Mandibular mechanical properties and material composition in a generalist pest insect feeding on different host plants

Adaptations of insect mouthparts to host plants play a key role in species distribution and evolutionary trajectories. We investigated the larval mandibles of the generalist lepidopteran Spodoptera frugiperda, focusing on material composition and mechanical properties in response to different larval food resources. Nanoindentation revealed pronounced functional differentiation within each mandible: the cutting edge exhibited the highest hardness and stiffness values, while basal regions were softer and more flexible, indicating adaptive gradients that balance wear resistance with shock absorption. Confocal laser scanning microscopy revealed a strong relationship between autofluorescence-based sclerotization signals and the gradients in elastic modulus (E) and hardness (H). Elemental composition analyses identified potential cross-linking elements, with zinc (Zn) showing the highest correlations with mechanical properties. Host plant-dependent differences were found, i.e., larvae feeding on silica phytolith-containing host plants (Zea mays, Avena sativa, Oryza sativa) exhibited higher Zn contents, increased degrees of sclerotization, and elevated E and H values, resulting in reduced mandibular wear compared with larvae feeding on plants with weaker mechanical defenses (Amaranthus hybridus, Conyza bonariensis). This intraspecific variation underscores the importance of elemental incorporation and tanning in mediating adaptation to plant mechanical defenses. Variation in mouthpart properties may enhance feeding performance across host plants; however, because all tested individuals were assigned to the C-strain, the present study addresses host-associated variation within a single strain rather than divergence between strains.