F-actin Re-organization Mediates Hierarchical Morphogenesis of Swallowtail Butterfly Wing Scale Nanostructures

Abstract

AbstractThe development of color patterning in lepidopteran wings is of fundamental interest in evolution and developmental biology. While significant advances have recently been made in unravelling the cell and molecular basis of lepidopteran pigmentary coloration, the morphogenesis of wing scales, often involved in structural color production, is not well understood. Contemporary research focuses almost exclusively on a few nymphalid model taxa (e.g., Bicyclus, Heliconius), despite an overwhelming diversity across lepidopteran families in the hierarchical nanostructural organization of the scale. Here, we present a time-resolved, comparative developmental study of hierarchical wing scale nanostructure in Parides eurimedes and other papilionid species. Our results uphold the putative conserved role of F-actin bundles in acting as spacers between developing ridges as previously documented in several nymphalid species. While ridges are developing, the plasma membrane manifests irregular crossribs, characteristic of Papilionidae, which delineate the accretion of cuticle into rows of planar disks in between ridges. Once ridges have grown, Arp2/3 appears to re-organize disintegrating F-actin bundles into a reticulate network that supports the extrusion of the membrane underlying the disks into honeycomb-like tubular lattices of air pores in cuticle. Our results uncover a previously undocumented role for F-actin in the morphogenesis of wing scale nanostructures prominently found in Papilionidae. They are also relevant to current challenges in engineering of mesophases, since understanding the diversity and biological basis of hierarchical morphogenesis may offer facile, biomimetic solutions.