Neutral and non-neutral factors shape an emergent plant–antagonist interaction

Discerning the mechanisms responsible for emergent evolutionary radiations, community assembly, and the maintenance of diversity is necessary for understanding the evolutionary ecology of species interactions in changing landscapes. These processes can be driven by stochastic (neutral) factors, such as genetic drift, or deterministic (non-neutral) factors, such as the external environment and heritable phenotypic variation. Neutral and non-neutral factors can shape species interactions, but the relative influence of these different processes on antagonistic relationships is not well understood. We leveraged the recent discovery of a novel herbivore (Caloptilia triadicae) on invasive Chinese tallow (Triadica sebifera) to investigate the nature and relative importance of different factors influencing plant–antagonist interactions. We assessed measures of host attributes, herbivore demography and herbivory across the North American range of Triadica according to geography, environmental variation, and host genetic variation. We found that leaf toughness corresponded to genetic variation in Triadica, longitude, and mean temperature. Genetic variation in Triadica was the strongest predictor of herbivore abundance, especially for the early leaf mining stages, though herbivore abundance also corresponded to longitude. Model variables did not explain leaf damage, which was driven by interactions with late-stage larvae. Trends in herbivore demography were not consistent with previously reported geographic patterns of Triadica genetic variation related to tannin defense, but were consistent with patterns revealed by other studies of Triadica phenolic compounds and C:N, as well as low sensitivity of endophagous herbivores to tannins in the absence of parasitoids. Our findings suggest that even simple geographic mosaics of genetic and environmental variation, as well as distance-dependent dispersal, can influence the establishment and trajectory of novel species interactions.