Plant genotypes affect aboveground and belowground herbivore interactions by changing chemical defense

Spatially separated aboveground (AG) and belowground (BG) herbivores are closely linked through shared host plants, and both patterns of AG-BG interactions and plant responses may vary among plant genotypes. We subjected invasive (USA) and native (China) genotypes of tallow tree (Triadica sebifera) to herbivory by the AG specialist leaf-rolling weevil Heterapoderopsis bicallosicollis and/or the root-feeding larvae of flea beetle Bikasha collaris. We measured leaf damage and leaves rolled by weevils, quantified beetle survival, and analyzed flavonoid and tannin concentrations in leaves and roots. AG and BG herbivores formed negative feedbacks on both native and invasive genotypes. Leaf damage by weevils and the number of beetle larvae emerging as adults were higher on invasive genotypes. Beetles reduced weevil damage and weevils reduced beetle larval emergence more strongly for invasive genotypes. Invasive genotypes had lower leaf and root tannins than native genotypes. BG beetles decreased leaf tannins of native genotypes but increased root tannins of invasive genotypes. AG herbivory increased root flavonoids of invasive genotypes while BG herbivory decreased leaf flavonoids. Invasive genotypes had lower AG and BG herbivore resistance, and negative AG-BG herbivore feedbacks were much stronger for invasive genotypes. Lower tannin concentrations explained overall better AG and BG herbivore performances on invasive genotypes. However, changes in tannins and flavonoids affected AG and BG herbivores differently. These results suggest that divergent selection on chemical production in invasive plants may be critical in regulating herbivore performances and novel AG and BG herbivore communities in new environments.