Fossilized Biophotonic Nanostructures Reveal the Original Colors of 47-Million-Year-Old Moths
Maria E. McNamara1,2*, Derek E. G. Briggs1,3, Patrick J. Orr2, Sonja Wedmann4, Heeso Noh5, Hui Cao5
1 Department of Geology & Geophysics, Yale University, New Haven, Connecticut, United States of America, 2 UCD School of Geological Sciences, University College Dublin, Belfield, Dublin, Ireland, 3 Yale Peabody Museum of Natural History, Yale University, New Haven, Connecticut, United States of America, 4Senckenberg Forschungsinstitut und Naturmuseum, Forschungsstation Grube Messel, Messel, Germany, 5Department of Applied Physics, Yale University, New Haven, Connecticut, United States of America
Abstract
Structural colors are generated by scattering of light by variations in tissue nanostructure. They are widespread among animals and have been studied most extensively in butterflies and moths (Lepidoptera), which exhibit the widest diversity of photonic nanostructures, resultant colors, and visual effects of any extant organism. The evolution of structural coloration in lepidopterans, however, is poorly understood. Existing hypotheses based on phylogenetic and/or structural data are controversial and do not incorporate data from fossils. Here we report the first example of structurally colored scales in fossil lepidopterans; specimens are from the 47-million-year-old Messel oil shale (Germany). The preserved colors are generated by a multilayer reflector comprised of a stack of perforated laminae in the scale lumen; differently colored scales differ in their ultrastructure. The original colors were altered during fossilization but are reconstructed based upon preserved ultrastructural detail. The dorsal surface of the forewings was a yellow-green color that probably served as a dual-purpose defensive signal, i.e. aposematic during feeding and cryptic at rest. This visual signal was enhanced by suppression of iridescence (change in hue with viewing angle) achieved via two separate optical mechanisms: extensive perforation, and concave distortion, of the multilayer reflector. The fossils provide the first evidence, to our knowledge, for the function of structural color in fossils and demonstrate the feasibility of reconstructing color in non-metallic lepidopteran fossils. Plastic scale developmental processes and complex optical mechanisms for interspecific signaling had clearly evolved in lepidopterans by the mid-Eocene.
Author Summary
Biological structural colors are generated when light is scattered by nanostructures in tissues. Such colors have diverse functions for communication both among and between species. Structural colors are most complex in extant butterflies and moths (lepidopterans), but the evolution of such colors and their functions in this group of organisms is poorly understood. Fossils can provide insights into the evolution of biological structures, but evidence of structurally colored tissues was hitherto unknown in fossil lepidopterans. Here, we report the preservation of structurally colored scales in fossil moths with striking metallic hues from the ~47-million-year-old (Eocene) GrubeMessel oil shales (Germany). We identify the color-producing nanostructure in the scales and show that the original colors were altered during fossilization. Preserved details in the scales allow us to reconstruct the original colors and show that the dorsal surface of the forewings was yellow-green. The optical properties of the scales strongly indicate that the color functioned as a warning signal during feeding but was cryptic when the moths were at rest. Our results confirm that structural colors can be reconstructed even in non-metallic lepidopteran fossils and show that defensive structural coloration had evolved in insects by the mid-Eocene.
Citation: McNamara ME, Briggs DEG, Orr PJ, Wedmann S, Noh H, et al. (2011) Fossilized Biophotonic Nanostructures Reveal the Original Colors of 47-Million-Year-Old Moths. PLoS Biol 9(11): e1001200. doi:10.1371/journal.pbio.1001200
Academic Editor: Michael J. Benton, University of Bristol, United Kingdom
Received: May 5, 2011; Accepted: October 13, 2011; Published: November 15, 2011
Copyright: © 2011 McNamara et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The research was funded by an IRCSET-Marie Curie International Mobility Fellowship (www.ircset.ie, http://ec.europa.eu/research/mariecurieactions) awarded to MEM and by NSF (www.nsf.gov) to HC (PHY-0957680). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: maria.mcnamara@yale.edu
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