Comprehensive phylogenomic analyses re-write the evolution of parasitism within cynipoid wasps

Background Parasitoidism, a specialized life strategy in which a parasite
eventually kills its host, is frequently found within the insect order
Hymenoptera (wasps, ants and bees). A parasitoid lifestyle is one of two
dominant life strategies within the hymenopteran superfamily Cynipoidea,
with the other being an unusual plant-feeding behavior known as galling.
Less commonly cynipoid wasps exhibit inquilinism, a strategy where some
species have adapted to usurp other species’ galls instead of inducing
their own. Using a phylogenomic data set of ultraconserved elements from
nearly all lineages of Cynipoidea, we here generate a robust phylogenetic
framework and timescale to understand cynipoid systematics and the
evolution of these life histories. Results Our reconstructed evolutionary
history for Cynipoidea differs considerably from previous hypotheses.
Rooting our analyses with non-cynipoid outgroups, the Paralaucini, a group
of inquilines, emerged as sister-group to the rest of Cynipoidea,
rendering the gall wasp family Cynipidae paraphyletic. The families
Ibaliidae and Liopteridae, long considered archaic and early-branching
parasitoid lineages, were found nested well within the Cynipoidea as
sister-group to the parasitoid Figitidae. Cynipoidea originated in the
early Jurassic around 190 Ma. Either inquilinism or parasitoidism is
suggested as the ancestral and dominant strategy throughout the early
evolution of cynipoids, depending on whether a simple (three states:
parasitoidism, inquilinism and galling) or more complex (seven states:
parasitoidism, inquilinism and galling split by host use) model is
employed. Conclusions Our study has significant impact on understanding
cynipoid evolution and highlights the importance of adequate outgroup
sampling. We discuss the evolutionary timescale of the superfamily in
relation to their insect hosts and host plants, and outline how
phytophagous galling behavior may have evolved from entomophagous,
parasitoid cynipoids. We hypothesize these seemingly diverging life
strategies may be considered as specializations of a similar underlying
molecular toolkit between which switches are possible. Our study has
established the framework for further physiological and comparative
genomic work between gall-making, inquiline and parasitoid lineages, which
could also have significant implications for the evolution of diverse life
histories in other Hymenoptera.