Developmental biomechanics and age polyethism in leaf-cutter ants

Abstract

Many social insects display age polyethism: young workers stay inside the nest, and only older workers forage. This behavioural transition is accompanied by genetic and physiological changes, but the mechanistic origin of it remains unclear. To investigate if the mechanical demands on the musculoskeletal system effectively prevent young workers from foraging, we studied the biomechanical development of the bite apparatus in Atta vollenweideri leaf-cutter ants. Fully matured foragers generated peak in vivo bite forces of around 100 mN, more than one order of magnitude in excess of those measured for freshly eclosed callows of the same size. This change in bite force was accompanied by a sixfold increase in the volume of the mandible closer muscle, and by a substantial increase of the flexural rigidity of the head capsule, driven by a significant increase in both average thickness and indentation modulus of the head capsule cuticle. Consequently, callows lack the muscle force capacity required for leaf-cutting, and their head capsule is so compliant that large muscle forces would be likely to cause damaging deformations. On the basis of these results, we speculate that continued biomechanical development post eclosion may be a key factor underlying age polyethism, wherever foraging is associated with substantial mechanical demands.

Large deformation diffeomorphic mapping of 3D shape variation reveals two distinct mandible and head capsule morphs in Atta vollenweideri leaf‐cutter worker ants

“…The three shape categories seemingly coincide with functional specialisation: the queen is the only reproductively active female; minims are rarely found outside the nest, but are by far the dominant size‐class inside the fungal gardens (Figure S3 ; Muratore et al., 2023 ; Wetterer, 1999 ; Wilson, 1980 ); medias of all sizes actively partake in foraging (Clark, 2006 ; Muratore et al., 2023 ; Rudolph & Loudon, 1986 ; note that task preference can further vary with size within the medias, e.g. Camargo et al., 2007 ; Püffel, Meyer, et al., 2023 ). Notably, we did not find strong evidence for a separate soldier morph in A. vollenweideri , and indeed have observed that even the largest workers sometimes partake in foraging (see Wetterer, 1995 for similar results on A. colombica ).…”

“…However, internal shape parameters may also vary with size. We characterised internal shape by extracting two metrics relevant to the mechanical demands induced by biting: the thickness of the cuticle of both head capsule and mandible, which influences cuticle deformation (Püffel, Meyer, et al., 2023 ); and the second moment of area of the mandible, which determines its rigidity in bending (see e.g. Kundanati et al., 2020 ).…”

Mechanical and elemental characterization of ant mandibles: consequences for bite mechanics

“…Several insect behaviours impose relevant mechanical demands on their exoskeleton, like flying, jumping, running, walking, biting and the associated muscle contractions. Such behaviours usually generate friction between body parts and the environment and even among body parts that can lead to cuticular wear, which could also happen with the frequent use of a structure like the mandibles to process hard materials [41][42][43][44][45]. Therefore, it is not surprising that substantial variation in cuticle material sclerotization levels is observed along the body of an insect [15,[46][47][48][49][50], besides the differences among the cuticular layers or the abundance of transition or alkaline earth metals.…”

Mandible elemental composition and mechanical properties from distinct castes of the leafcutter ant Atta laevigata (Attini; Formicidae)

“…[2]). This can be associated with morphological adaptations as muscle and mandible size and shape, leading to improved performance in their respective roles [2][3][4][5][6][7][8][9][10].…”

“…However, the executed tasks also depend on the age of the individuals, with young workers (callows) caring for nest duties and older ones for tasks outside the nest. This is related to the ontogeny of the bite apparatus (head capsule and muscles), as callows can generate less force with their mandibles than mature workers [ 7 ]. Task allocation, on the other hand, is also influenced by polymorphism, with the larger majors being more effective in defending against vertebrates and smaller workers in defending against foreign ants [ 14 , 19 , 20 ].…”