4.8 Article

Hierarchical morphogenesis of swallowtail butterfly wing scale nanostructures

Journal

ELIFE
Volume 12, Issue -, Pages -

Publisher

eLIFE SCIENCES PUBL LTD
DOI: 10.7554/eLife.89082

Keywords

butterfly scale; biological nanostructures; hierarchical morphogenesis; structural coloration; F-Actin reorganization; plasma membrane invagination; Other; Parides eurimedes; Parides arcas; Parides iphidamas; Papilio polytes; Papilio nireus; Papilio palinurus

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The study of color patterns in the animal integument is a fundamental question in biology. Lepidopteran species have been exemplary models in this field due to their relative simplicity and elegance. However, the formation of wing scale nanostructures in Lepidoptera is still not well understood. This study focuses on the developmental study of hierarchical scale nanostructures in Parides eurimedes and other papilionid species, revealing a previously undocumented role for F-actin in the morphogenesis of complex wing scale nanostructures, likely specific to the Papilionidae.
The study of color patterns in the animal integument is a fundamental question in biology, with many lepidopteran species being exemplary models in this endeavor due to their rela-tive simplicity and elegance. While significant advances have been made in unraveling the cellular and molecular basis of lepidopteran pigmentary coloration, the morphogenesis of wing scale nano-structures involved in structural color production is not well understood. Contemporary research on this topic largely focuses on a few nymphalid model taxa (e.g., Bicyclus, Heliconius), despite an over-whelming diversity in the hierarchical nanostructural organization of lepidopteran wing scales. Here, we present a time-resolved, comparative developmental study of hierarchical scale nanostructures in Parides eurimedes and five 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. Interestingly, while ridges are developing in P. eurimedes, plasma membrane manifests irregular mesh- like crossribs characteristic of Papilionidae, which delineate the accretion of cuticle into rows of planar disks in between ridges. Once the ridges have grown, disintegrating F- actin bundles appear to reorganize into a network that supports the invagination of plasma membrane underlying the disks, subsequently forming an extruded honeycomb lattice. Our results uncover a previously undocumented role for F- actin in the morphogenesis of complex wing scale nanostructures, likely specific to Papilionidae.

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