Musculoskeletal modelling under an evolutionary perspective: deciphering the role of single muscle regions in closely related insects

Abstract

Insects show a remarkable diversity of muscle configurations, yet the factors leading to this functional diversity are poorly understood. Here, we use musculoskeletal modelling to understand the spatio-temporal activity of an insect muscle in several dragonfly species and to reveal potential mechanical factors leading to a particular muscle configuration. Bite characteristics potentially show systematic signal, but absolute bite force is not correlated with size. Muscle configuration and inverse dynamics show that the wider relative area of muscle attachment and the higher activity of subapical muscle groups are responsible for this high bite force. This wider attachment area is, however, not an evolutionary trend within dragonflies. Our inverse dynamic data, furthermore, show that maximum bite forces most probably do not reflect maximal muscle force production capability in all studied species. The thin head capsule and the attachment areas of muscles most probably limit the maximum force output of the mandibular muscles.

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

“…Due to the sparse literature record concerning insect bite forces (Wheater & Evans, ; Goyens et al ., ; Weihmann et al ., ; David et al ., ), it was, however, unclear whether insects from these different lineages but with comparable head sizes (and thus muscle volumes) really show larger bite forces. Indeed, the bite forces predicted in the present study are in line with earlier bite force measurements for other insects with comparable head widths and mandibular set‐ups (Wheater & Evans, ; Weihmann et al ., ; David et al ., ). Given the increase in bite force from mayflies to Neoptera, this implies that the morphological changes in the above‐mentioned structures allow a better distribution of the strain resulting from the larger bite forces.…”

“…By contrast to this variety, the four lineages show mandibles of the same principal construction. They are attached with two joints, one anterior and one posterior to the head, and moved primarily by a mandibular adductor attached to the head and a lineage‐dependent set of 1–4 smaller associated adductors attached to the endoskeleton (Figure ), which seem to have a negligible influence on bite forces (David et al ., ,).…”

Form–function relationships in dragonfly mandibles under an evolutionary perspective

“…In order to understand how bite force influences strain levels, we measured the bite force of five out of the 21 studied species (Sympetrum, Cordulegaster, Onychogomphus, Aeshna and Anax), covering a wide range of body size and taxonomy, that were available locally (collection permit 67.1-2.03.20-33/13-M (ZFMK)). Bite force measurements were performed using a bespoke set-up described in other studies [22,23]. Briefly, it consisted of a custom-built specimen fixation device and an adjustable piezoelectric mini-force sensor (SKB pinforce sensor Z18152X2A3sp and Z18152X2A7sp; Kistler, Winterthur, Switzerland).…”

Computational biomechanics changes our view on insect head evolution

“…Combinations of these morphological structures have been used previously to infer the relationships of basal winged insects [10][11][12]44], but this analysis now clearly establishes that they are in fact mechanically connected to each other. It appears that the evolution of a fixed axis of rotation of the mandible, as it is present in basal winged insects except mayflies, also selected for a strong subgenal and epistomal ridge and stronger endoskeletal arms, and coincided with the trend of a loss or reduction of the small tentoriomandibular muscles in winged insects [52]. Evidence from the present (table in electronic supplementary material, figure S2) and other studies [33,53] indicates that the small tentoriomandibular muscles contribute less than 3-6% of the force of the main adductor muscle (additionally with a suboptimal attachment geometry) in dragonflies and this is probably also the case for other winged insects where lineage-dependent (electronic supplementary material, table S1) remnants of these muscles exist with a similar geometrical configuration as in dragonflies [52].…”

“…It appears that the evolution of a fixed axis of rotation of the mandible, as it is present in basal winged insects except mayflies, also selected for a strong subgenal and epistomal ridge and stronger endoskeletal arms, and coincided with the trend of a loss or reduction of the small tentoriomandibular muscles in winged insects [52]. Evidence from the present (table in electronic supplementary material, figure S2) and other studies [33,53] indicates that the small tentoriomandibular muscles contribute less than 3-6% of the force of the main adductor muscle (additionally with a suboptimal attachment geometry) in dragonflies and this is probably also the case for other winged insects where lineage-dependent (electronic supplementary material, table S1) remnants of these muscles exist with a similar geometrical configuration as in dragonflies [52]. Apparently, the large mandibular adductor muscle M. craniomanibularis internus provides the main force proportion which is in agreement with the large head volume this muscle occupies in those insects which use their mandibles for feeding [54,55], securing mating rights [56,57] or other functions where high or quickly released bite forces are advantageous.…”