A review of the diversity and evolution of photonic structures in butterflies, incorporating the work of John Huxley (The Natural History Museum, London from 1961 to 1990)

The photonic structures of butterfly wings are among the most anatomically diverse of all those in nature, giving rise to an unrivalled display of structural colours. These have recently become the focus of research by workers in a variety of disciplines, stimulated by their potential applications to technology (‘biomimetics’). This interest, together with the discovery of unpublished electron micrographs taken by the late Dr John Huxley (Natural History Museum, London), prompted this review of butterfly photonics in general. The current work provides a synopsis of the literature to date, covering the diversity and evolution of these optical structures and incorporating Huxley's work, which represents an important biomimetic and evolutionary database on its own. This review deals with butterfly photonic devices according to the parts of the butterfly scales on which they occur. In this way, the information is ripe for evolutionary study.

[1]  C. W. Mason,et al.  Structural Colors in Feathers. II , 1922 .

[2]  F. Süffert Morphologie und optik der schmetterlingsschuppen, insbesondere die schillerfarben der schmetterlinge , 1924, Zeitschrift für Morphologie und Ökologie der Tiere.

[3]  Rodolfo H. Torres,et al.  Two-dimensional Fourier analysis of the spongy medullary keratin of structurally coloured feather barbs , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  J. Huxley,et al.  The basis of structural colour variation in two species of Papilio , 2009 .

[5]  A. Parker,et al.  Aphrodite's iridescence , 2001 .

[6]  L. Biró,et al.  Microstructures and nanostructures of high Andean Penaincisalia lycaenid butterfly scales (Lepidoptera: Lycaenidae): descriptions and interpretations , 2005 .

[7]  Jean-Pol Vigneron,et al.  Structural origin of the colored reflections from the black-billed magpie feathers. , 2006 .

[8]  D. Stavenga,et al.  An ultraviolet absorbing pigment causes a narrow-band violet receptor and a single-peaked green receptor in the eye of the butterfly Papilio , 1999, Vision Research.

[9]  Leon Poladian,et al.  Exaggeration and suppression of iridescence: the evolution of two-dimensional butterfly structural colours , 2006, Journal of The Royal Society Interface.

[10]  J. Huxley,et al.  The coloration of Papilio zalmoxis and P. antimachus, and the discovery of Tyndall blue in butterflies , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[11]  A. Parker Discovery of functional iridescence and its coevolution with eyes in the phylogeny of Ostracoda (Crustacea) , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  J. Nicol,et al.  Studies on reflexion of light from silvery surfaces of fishes, with special reference to the bleak, Alburnus alburnus , 1965, Journal of the Marine Biological Association of the United Kingdom.

[13]  K. Gentil Elektronenmikroskopische Untersuchung des Feinbaues Schillernder Leisten von Morpho-Schuppen , 1942, Zeitschrift für Morphologie und Ökologie der Tiere.

[14]  Serge Berthier,et al.  Thermoregulation and spectral selectivity of the tropical butterfly Prepona meander: a remarkable example of temperature auto-regulation , 2005 .

[15]  D. Stavenga,et al.  Random array of colour filters in the eyes of butterflies , 1997, The Journal of experimental biology.

[16]  Rodolfo H. Torres,et al.  Anatomically diverse butterfly scales all produce structural colours by coherent scattering , 2006, Journal of Experimental Biology.

[17]  H. Ghiradella,et al.  Structure and Development of Iridescent Lepidopteran Scales: the Papilionidae as a Showcase Family , 1985 .

[18]  The cause of colouration in the ctenophore Beroë cucumis , 2005, Current Biology.

[19]  Shuichi Kinoshita,et al.  Polarization-sensitive color mixing in the wing of the Madagascan sunset moth. , 2007, Optics express.

[20]  Serge Berthier,et al.  Iridescences: The Physical Colors of Insects , 2006 .

[21]  Krisztián Kertész,et al.  Gleaming and dull surface textures from photonic-crystal-type nanostructures in the butterfly Cyanophrys remus. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  F. Schlote,et al.  Die Entwicklung der Schmetterlingsschuppe bei Ephestia kühniella Zeller , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[23]  J. R. Sambles,et al.  Structural colour: Colour mixing in wing scales of a butterfly , 2000, Nature.

