The phylogeny of gall wasps (Cynipidae) and their parasitic relatives has attracted considerable attention in recent years. The family is now widely recognized to fall into twelve natural lineages, designated tribes, but the relationships among them have remained elusive. This has stymied any progress in understanding how cynipid gall inducers evolved from insect parasitoids, and what role inquilines (species that develop inside the galls of other species) might have played in this transition. A recent analysis of ultraconserved elements (UCEs) represents the first attempt at resolving these questions using phylogenomics. Here, we present the first analysis of gall-wasp relationships based on protein-coding sequences from genome and transcriptome assemblies. To address potential problems due to model misfit, we focus on models that accommodate site-specific amino-acid profiles and that are less sensitive to long-branch attraction than standard models. Our results show that the Cynipidae as previously circumscribed are not monophyletic. Specifically, the Paraulacini and a clade formed by Diplolepidini + Pediaspidini both fall outside of a core clade (Cynipidae sensu stricto), which is more closely related to Figitidae. This result is robust to the exclusion of long-branch taxa that could potentially mislead the analysis, and it is consistent with the previous UCE analysis. Given this, we propose that the Cynipidae be divided into three families: the Paraulacidae, Diplolepididae and Cynipidae (s. str.). Our results suggest that the Eschatocerini are the sister group of the remaining Cynipidae (s. str.). Within Cynipidae s. str., our results are consistent with the UCE analysis but place two additional tribes: (1) the Aylacini (s.str.), which are more closely related to the oak gall wasps (Cynipini) and some of their inquilines (Ceroptresini) than to the other herb gallers (Aulacideini and Phanacidini); and (2) the Qwaqwaiini, which are likely the sister group to Synergini (s. str.) + Rhoophilini. Many alternative scenarios for the evolution of cynipid life histories are compatible with the relationships suggested by our analysis, but all of them display an astonishing level of complexity with multiple shifts between parasitoids, inquilines and gall inducers. Linking the different types of life-history transitions to specific genomic signatures may be one of the best ways of differentiating among these alternative scenarios. Our study represents the first step towards enabling such analyses.

Helsinki, Finland, July 17-22, 2022