Structure-function relationships in mole crickets: Patterns of transition metal allocation among cuticular tools support the metal-prioritization hypothesis.

Abstract

Transition metals are well known to enrich the cuticle of structural tools among many insect lineages through the formation of metal-ligand coordinated bonds. Investigations that focus on the distribution patterns of metals among different structures, however, are lacking, despite some structural tools hosting different transition metal profiles. Here, we hypothesized that the enrichment of structures with transition metals, including specific metals and their abundances, is contingent on the types of physical forces those structures experience. We used scanning electron microscopy with energy dispersive X-ray spectroscopy, nanoindentation, and confocal laser scanning microscopy to study the material and mechanical properties of the dactyls of fossorial forelegs, mandibles, and proventriculus of two species of mole crickets. We found that our hypothesis was not supported, i.e., the same structures of each species, though performing similar functions, did not have a similar elemental composition. However, we did find a pattern in metal allocation that prioritizes the cuticle enrichment of structures that are arguably the most important to fitness, which we term "the metal-prioritization hypothesis." According to our proposed mechanism, zinc is ranked as the best transition metal for insect cuticle due to its ability to form stable redox-inactive complexes with histidine, followed by copper, manganese, then iron is last. The life history traits of the mole crickets, including differences in their tunneling and feeding behaviors, provide support for the metal-prioritization hypothesis. We suggest future studies consider this hypothesis when assessing metal diversity in insect cuticle. STATEMENT OF SIGNIFICANCE: Insect cuticle has the ability to change its mechanical properties, particularly its hardness and elastic modulus, through the incorporation of transition metals. Here, we studied the elemental composition (SEM-EDS), extent of sclerotization (confocal microscopy), and hardness and elastic modulus (nanoindentation) of three structures of two mole cricket species, the dactyls of their fossorial forelegs, mandibles, and proventriculus. Our hypothesis that the elemental profiles of structures relate to the different physical forces they experience was not supported. However, our findings did reveal a different pattern of metal allocation that we term the "metal-prioritization hypothesis." This hypothesis proposes that patterns of metal allocation are strongly dependent on their chemical properties and ability to form bonds with insect cuticle.