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)

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1502, 2008, Pages 2465-2480

  Ingram, A L ^a   Parker, A R ^a  

^a DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

Author keywords

Butterfly; Diversity; Evolution; Interference; Photonic; Structural colour

Indexed keywords

BUTTERFLY; COLOR MORPH; ELECTRON PROBE ANALYSIS; EVOLUTION; SPECIES DIVERSITY; WING MORPHOLOGY;

PAPILIONOIDEA;

EID: 45249092517     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2007.2258     Document Type: Review

References (102)

1. Allyn, A. C. & Downey, J. C. 1976 Diffraction structures in the wing scales of Callophrys (Mitoura) siva siva (Lycaenidae). Bull. Allyn Museum 40, 1-6.
2. Anderson, T. F. & Richards, A. G. 1942 An electron microscope study of some structural colours of insects. J. Appl. Phys. 13, 748-758. (doi:10.1063/1.1714827)
3. Argyros, A., Manos, S., Large, M. C. J., McKenzie, D. R., Cox, G. C. & Dwarte, D. M. 2002 Electron tomography and computer visualisation of a three-dimensional 'photonic' crystal in a butterfly wing-scale. Micron 33, 483-487. (doi:10.1016/S0968-4328(01)00044-0)
4. Arikawa, K. & Stavenga, D. G. 1997 Random array of colour filters in the eyes of butterflies. J. Exp. Biol. 200, 2501-2506.
5. Arikawa, K., Inokuma, K. & Eguchi, E. 1987 Pentachromatic visual system in a butterfly. Naturwissenschaften 74, 297-298. (doi:10.1007/BF00366422)
6. Arikawa, K., Mizuno, S., Scholten, D. G. W., Kinoshita, M., Seki, T., Kitamoto, J. & Stavenga, D. G. 1999a An ultraviolet-absorbing pigment causes a narrow-band violet receptor and a single-peaked green receptor in the eye of the butterfly Papilio. Vis. Res. 39, 1-8. (doi:10.1016/S0042-6989(98)00070-4)
7. Arikawa, K., Scholten, D. G. W., Kinoshita, M. & Stavenga, D. G. 1999b Tuning of photoreceptor spectral sensitivities by red and yellow pigments in the butterfly Papilio xuthus. Zool. Sci. 16, 17-24. (doi:10.2108/zsj.16.17)
8. Bálint, Z., Vértesy, Z. & Biró, L. P. 2005 Microstructures and nanostructures of high Andean Penaincisalia lycaenid butterfly scales (Lepidoptera: Lycaenidae): descriptions and interpretations. J. Nat. Hist. 39, 2935-2952. (doi:10.1080/00222930500140629)
9. Berthier, S. 2005 Thermoregulation and spectral selectivity of the tropical butterfly Prepona meander: a remarkable example of temperature auto-regulation. Appl. Phys. A 80, 1397-1400. (doi:10.1007/s00339- 004-3185-x)
10. Berthier, S. 2007 Iridescences: The Physical Colors of Insects. New York: Springer.
11. Berthier, S., Charron, E. & Da Silva, A. 2003 Determination of the cuticle index of the scales of the iridescent butterfly Morpho menelaus. Optics Commun. 228, 349-356. (doi:10.1016/j.optcom.2003.10.032)
12. Berthier, S., Charron, E. & Boulenguez, J. 2006 Morphological structure and optical properties of the wings of Morphidae. Insect Sci. 13, 145-157. (doi:10.1111/j.1744-7917.2006.00077.x)
13. Bingham, L., Bingham, I., Geary, S., Tanner, J., Driscoll, C., Cluff, B. & Gardener, J. S. 1995 SEM comparison of Morpho butterfly dorsal and ventral scales. Microsc. Res. Tech. 31, 93-94. (doi:10.1002/jemt.1070310108)
14. Biró, L. P. et al. 2003 Role of photonic crystal-type structures in the thermal regulation of a lycaenid butterfly sister species pair. Phys. Rev. E 67, 0 219 071-0 219 077. (doi:10.1103/PhysRevE. 67.021907)
15. Brink, D. J. & Lee, M. E. 1996 Ellipsometry of diffractive insect reflectors. Appl. Opt. 35, 1950-1955.
16. Brink, D. J., Smit, J. E., Lee, M. E. & Moller, A. 1995 Optical diffraction by the microstructure of the wing of a moth. Appl. Opt. 34, 6049-6057.
