Wet shells and dry tales: the evolutionary ‘Just-So’ stories behind the structure–function of biominerals

Abstract

The ability of evolution to shape organic form involves the interactions of multiple systems of constraints, including fabrication, phylogeny and function. The tendency to place function above everything else has characterized some of the historical biological literature as a series of ‘Just-So’ stories that provided untested explanations for individual features of an organism. A similar tendency occurs in biomaterials research, where features for which a mechanical function can be postulated are treated as an adaptation. Moreover, functional adaptation of an entire structure is often discussed based on the local characterization of specimens kept in conditions that are far from those in which they evolved. In this work, environmental- and frequency-dependent mechanical characterization of the shells of two cephalopods, Nautilus pompilius and Argonauta argo , is used to demonstrate the importance of multi-scale environmentally controlled characterization of biogenic materials. We uncover two mechanistically independent strategies to achieve deformable, stiff, strong and tough highly mineralized structures. These results are then used to critique interpretations of adaptation in the literature. By integrating the hierarchical nature of biological structures and the environment in which they exist, biomaterials testing can be a powerful tool for generating functional hypotheses that should be informed by how these structures are fabricated and their evolutionary history.