Abstract
ABSTRACTThe wings of butterflies and moths (Lepidoptera) are typically covered with thousands of flat, overlapping scales that endow the wings with colorful patterns. Yet, numerous species of Lepidoptera have evolved highly transparent wings, which often possess scales of altered morphology and reduced size, and the presence of membrane surface nanostructures that dramatically reduce reflection. Optical properties and anti-reflective nanostructures have been characterized for several ‘clearwing’ Lepidoptera, but the developmental processes underlying wing transparency are unknown. Here, we applied confocal and electron microscopy to create a developmental time series in the glasswing butterfly, Greta oto, comparing transparent and non-transparent wing regions. We found that during early wing development, scale precursor cell density was reduced in transparent regions, and cytoskeletal organization during scale growth differed between thin, bristle-like scale morphologies within transparent regions and flat, round scale morphologies within opaque regions. We also show that nanostructures on the wing membrane surface are composed of two layers: a lower layer of regularly arranged nipple-like nanostructures, and an upper layer of irregularly arranged wax-based nanopillars composed predominantly of long-chain n-alkanes. By chemically removing wax-based nanopillars, along with optical spectroscopy and analytical simulations, we demonstrate their role in generating anti-reflective properties. These findings provide insight into morphogenesis and composition of naturally organized microstructures and nanostructures, and may provide bioinspiration for new anti-reflective materials.
Highlights
The wings of butterflies and moths (Lepidoptera) have inspired studies across a variety of scientific fields, including evolutionary biology, ecology and biophysics (Beldade and Brakefield, 2002; Prum et al, 2006; Gilbert and Singer, 1975)
Lepidopteran wings are generally covered with rows of flat, partially overlapping scales that endow the wings with colorful patterns
Using chemical treatments, scanning electron microscopy and gas chromatography–mass spectrometry, we found that nanostructures on the wing membrane surface are composed of two layers: a lower layer of chitin-based nipple-like nanostructures, and an upper layer of wax-based nanopillars composed predominantly of long-chain nalkanes
Summary
The wings of butterflies and moths (Lepidoptera) have inspired studies across a variety of scientific fields, including evolutionary biology, ecology and biophysics (Beldade and Brakefield, 2002; Prum et al, 2006; Gilbert and Singer, 1975). In contrast to typical colorful wings, numerous species of butterflies and moths possess transparent wings that allow light to pass through, so that objects behind them can be distinctly seen (Fig. 1A–H) (Goodwyn et al, 2009; Yoshida et al, 1997; Siddique et al, 2015). This trait has been interpreted as an adaptation in the context of camouflage, in which some lineages evolved transparent wings as crypsis to reduce predation (Arias et al, 2019; 2020; Mcclure et al, 2019). Transparency is rare and more challenging to achieve on land, primarily owing to the large difference between the refractive indices of terrestrial organism’s tissue (n=∼1.3–1.5) and air (n=1), which results in significant surface reflection (Yoshida et al, 1997; Johnsen, 2014; Bagge, 2019)
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