Structure formation in butterfly scales: Interplay of genetic control, mechanical instabilities, and dynamic material properties

Butterfly scales contribute to a butterfly's vibrant coloration and play crucial roles in functions such as thermoregulation, water repellency, and aerodynamics. However, the underlying mechanisms that drive scale structure formation in vivo are not well understood. In this perspective, we propose that mechanical instabilities are central to the morphogenesis of scales and can lead to the observed wide variety of scale morphologies in adult butterflies. We specifically focus on the interplay between a growing soft compartment formed by the plasma membrane and an epicuticular envelope, the constraints imposed on this compartment by the actin cytoskeleton, and the spatio-temporally heterogeneous sclerotization of the cuticle precursors. We discuss hypotheses on how intracellular processes control the composition of the cuticle precursor secreted into soft compartments and how mechanical instabilities may lead to the morphological diversity of ridges, lamellae, and other scale structures. Putting forward a set of hypotheses about the fundamental mechanical processes that enable the secretion of non-living functional biological matter, we aim to inspire novel fabrication approaches in material science and engineering.