An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores

A general prediction of the specialist/generalist paradigm indicates that plant responses to insect herbivores may depend on the degree of ecological specialization of the insect attacker. However, results from a single greenhouse experiment evaluating the responses of the model plant Arabidopsis thaliana to three specialist (Plutella xylostella, Pieris rapae, and Brevicoryne brassicae) and three generalist (Trichoplusia ni, Spodoptera exigua, and Myzus persicae) insect species did not support the previous prediction. Using an ecological genomic approach, we assessed plant responses in terms of herbivore-induced changes in genome-wide gene expression, defense-related pathways, and concentrations of glucosinolates (i.e., secondary metabolites that are ubiquitously present in cruciferous plants). Our results showed that plant responses were not influenced by the degree of specialization of insect herbivores. In contrast, responses were more strongly shaped by insect taxa (i.e., aphid vs. lepidopteran species), likely due to their different feeding modes. Interestingly, similar patterns of plant responses were induced by the same insect herbivore species in terms of defense signaling (jasmonic acid pathway), aliphatic glucosinolate metabolism (at both the gene expression and phenotypic levels) and genome-wide responses. Furthermore, plant responses to insect herbivores belonging to the same taxon (i.e., four lepidopteran species) were not explained by herbivore specialization or phylogenetic history. Overall, this study suggests that different feeding modes of insect taxa as well as herbivore-specific plant responses, which may result from distinct ecological/evolutionary interactions between A. thaliana (or a close relative) and each of the lepidopteran species, may explain why observed responses deviate from those predicted by the specialist/generalist paradigm.