Hierarchical woven fibrillar structures in developing single gyroids in butterflies

Abstract

Nature offers a remarkable diversity of nanomaterials that have extraordinary functional and structural properties. Intrinsic to nature is the impressive ability to form complex ordered nanomaterials via self-organization. One particularly intriguing nanostructure is the gyroid, a network-like structure exhibiting high symmetry and complex topology. Although its existence in cells and tissues across many biological kingdoms is well documented, how and why it forms remains elusive and uncovering these formation mechanisms will undoubtedly inform bioinspired designs. A beautiful example is the smooth single gyroid that is found in the wing scales of several butterflies, where it behaves as a photonic crystal generating a vibrant green color. Here, we report that the gyroid structures of the Emerald-patched Cattleheart, Parides sesostris , develop as woven fibrillar structures, in contrast to the commonly held assumption that they form as smooth constructs. Ultramicroscopy of pupal tissue reveals that the gyroid geometry consists of helical weavings of fibers, akin to hyperbolic line patterns decorating the gyroid. Interestingly, despite their fibrillar nature, electron diffraction reveals the absence of crystalline order within this material. Similar fibrillar structures are also observed in the mature wing scales of P. sesostris specimens with surgically altered pupal development, leading to a blue coloration. Our findings not only introduce a variation of the gyroid in biology but also have significant implications for our understanding of its formation in nature.