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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 of foraging effectively prevent young workers from partaking, we studied the biomechanical development of the bite apparatus in Atta vollenweideri leaf-cutter ants. Fully-matured foragers generate 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 may 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 mechanical demands on the musculoskeletal system.

Model derivations, plausibility of model assumptions and bite force measurement

The SI contains descriptions of the tomographic scanning procedure, image segmentation and morphometric analysis. In addition, the custom-written fibre-tracking algorithm is presented in detail, including the fibre identification and growing process, and a detailed error analysis (see Fig. 1). The results of the ordinary least square and standardised major axis regressions are shown in Tables 1 and 2, respectively. Further details are provided on the effects of filament-attachment in muscle fibres, the area coverage and safety factor of the apodeme, and the geometric model of the head capsule.