Direct and indirect effects of a sex-biased antagonist on male and female fertility: consequences for reproductive trait evolution in a gender-dimorphic plant

Abstract

Gender-dimorphic plants are often subject to sex-differential enemy attack, but whether and how this contributes to trait evolution is unknown. To address this gap, we documented the spatiotemporal prevalence of sex-biased weevil damage in a gynodioecious strawberry. We then conducted path analysis to evaluate the direct and indirect pathways for weevils to affect female and male fertility and to mediate selection in two experimental gardens. Direct effects of weevils significantly reduced fertility and mediated selection on reproductive traits, even in the nonpreferred sex (females). Weevils significantly reduced floral display size in hermaphrodites in both gardens, and this translated into a substantial negative indirect effect on male fertility in the garden where the pathway to fertility via display was stronger. Thus, indirect effects of weevils can contribute to selection in hermaphrodites, which gain the majority of their fitness via male function. Our results also indicate that weevils often play a larger role than pollinators in shaping reproductive phenotype and thus raise the intriguing possibility that antagonists may be drivers of sexual dimorphism. Finally, our results support the view that mutualists, antagonists, and the abiotic environment should be considered when attempting to understand reproductive trait evolution in gender-dimorphic species.