Dynamics of F-actin prefigure the structure of butterfly wing scales

Abstract

The wings of butterflies and moths consist of dorsal and ventral epidermal surfaces that give rise to overlapping layers of scales and hairs (Lepidoptera, "scale wing"). Wing scales (average length ~200 µm) are homologous to insect bristles (macrochaetes), and their colors create the patterns that characterize lepidopteran wings. The topology and surface sculpture of wing scales vary widely, and this architectural complexity arises from variations in the developmental program of the individual scale cells of the wing epithelium. One of the more striking features of lepidopteran wing scales are the longitudinal ridges that run the length of the mature (dead) cell, gathering the cuticularized scale cell surface into pleats on the sides of each scale. While also present around the periphery of other insect bristles and hairs, longitudinal ridges in lepidopteran wing scales gain new significance for their creation of iridescent color through microribs and lamellae. Here we show the dynamics of the highly organized F-actin filaments during scale cell development, and present experimental manipulations of actin polymerization that reveal the essential role of this cytoskeletal component in wing scale elongation and the positioning of longitudinal ribs.

Butterfly gyroid nanostructures as a time-frozen glimpse of intracellular membrane development

“…The most direct evidence of the formation process would be provided by time-resolved in vivo imaging of the nanostructure growth during metamorphosis. However, real-space in vivo imaging, by its nature restricted to optical microscopy methods, is complicated by the complexity of the organisms and by surrounding optically thick and soft tissue ( 29 – 31 ). Further complications are the resolution [limited by the diffraction limit, unless super-resolution fluorescence microscopy is used ( 25 , 32 )], the need to image deep inside tissue, and limited contrast between biological agents and the aqueous environment, which requires biomarkers to enhance local contrast.…”

“…Further complications are the resolution [limited by the diffraction limit, unless super-resolution fluorescence microscopy is used ( 25 , 32 )], the need to image deep inside tissue, and limited contrast between biological agents and the aqueous environment, which requires biomarkers to enhance local contrast. The next most direct evidence is provided by rearing butterflies in a controlled fashion whereby the development is aborted at specific stages, followed by structural investigations of fixed tissue postmortem, either by confocal microscopy with biomarker-enhanced optical contrast ( 29 ) or transmission electron microscopy (TEM) ( 33 , 34 ). Over the past decades, Ghiradella ( 30 , 33 , 35 ) and others ( 12 , 36 ) have proposed a formation mechanism for chitinous nanostructures viz.…”

Exploring the molecular basis of monarch butterfly color pattern variation

“…However, this new clue points to cytoskeleton dynamics as a possible mechanism. Recently, Dinwiddie et al (2014) explored the development of the actin cytoskeleton in butterfly wing scales, showing how it determines scale size and shape. As part of their analysis, Dinwiddie et al (2014) inhibited actin polymerization during scale development with cytochalsin D, which yielded a variety of defects including misshapen and bent scales.…”

“…Recently, Dinwiddie et al (2014) explored the development of the actin cytoskeleton in butterfly wing scales, showing how it determines scale size and shape. As part of their analysis, Dinwiddie et al (2014) inhibited actin polymerization during scale development with cytochalsin D, which yielded a variety of defects including misshapen and bent scales. While Dinwiddie et al (2014) did not examine microtubules in butterfly scales, there is a well-characterized role of microtubules in shaping the development of the homologous structure in flies, the mechanosensory bristle (Bitan et al, 2010a).…”

“…As part of their analysis, Dinwiddie et al (2014) inhibited actin polymerization during scale development with cytochalsin D, which yielded a variety of defects including misshapen and bent scales. While Dinwiddie et al (2014) did not examine microtubules in butterfly scales, there is a well-characterized role of microtubules in shaping the development of the homologous structure in flies, the mechanosensory bristle (Bitan et al, 2010a). In the sensory bristle of Drosophila , stable, polarized microtubules, with the minus end distal to the cell, fill the shaft while dynamic, mixed-polarity microtubules exist at the tip (Bitan et al, 2012).…”