Department of Integrative Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
Marine Biological Laboratory, Woods Hole, MA 02543, USA.
J Exp Biol. 2021 May 15;224(10). doi: 10.1242/jeb.237917. Epub 2021 May 28.
The 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.
蝴蝶和蛾类（鳞翅目）的翅膀通常覆盖着数千片扁平、重叠的鳞片，这些鳞片赋予了翅膀丰富多彩的图案。然而，许多鳞翅目物种已经进化出高度透明的翅膀，这些翅膀通常具有形态改变和尺寸减小的鳞片，以及显著减少反射的膜表面纳米结构。已经对几种“透明翅”鳞翅目昆虫的光学特性和抗反射纳米结构进行了表征，但翅膀透明度的发育过程尚不清楚。在这里，我们应用共聚焦和电子显微镜技术，在玻璃翅蝶 Greta oto 中创建了一个发育时间序列，比较透明和不透明的翅膀区域。我们发现，在早期翅膀发育过程中，透明区域的鳞片前体细胞密度降低，并且在鳞片生长过程中的细胞骨架组织在透明区域内的薄、刚毛状鳞片形态和不透明区域内的扁平、圆形鳞片形态之间存在差异。我们还表明，翅膀膜表面上的纳米结构由两层组成：一层是规则排列的乳突状纳米结构的下层，另一层是由主要由长链正烷烃组成的不规则排列的蜡基纳米柱的上层。通过化学去除蜡基纳米柱，以及光学光谱和分析模拟，我们证明了它们在产生抗反射特性方面的作用。这些发现为自然组织的微观结构和纳米结构的形态发生和组成提供了深入的了解，并可能为新的抗反射材料提供生物启示。
