Disentangling the effects of jasmonate and tissue loss on the sex allocation of an annual plant

Abstract

Selection through pollinators plays a major role in the evolution of reproductive traits. However, herbivory can also induce changes in plant sexual expression and sexual systems, potentially influencing conditions governing transitions between sexual systems. Previous work has shown that herbivory has a strong effect on sex allocation in the wind-pollinated annual plant Mercurialis annua, likely via responses to resource loss. It is also known that many plants respond to herbivory by inducing signaling, and endogenous responses to it, via the plant hormone jasmonate. Here, we attempt to uncouple the effects of herbivory on sex allocation in M. annua through resource limitation (tissue loss) versus plant responses to jasmonate hormone signaling. We used a two-factorial experiment with four treatment combinations: control, herbivory (25% chronic tissue loss), jasmonate, and combined herbivory and jasmonate. We estimated the effects of tissue loss and defense-inducing hormones on reproductive allocation, male reproductive effort, and sex allocation. Tissue loss caused plants to reduce their male reproductive effort, resulting in changes in total sex allocation. However, application of jasmonate after herbivory reversed its effect on male investment. Our results show that herbivory has consequences on plant sex expression and sex allocation, and that defense-related hormones such as jasmonate can buffer the impacts. We discuss the physiological mechanisms that might underpin the effects of herbivory on sex allocation, and their potential implications for the evolution of plant sexual systems.

Keywords: Mercurialis annua; anti-herbivore defenses; defoliation; herbivory; hormone; jasmonate; sex allocation; sexual system.

FIGURE 1

Direct (tissue loss) and indirect (jasmonate-mediated) effects of herbivory on (A) male reproductive effort (male inflorescence biomass/vegetative biomass), (B) female reproductive function (seed biomass/vegetative biomass), (C) total reproductive effort (reproductive biomass/vegetative biomass), (D) total aboveground plant biomass. Note that variables in panels (A–C) were calculated on the basis of measurements of the apical subsample for each individual sampled. Treatments are abbreviated as follows, C, control; H, herbivory treatment with a chronic tissue loss of 25% of foliar area; JA, jasmonate application; JAH, tissue loss and jasmonate application treatment. Different letters indicate significant differences between treatment levels (P < 0.05). Total N = 273 plants.