Effect of Plant Defenses and Plant Nutrients on the Performance of Specialist and Generalist Herbivores of Datura: A Macroevolutionary Study

Abstract

Macroevolutionary patterns in the association between plant species and their herbivores result from ecological divergence promoted by, among other factors, plants’ defenses and nutritional quality, and herbivore adaptations. Here, we assessed the performance of the herbivores Lema trilineata daturaphila, a trophic specialist on Datura, and Spodoptera frugiperda, a polyphagous pest herbivore, when fed with species of Datura. We used comparative phylogenetics and multivariate methods to examine the effects of Datura species’ tropane alkaloids, leaf trichomes, and plant macronutrients on the two herbivores´ performances (amount of food consumed, number of damaged leaves, larval biomass increment, and larval growth efficiency). The results indicate that species of Datura do vary in their general suitability as food host for the two herbivores. Overall, the specialist performs better than the generalist herbivore across Datura species, and performance of both herbivores is associated with suites of plant defenses and nutrient characteristics. Leaf trichomes and major alkaloids of the Datura species are strongly related to herbivores’ food consumption and biomass increase. Although hyoscyamine better predicts the key components of the performance of the specialist herbivore, scopolamine better predicts the performance of the generalist; however, only leaf trichomes are implicated in most performance components of the two herbivores. Nutrient quality more widely predicts the performance of the generalist herbivore. The contrasting effects of plant traits and the performances of herbivores could be related to adaptive differences to cope with plant toxins and achieve nutrient balance and evolutionary trade-offs and synergisms between plant traits to deal with a diverse community of herbivores.

Comparative transcriptome profiling reveals distinct regulatory responses of secondary defensive metabolism in Datura species (Solanaceae) under plant development and herbivory‐mediated stress

“…However, high concentration of major alkaloids hyoscyamine and scopolamine previously documented in these species may result from continuous levels of high gene expression instead of induction. In a recent study that examined the performance of specialist and generalist herbivores in the genus Datura , it was documented that D. inoxia is one of the few species of the genus in which L. t. daturaphila performs poorly (Kariñho‐Betancourt et al., 2023 ), suggesting a strong negative effect of defensive alkaloids. Notably, even when almost no differential expression was detected in D. inoxia , this species showed the highest expression of TR‐I and H6H , suggesting that the highest relative concentration of hyoscyamine documented for the genus (Kariñho‐Betancourt et al., 2015 ) is not associated to transcriptional changes.…”

“…These compounds exhibit large variation during development, which seems to be associated with their adaptive role to cope with diverse herbivore guilds (De‐la‐Cruz et al., 2020 , 2021 ; Kariñho‐Betancourt et al., 2015 ; Miranda‐Pérez et al., 2016 ). Across the phylogeny of Datura , the specialist herbivore L. t. daturaphila has shown to be differentially affected by specific classes of defensive compounds, including major alkaloids scopolamine and hyoscyamine (Kariñho‐Betancourt et al., 2023 ). Nonetheless, the molecular basis of response to herbivory and their interplay with developmental variation of secondary metabolites has never been evaluated in Datura .…”