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Abstract Many herbivorous insect species are capable of hijacking plant development to induce novel plant organs called galls. In most groups of galling insects, the insect organs and molecular signals involved in gall induction are poorly understood. We focused on gall wasps (Hymenoptera:Cynipidae), the second largest clade of gall inducers (~1,400 spp.), for which the developmental stages and organs responsible for gall development are unclear. We investigated the female metasomal anatomy of 69 gall-inducing and 29 non-gall-inducing species across each of the major lineages of Cynipoidea, to test relationships between this lifestyle and the relative size of secretory organs. We confirmed that the venom apparatus in gall-inducing species is greatly expanded, although gall-inducing lineages vary in the relative size of these glands. Among these gallers, we measured the largest venom gland apparatus relative to body size ever recorded in insects. Non-galling inquiline species are accompanied by a reduction of this apparatus. Comparative microscopic analysis of venom glands suggests varying venom gland content across the lineages. Some oak gallers also had enlarged accessory glands, a lipid-rich organ whose function remains unclear, and which has not been previously studied in relation to gall formation. Together, the massive expansion of secretory organs specifically in gall-inducing species suggests a role of these secretions in the process of gall formation, and the variance in size of venom glands, accessory glands, and the contents of these glands among gallers, suggests that gall formation across this clade is likely to employ a diversity of molecular strategies. 

The morphology of insect-induced galls contributes to defences of the gall-inducing insect species against its natural enemies. In terms of gall chemistry, the only defensive compounds thus far identified in galls are tannins that accumulate in many galls, preventing damage by herbivores. Intrigued by the fruit-like appearance of the translucent oak gall (TOG; Amphibolips nubilipennis , Cynipidae, Hymenoptera) induced on red oak ( Quercus rubra ), we hypothesized that its chemical composition may deviate from other galls. We found that the pH of the gall is between 2 and 3, making it among the lowest pH levels found in plant tissues. We examined the organic acid content of TOG and compared it to fruits and other galls using high-performance liquid chromatography and gas chromatography–mass spectrometry. Malic acid, an acid with particularly high abundance in apples, represents 66% of the organic acid detected in TOGs. The concentration of malic acid was two times higher than in other galls and in apples. Gall histology showed that the acid-containing cells were enlarged and vacuolized just like fruits mesocarp cells. Accumulation of organic acid in gall tissues is convergent with fruit morphology and may constitute a new defensive strategy against predators and parasitoids. 

Ants disperse oak galls of some cynipid wasp species similarly to how they disperse seeds with elaiosomes. We conducted choice assays in field and laboratory settings with ant-dispersed seeds and wasp-induced galls found in ant nests and found that seed-dispersing ants retrieve these galls as they do myrmecochorous seeds. We also conducted manipulative experiments in which we removed the putative ant-attracting appendages (“kapéllos”) from galls and found that ants are specifically attracted to kapéllos. Finally, we compared the chemical composition and histology of ant-attracting appendages on seeds and galls and found that they both have similar fatty acid compositions as well as morphology. We also observed seed-dispersing ants retrieving oak galls to their nests and rodents and birds consuming oak galls that were not retrieved by ants. These results suggest convergence in ant-mediated dispersal between myrmecochorous seeds and oak galls. Based on our observations, a protective advantage for galls retrieved to ant nests seems a more likely benefit than dispersal distance, as has also been suggested for myrmecochorous seeds. These results require reconsideration of established ant-plant research assumptions, as ant-mediated seed and gall dispersal appear strongly convergent and galls may be far more abundant in eastern North American deciduous forests than myrmecochorous seeds.