[24]  R. B. Morris,et al.  Iridescence from diffraction structures in the wing scales of Callophrys rubi, the Green Hairstreak , 2009 .

[25]  L. Biró,et al.  Modifications to Wing Scale Microstructures in Lycaenid Butterflies , 2004 .

[26]  R. Wootton,et al.  Limited-view iridescence in the butterfly Ancyluris meliboeus , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  Serge Berthier,et al.  Determination of the cuticle index of the scales of the iridescent butterfly Morpho menelaus , 2003 .

[28]  Shuichi Kinoshita,et al.  Single-scale spectroscopy of structurally colored butterflies: measurements of quantified reflectance and transmittance. , 2006, Journal of the Optical Society of America. A, Optics, image science, and vision.

[29]  H. Ghiradella,et al.  Structure of butterfly scales: Patterning in an insect cuticle , 1994, Microscopy research and technique.

[30]  Virginie Lousse,et al.  Optical properties of the iridescent organ of the comb-jellyfish Beroë cucumis (Ctenophora). , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  D R McKenzie,et al.  Photonic engineering. Aphrodite's iridescence. , 2001, Nature.

[32]  J. Nicol,et al.  A survey of reflectivity in silvery teleosts , 1966, Journal of the Marine Biological Association of the United Kingdom.

[33]  Masha Etkin Greenstein The ultrastructure of developing wings in the giant silkmoth, Hyalophora cecropia. I. Generalized epidermal cells , 1972, Journal of morphology.

[34]  Peter Vukusic,et al.  Grazing-incidence iridescence from a butterfly wing. , 2002, Applied optics.

[35]  Francis Arthur Jenkins,et al.  Fundamentals of Optics , 1976 .

[36]  H. Onslow,et al.  On a Periodic Structure in Many Insect Scales, and the Cause of Their Iridescent Colours , 1923 .

[37]  Jean-Pol Vigneron,et al.  Photonic crystal type structures of biological origin: Structural and spectral characterization , 2006 .

[38]  S. Kinoshita,et al.  Mechanisms of structural colour in the Morpho butterfly: cooperation of regularity and irregularity in an iridescent scale , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[39]  J. Gardner,et al.  Sem comparison of morpho butterfly dorsal and ventral scales , 1995, Microscopy research and technique.

[40]  S Enoch,et al.  Morpho butterflies wings color modeled with lamellar grating theory. , 2001, Optics express.

[41]  R. Wootton,et al.  Quantified interference and diffraction in single Morpho butterfly scales , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[42]  T Eisner,et al.  Ultraviolet Reflection of a Male Butterfly: Interference Color Caused by Thin-Layer Elaboration of Wing Scales , 1972, Science.

[43]  W. Lippert,et al.  Über lamellare feinstrukturen bei den schillerschuppen der schmetterlinge vom urania- und morpho-typ , 2004, Zeitschrift für Morphologie und Ökologie der Tiere.

[44]  A. Parker,et al.  A unique form of light reflector and the evolution of signalling in Ovalipes (Crustacea: Decapoda: Portunidae) , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[45]  J. Vigneron,et al.  Beyond butterflies—the diversity of biological photonic crystals , 2007 .

[46]  Shuichi Kinoshita,et al.  Structural colors in nature: the role of regularity and irregularity in the structure. , 2005, Chemphyschem : a European journal of chemical physics and physical chemistry.

[47]  Akira Saito,et al.  Reproduction of the Morpho butterfly's blue: arbitration of contradicting factors , 2004, SPIE Optics + Photonics.

[48]  F. Schlote,et al.  [DEVELOPMENT OF THE LEPIDOPTERAN SCALES IN EPHESTIA KUEHNIELLA ZELLER]. , 1964, Zeitschrift fur Zellforschung und mikroskopische Anatomie.

[49]  A. Parker,et al.  Dual gratings interspersed on a single butterfly scale , 2008, Journal of The Royal Society Interface.

[50]  G. Borgia SEXUAL SELECTION AND THE EVOLUTION OF MATING SYSTEMS , 1979 .

[51]  A. Richards,et al.  An Electron Microscope Study of Some Structural Colors of Insects , 1942 .

[52]  L. Plattner Optical properties of the scales of Morpho rhetenor butterflies: theoretical and experimental investigation of the back-scattering of light in the visible spectrum , 2004, Journal of The Royal Society Interface.

