External insect gall morphology influences the functional guilds of natural enemy communities

The evolution of diverse and novel morphological traits is poorly understood, especially how symbiotic interactions can drive these adaptations. The extreme diversity of external traits in insect-induced galls is currently explained by the Enemy Hypothesis, in which these traits have selective advantage in deterring parasitism. While previous tests of this hypothesis used only taxonomic identity, we argue that ecologically functional traits of enemies (i.e. mode of parasitism, larval development strategy) are a crucial addition. Here, we characterize parasitoid guild composition across four disparate gall systems and find consistent patterns of association between enemy guild and gall morphology. Specifically, galls with a longer average larva-to-surface distance host a significantly higher proportion of enemies with a distinct combination of functional traits (i.e. ectoparasitic, idiobiont, elongate ovipositor). Our results support the Enemy Hypothesis and highlight the importance of species ecology in examining insect communities and the evolution of novel defensive characters.