Butterflies form functional cuticles by assembling chitinous micro- and nanostructures. The intricate architectures in butterfly scales are made by individual cells during metamorphosis, but the biomechanical processes that enable structure formation still need to be better understood. During the development of butterfly wing scales, ordered periodic cell membrane undulations occur at the upper surface of scale-forming cells, priming the formation of ridges. Ridges are critical for wing scale functionality, including structural color, wetting characteristics, and thermal performance.
The HFSP Research Grant Team, led by Mathias Kolle, from MIT, USA, used in vivo phase microscopy data from developing butterflies to inform an analytical model based on Föppl-von-Kármán plate theory (Fig. 1a, b). The scientists describe the early-stage scale cell membrane undulations preceding ridge formation as the buckling of a thin, growing sheet, subject to spatial constraints, pressure, and the sheet's growth strain and bending stiffness. Specifically, by combining this morphoelastic model with in vivo imaging, researchers revealed that buckling is the key biomechanical process that governs early-stage ridge formation in Painted Lady butterflies.
a) Cell plasma membrane where cuticle precursor secretion takes place is modeled as a growing membrane confined by actin cytoskeleton.
b) Height maps and surface profiles (yellow, orange, violet) of the growing cell membrane and the undulations that it forms at the early stages of ridge formation.
c) Comparison between in vivo imaging data (black-average profile, gray-standard deviation) and model predictions (colored dashed lines) for ~ 40%, 40.5%, and 41% of pupal development.
e) Transmission electron microscopy cross-section of developing scale of Colias eurytheme showing ridges form at the top surface but not at the bottom lamina; adapted with permission from Ghiradella, J. Morphol. 142, 395–409 (1974), copyright 1974, John Wiley & Sons.
f) Confocal fluorescence image of the upper surface of a silver wing scale on Agraulis vanilla; adapted with permission from Dinwiddie, Dev. Biol. 392, 404–418 (2014), copyright 2014, Elsevier.
The model helps explain why ridges form on the upper surface of wing scales, while the bottom surface remains flat. It also explains why, in some species, ridges only form in every other space between actin filaments, rather than between each pair of filaments (Fig. 1e, f). The model also shows that ridges only appear after a critical amount of strain is reached, which depends on the spacing of the actin filaments, revealing a general rule for how these structures develop.
The HFSP awardees' findings support the long-standing but unproven idea that mechanical buckling helps ridges form. They also suggest specific conditions that determine whether ridges will form or not. This approach, which links experimental data with modeling, lays the groundwork for understanding how butterfly wings develop their structures and can also provide insights into biological and synthetic material design.