Evidence for Cascading Host-Associated Differentiation in Insect Gall Trophic Networks

The generation and maintenance of biodiversity are strongly influenced by adaptations to symbiotic interactions. In antagonistic host-parasite systems, such as phytophagous insects on plants, the prevalence of host-associated differentiation (HAD) may be underestimated as a key driver in parasite diversification. Even less well understood is how HAD may cascade up the food chain to influence diversification in higher trophic levels. Gall-inducing insects, which exhibit strong plant host specialisation, create microhabitats that support diverse associated communities that include predators, parasitoids and inquilines. In this study, we investigate whether HAD in gall-inducing Aciurina flies extends to their associates, resulting in a pattern of cascading HAD. We analysed genomic and ecological data across parasitoid species from three functional guilds, testing for host-driven divergence. Our results reveal that cascading HAD in Aciurina galling systems occurs in endoparasitoids, with no evidence for it in generalist ectoparasitoids and inquilines, underscoring that different types of interactions have different impacts on diversification. Additionally, evidence for host-specific cryptic species within the dominant endoparasitoid allowed us to formally describe Eurytoma trixa, Eurytoma ericameria and Eurytoma luminaria as new species. These findings provide strong evidence of multiple cascading HAD events within a galling insect community and highlight the compounding influence of gall inducers, as ecosystem engineers, on biodiversity.