Testing the optimal defense hypothesis in nature: Variation for glucosinolate profiles within plants

Abstract

Plants employ highly variable chemical defenses against a broad community of herbivores, which vary in their susceptibilities to specific compounds. Variation in chemical defenses within the plant has been found in many species; the ecological and evolutionary influences on this variation, however, are less well-understood. One central theory describing the allocation of defenses in the plant is the Optimal Defense Hypothesis (ODH), which predicts that defenses will be concentrated in tissues that are of high fitness value to the plant. Although the ODH has been repeatedly supported within vegetative tissues, few studies have compared vegetative and reproductive tissues, and the results have not been conclusive. We quantified variation in glucosinolate profile and tissue value between vegetative and reproductive tissues in Boechera stricta, a close relative of Arabidopsis. B. stricta manufactures glucosinolates, a set of defensive compounds that vary genetically and are straightforward to quantify. Genetic diversity in glucosinolate profile has been previously demonstrated to be important to both herbivory and fitness in B. stricta; however, the importance of glucosinolate variation among tissues has not. Here, we investigate whether allocation of glucosinolates within the plant is consistent with the ODH. We used both clipping experiments on endogenous plants and ambient herbivory in a large-scale transplant experiment at three sites to quantify fitness effects of loss of rosette leaves, cauline leaves, and flowers and fruits. We measured glucosinolate concentration in leaves and fruits in the transplant experiment, and asked whether more valuable tissues were more defended. We also investigated within-plant variation in other aspects of the glucosinolate profile. Our results indicated that damage to fruits had a significantly larger effect on overall fitness than damage to leaves, and that fruits had much higher concentrations of glucosinolates, supporting the ODH. This is, to the best of our knowledge, the first study to explicitly compare both tissue value and chemical defense concentrations between vegetative and reproductive tissues under natural conditions.

Antagonistic selection and pleiotropy constrain the evolution of plant chemical defenses

“…). Glucosinolates vary among tissues both in total concentration and BC‐ratio (Keith and Mitchell‐Olds ).…”

“…; Velasco et al. ; Keith and Mitchell‐Olds ). Glucosinolates are not manufactured independently in each tissue; long‐distance transport of glucosinolates and precursors has been documented in Arabidopsis thaliana (reviewed in Halkier and Gershenzon ; Jørgensen et al.…”

“…Both glucosinolate concentration and chemical composition (“glucosinolate profile”) vary genetically among individuals as well as within plants (Prasad et al. ; Keith and Mitchell‐Olds ). Boechera stricta has four major types of aliphatic glucosinolates.…”

“…Like many other traits, defenses, both chemical and physical, are not homogeneous within a plant (Nitao and Zangerl 1987;Zangerl and Rutledge 1996;Ohnmeiss and Baldwin 2000). For glucosinolates, the primary defensive compounds found in the Brassicaceae, concentration and composition have been shown to vary among tissue types (Brown et al 2003;Bellostas et al 2007;Velasco et al 2008;Keith and Mitchell-Olds 2017). Glucosinolates are not manufactured independently in each tissue; long-distance transport of glucosinolates and precursors has been documented in Arabidopsis thaliana (reviewed in Halkier and Gershenzon 2006;Jørgensen et al 2015;Burow and Halkier 2017).…”

Divergent host plant utilization by adults and offspring is related to intra‐plant variation in chemical defences

“…Plant defences are often differentially expressed among tissues, impacting how resources are utilized by herbivores (Agrawal & Fishbein, ; Farrell, Mitter, & Futuyma, ; Futuyma & Agrawal, ). Expression of defences can be influenced by numerous environmental and physiological mechanisms, and vary across different phenological windows (Aide, ; Keith & Mitchell‐Olds, ; Kursar & Coley, ; Meyer & Paul, ; Wurst, Van Dam, Monroy, Biere, & Van Der Putten, ). Different herbivore species are capable of co‐occurring in populations through inter‐ and intraspecific spatial and successional segregation that ultimately reduces competition (Amarasekare, ).…”