, and also essential nutrients. Our findings suggest that defense synergies could explain co-expression of latex and cardenolides in milkweeds. This synergy may be common among the diverse plant species that employ latex as a defense. Future studies should test carbon-based synergies, which our work suggests are prevalent, as well as the other synergies identified in our exploratory analysis. Our analytic approach provides a general, flexible framework for more broadly discovering and predicting the coexpression of traits through their synergistic function.