[53]  H. Ghiradella,et al.  Development of ultraviolet‐reflecting butterfly scales: How to make an interference filter , 1974, Journal of morphology.

[54]  H. Ghiradella,et al.  Structure and development of iridescent butterfly scales: Lattices and laminae , 1989, Journal of morphology.

[55]  O. Taylor,et al.  Ultraviolet Differences between the Sulphur Butterflies, Colias eurytheme and C. philodice, and a Possible Isolating Mechanism , 1973, Nature.

[56]  Jean-Pol Vigneron,et al.  Natural layer-by-layer photonic structure in the squamae of Hoplia coerulea (Coleoptera). , 2005 .

[57]  J. Sambles,et al.  Structurally assisted blackness in butterfly scales , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[58]  M F Land,et al.  Mechanism of reflexion in silvery layers of fish and cephalopods , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[59]  Eli Yablonovitch,et al.  Optics: Liquid versus photonic crystals , 1999, Nature.

[60]  Jian Zi,et al.  Structural origin of the brown color of barbules in male peacock tail feathers. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[61]  D. Stavenga,et al.  Tuning of Photoreceptor Spectral Sensitivities by Red and Yellow Pigments in the Butterfly Papilio xuthus , 1999 .

[62]  M F Land,et al.  The physics and biology of animal reflectors. , 1972, Progress in biophysics and molecular biology.

[63]  E. Yablonovitch,et al.  Inhibited spontaneous emission in solid-state physics and electronics. , 1987, Physical review letters.

[64]  P. Vukusic,et al.  Directionally Controlled Fluorescence Emission in Butterflies , 2005, Science.

[65]  H. Ghiradella,et al.  Structure of Iridescent Lepidopteran Scales: Variations on Several Themes , 1984 .

[66]  Shuichi Kinoshita,et al.  Wavelength–selective and anisotropic light–diffusing scale on the wing of the Morpho butterfly , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  P. Wong,et al.  Effects of a butterfly scale microstructure on the iridescent color observed at different angles. , 1999, Optics express.

[68]  R. Rutowski Sexual Discrimination Using Visual Cues in the Checkered White Butterfly (Pieris protodice) , 2010 .

[69]  D R McKenzie,et al.  Electron tomography and computer visualisation of a three-dimensional 'photonic' crystal in a butterfly wing-scale. , 2002, Micron.

[70]  J. Robertson,et al.  Structure and molecular anisotropy of sorbic acid, CH3 . CH : CH . CH : CH . COOH , 1941, Proceedings of the Royal Society of London. Series A. Mathematical and Physical Sciences.

[71]  J. Zeil,et al.  Butterfly wing colours: scale beads make white pierid wings brighter , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[72]  H. Ghiradella Light and color on the wing: structural colors in butterflies and moths. , 1991, Applied optics.

[73]  Jane Overton,et al.  MICROTUBULES AND MICROFIBRILS IN MORPHOGENESIS OF THE SCALE CELLS OF EPHESTIA KÜHNIELLA , 1966, The Journal of cell biology.

[74]  C. W. Mason,et al.  Structural Colors in Insects. II , 1926 .

[75]  J. Zi,et al.  Coloration strategies in peacock feathers , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Andrew R. Parker,et al.  Diffractive optics in spiders , 2003 .

[77]  H. Ghiradella,et al.  Development of butterfly scales. II. Struts, lattices and surface tension , 1976, Journal of morphology.

[78]  Andrew R. Parker,et al.  Biomimetics of photonic nanostructures. , 2007, Nature nanotechnology.

[79]  John Huxley,et al.  Wing‐scales of Pseudoleptocerus chirindensis Kimmins (Trichoptera: Leptoceridae) , 1988 .

[80]  K. Arikawa,et al.  Pentachromatic visual system in a butterfly , 1987, Naturwissenschaften.

[81]  Makio Akimoto,et al.  Microstructures and Optical Properties of Scales of Butterfly Wings , 1996 .

[82]  L. Biró,et al.  Role of photonic-crystal-type structures in the thermal regulation of a Lycaenid butterfly sister species pair. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[83]  Andrew R. Parker,et al.  Structural colour: Opal analogue discovered in a weevil , 2003, Nature.

[84]  S. Berthier,et al.  Morphological structure and optical properties of the wings of Morphidae , 2006 .