The inelastic deformability of the mineralized matrix in bones is critical to their high toughness, but the nanoscale mechanisms are incompletely understood. We track the fibrillar deformation of antler tissue during cyclic loading using in situ synchrotron small-angle X-ray diffraction (SAXD), finding that residual strain remains in the fibrils after the load was removed.

During repeated unloading/reloading cycles, the fibril strain shows minimal hysteresis when plotted as a function of tissue strain, indicating that permanent plastic strain accumulates inside the fibril. We model the tensile response of the mineralized collagen fibril by a two – level staggered model - including both elastic- and inelastic regimes - with debonding between mineral and collagen within fibrils triggering macroscopic inelasticity. In the model, the subsequent frictional sliding at intrafibrillar mineral/collagen interfaces accounts for subsequent inelastic deformation of the tissue in tension.

Our application of the model to antler bone (one of the toughest biomineralized tissues known) results in extremely good agreement of model predictions to experiment at the molecular, nanoscale and macroscopic levels. Based on the finding that intrafibrillar sliding between mineral and collagen leads to permanent plastic strain at both the fibril and the tissue level, we are extending this model to a wider range of other mineralized collagen tissue types