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Developmental, cellular and biochemical basis of transparency in clearwing butterflies

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...

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Autores principales: Pomerantz, Aaron F., Siddique, Radwanul H., Cash, Elizabeth I., Kishi, Yuriko, Pinna, Charline, Hammar, Kasia, Gomez, Doris, Elias, Marianne, Patel, Nipam H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8340268/
https://www.ncbi.nlm.nih.gov/pubmed/34047337
http://dx.doi.org/10.1242/jeb.237917
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author Pomerantz, Aaron F.
Siddique, Radwanul H.
Cash, Elizabeth I.
Kishi, Yuriko
Pinna, Charline
Hammar, Kasia
Gomez, Doris
Elias, Marianne
Patel, Nipam H.
author_facet Pomerantz, Aaron F.
Siddique, Radwanul H.
Cash, Elizabeth I.
Kishi, Yuriko
Pinna, Charline
Hammar, Kasia
Gomez, Doris
Elias, Marianne
Patel, Nipam H.
author_sort Pomerantz, Aaron F.
collection PubMed
description 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.
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spelling pubmed-83402682021-08-12 Developmental, cellular and biochemical basis of transparency in clearwing butterflies Pomerantz, Aaron F. Siddique, Radwanul H. Cash, Elizabeth I. Kishi, Yuriko Pinna, Charline Hammar, Kasia Gomez, Doris Elias, Marianne Patel, Nipam H. J Exp Biol Research Article 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. The Company of Biologists Ltd 2021-05-28 /pmc/articles/PMC8340268/ /pubmed/34047337 http://dx.doi.org/10.1242/jeb.237917 Text en © 2021. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Pomerantz, Aaron F.
Siddique, Radwanul H.
Cash, Elizabeth I.
Kishi, Yuriko
Pinna, Charline
Hammar, Kasia
Gomez, Doris
Elias, Marianne
Patel, Nipam H.
Developmental, cellular and biochemical basis of transparency in clearwing butterflies
title Developmental, cellular and biochemical basis of transparency in clearwing butterflies
title_full Developmental, cellular and biochemical basis of transparency in clearwing butterflies
title_fullStr Developmental, cellular and biochemical basis of transparency in clearwing butterflies
title_full_unstemmed Developmental, cellular and biochemical basis of transparency in clearwing butterflies
title_short Developmental, cellular and biochemical basis of transparency in clearwing butterflies
title_sort developmental, cellular and biochemical basis of transparency in clearwing butterflies
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8340268/
https://www.ncbi.nlm.nih.gov/pubmed/34047337
http://dx.doi.org/10.1242/jeb.237917
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