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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. 

Abstract Insect-induced galls are novel structures that serve as habitat to whole communities of associate arthropods that include predators, parasitoids, and inquilines. Galling insects are generally under-described, but their associate communities, which can include many specialist organisms, are virtually unknown, particularly in the southwest United States. Aciurina bigeloviae (Cockerell 1890) and Aciurina trixa Curran 1932 (Diptera: Tephritidae) are unusually common and abundant galling flies in New Mexico. The 2 species are sister and occur in sympatric areas but have distinct gall morphologies. We reared all arthropods from 3,800 galls from 14 sites in the northern and central regions of the state and as a result characterized the complete communities of both species, including barcode sequences and eclosion phenology. We also investigate interactions of A. trixa galls with the abundant inquiline weevil Anthonomus cycliferus Fall 1913 (Coleoptera: Circulionidae) and find no measurable effect of inquiline abundance on the size of the emerged adult fly or gall. The total species count is 24 and includes 6 guilds; both A. bigeloviae and A. trixa communities are richer and more complex than other documented Tephritidae–Asteraceae galling systems. This study highlights the potential of galling insects as ecosystem engineers to maintain large, rich, and multi-trophic communities.