A biomechanical analysis of prognathous and orthognathous insect head capsules: evidence for a many‐to‐one mapping of form to function

Abstract

Insect head shapes are remarkably variable, but the influences of these changes on biomechanical performance are unclear. Among 'basal' winged insects, such as dragonflies, mayflies, earwigs and stoneflies, some of the most prominent anatomical changes are the general mouthpart orientation, eye size and the connection of the endoskeleton to the head. Here, we assess these variations as well as differing ridge and sclerite configurations using modern engineering methods including multibody dynamics modelling and finite element analysis in order to quantify and compare the influence of anatomical changes on strain in particular head regions and the whole head. We show that a range of peculiar structures such as the genal/subgenal, epistomal and circumocular areas are consistently highly loaded in all species, despite drastically differing morphologies in species with forward-projecting (prognathous) and downward-projecting (orthognathous) mouthparts. Sensitivity analyses show that the presence of eyes has a negligible influence on head capsule strain if a circumocular ridge is present. In contrast, the connection of the dorsal endoskeletal arms to the head capsule especially affects overall head loading in species with downward-projecting mouthparts. Analysis of the relative strains between species for each head region reveals that concerted changes in head substructures such as the subgenal area, the endoskeleton and the epistomal area lead to a consistent relative loading for the whole head capsule and vulnerable structures such as the eyes. It appears that biting-chewing loads are managed by a system of strengthening ridges on the head capsule irrespective of the general mouthpart and head orientation. Concerted changes in ridge and endoskeleton configuration might allow for more radical anatomical changes such as the general mouthpart orientation, which could be an explanation for the variability of this trait among insects. In an evolutionary context, many-to-one mapping of strain patterns onto a relatively similar overall head loading indeed could have fostered the dynamic diversification processes seen in insects.

The biology of seed discrimination and its role in shaping the foraging ecology of carabids: A review

“…The importance of body mass and bite force for the feeding ecology of insects remains poorly understood, nonetheless. Emerging evidence in this regard suggests that body mass and bite force underlie fundamental aspects of the feeding ecology of predatory insects as well (Weihmnann et al, 2015 ; Blanke et al, 2018 ). Recent studies, for instance, have shown that match between bite force and cuticular hardness of prey was the most powerful factor in predicting prey preferences when carabid species were offered different types of prey (Brousseau et al., 2018 ; Konuma & Chiba, 2007 ).…”

Mechanical demands of bite in plane head shapes of ant (Hymenoptera: Formicidae) workers

“…Further studies are required to investigate in more detail the role of Pheidole worker head shape in bite mechanical performance, especially considering the three-dimensional morphology of this structure. This way, relevant aspects of the head morphology can be addressed, such as the role of the endoskeleton (Blanke et al, 2018;Boudinot et al, 2021;Kubota et al, 2019;Richter et al, 2019Richter et al, , 2020Richter et al, , 2021 and cuticle thickness on stress distribution. In addition, the influence of cuticular sculpturing on the mechanical response to loading remains to be further tested (Buxton et al, 2021;Hellenbrand, 2022).…”

“…Among bilateral animals, the mechanical processing of food usually happens with the aid of head structures (Brusca & Brusca, 2003), in a way that the head morphological evolution can be strongly linked to food processing demands. Among insects, which show an incredible species diversity and evolved several modes of food consumption (Krenn, 2019), the biomechanics of food capture and processing seems to be a relevant evolutionary pressure for head and mouth appendices morphological variation (Blanke, Schmitz, et al, 2017;Blanke, Watson, et al, 2017;Blanke et al, 2018;Camargo et al, 2015Camargo et al, , 2016Hörnschemeyer et al, 2013;Weihmann et al, 2015). In some insect lineages, evolutionary pressures lead to the development of strong intraspecific morphological variation.…”

Morphometric Analysis of Coptotermes spp. Soldier Caste (Blattodea: Rhinotermitidae) in Indonesia and Evidence of Coptotermes gestroi Extreme Head-Capsule Shapes

“…Different levels of mandible curvature independently evolved in Coptotermes and were not correlated with the HC posterior lateral expansion. Lateral expansion of the HC posterior part may be associated with the wider attachment area of the craniomandibular muscle that will amplify bite force [106][107][108]. We assumed craniomandibular muscle development affects the postmentum elongation and HC widening during soldier differentiation in Coptotermes.…”