Eco-evolutionary factors contribute to chemodiversity in aboveground and belowground cucurbit herbivore-induced plant volatiles

When attacked by insect herbivores, plants emit blends of chemical compounds known as herbivore-induced plant volatiles (HIPVs). Although HIPVs are produced both aboveground and belowground, how HIPVs vary across plant tissues remains unresolved, as do the selective forces shaping interspecific HIPV emission patterns. Here, we compared foliar and root HIPVs within and among closely related plant species and evaluated if different eco-evolutionary forces, including plant domestication, coexistence histories with herbivores, or phylogenetic relatedness, explain HIPV blends. To examine aboveground and belowground patterns in HIPVs, we compared leaf and root volatile profiles for six species in the Cucurbitaceae that differed in domestication status and coexistence history with specialist insect herbivores. We predicted that within-species HIPVs from different tissues would be more similar than HIPV blends among different species, and that plant volatile chemodiversity was reduced by domestication and enhanced by coexistence histories with herbivores. We found that herbivory induced both quantitative and qualitative changes in volatile emissions across all plant species, which were more pronounced aboveground than belowground. Each species produced tissue-specific HIPVs, and foliar and root HIPVs differed among species. Contrary to our predictions, plant domestication enhanced foliar volatile diversity, while coexistence histories with herbivores reduced foliar and root volatile diversity. Additionally, phylogenetic relatedness did not correlate with aboveground or belowground volatiles. Overall, this work furthers our understanding of the eco-evolutionary forces driving patterns in aboveground and belowground HIPV emissions, elucidating an important and previously undescribed component of within-plant variation in chemodiversity. Herbivore-induced plant volatiles differ between aboveground leaves and belowground roots both within and among plant species in the Cucurbitaceae, and these differences are correlated with plant domestication and herbivore coexistence history, but not phylogenetic relatedness.image