17. Darwin, C. 1880 The sexual colours of certain butterflies. Nature 8, 237.
18. Denton, E. J. & Land, M. F. 1971 Mechanism of reflexion in silvery layers of fish and cephalopods. Proc. R. Soc. A 178, 43-61.
19. Denton, E. J. & Nichol, J. A. C. 1965 Studies on reflexion of light from silvery surfaces of fishes, with special reference to the bleak, Alburnus alburnus. J. Mar. Biol. Assoc. UK 45, 683-702.
20. Denton, E. J. & Nichol, J. A. C. 1966 A survey of reflectivity in silvery teleosts. J. Mar. Biol. Assoc. UK 46, 685-722.
21. Downey, J. C. & Allyn, A. C. 1975 Wing-scale morphology and nomenclature. Bull. Allyn Museum 31, 1-32.
22. Gentil, K. 1942 Elektronenmikrosckopische Unetersuchung des Feinbaues schillernder Leisten von Morpho-Schuppen. Z. Morphol. Okol. Tiere 38, 344. (doi:10.1007/BF01434120)
23. Ghiradella, H. 1974 Development of ultraviolet-reflecting butterfly scales: how to make an interference filter. J. Morphol. 142, 395-410. (doi:10.1002/jmor.1051420404)
24. Ghiradella, H. 1984 Structure of iridescent lepidopteran scales - variations on several themes. Ann. Entomol. Soc. Am. 77, 637-645.
25. Ghiradella, H. 1985 Structure and development of iridescent Lepidopteran scales - the Papilionidae as a showcase family. Ann. Entomol. Soc. Am. 78, 252-264.
26. Ghiradella, H. 1989 Structure and development of iridescent butterfly scales - lattices and laminae. J. Morphol. 202, 69-88. (doi:10.1002/jmor.1052020106)
27. Ghiradella, H. 1991 Light and color on the wing - structural colors in butterflies and moths. Appl. Opt. 30, 3492-3500.
28. Ghiradella, H. 1994 Structure of butterfly scales - patterning in an insect cuticle. Microsc. Res. Tech. 27, 429-438. (doi:10.1002/jemt.1070270509)
29. Ghiradella, H. 1998 Hairs, bristles and scales. In Microscopic anatomy of invertebrates (ed. M. Locke), pp. 257-287. New York, NY: Wiley-Liss Publishers.
30. Ghiradella, H. & Radigan, W. 1976 Development of butterfly scales. II. Struts, lattices and surface tension. J. Morphol. 150, 279-298. (doi:10.1002/jmor.1051500202)
31. Ghiradella, H., Aneshansley, D., Eisner, T., Silberglied, R. E. & Hinton, H. E. 1972 Ultraviolet reflection of a male butterfly : interference color caused by thin-layer elaboration of wing scales. Science 178, 1214-1217. (doi:10.1126/science.178.4066.1214)
32. Gralak, B., Tayeb, G. & Enoch, S. 2001 Morpho butterflies wings color modeled with lamellar grating theory. Opt. Express 9, 567-578.
33. Greenstein, M. E. 1972 The ultrastructure of developing wings in the giant silkmoth, Hyalophora cecropia. I. Generalized epidermal cells. J. Morphol. 136, 1-22. (doi:10.1002/jmor.1051360102)
34. Huxley, J. 1975 The basis of structural colour variation in two species of Papilio. J. Entomol. (A) 50, 9-22.
35. Huxley, J. 1976 The colouration of Papilio zalmoxis and P. antimachus and the discovery of Tyndall blue in butterflies. Proc. R. Soc. B 193, 441-453. (doi:10.1098/rspb.1976.0056)
36. Huxley, J. & Barnard, P. C. 1988 Wing scales of Pseudoleptocerus chirindensis Kimmins (Trichoptera, Leptoceridae). Zool. J. Linn. Soc. 92, 285-312.
37. Ingram, A. L. In press. Butterfly photonics. In Functional surfaces in biology (ed. S. Gorb). New York, NY: Springer.
38. Ingram, A. L., Vigneron, J. P., Parker, A. R. & Lousse, V. Accepted. Dual gratings interspersed on a single butterfly scale. J. R. Soc. Interface.
39. Ingram, A. L., Vigneron, J. P., Parker, A. R. & Lousse, V. In press. Blazed gratings on a butterfly scale produce novel iridescence patterns. Phys. Rev. E.
40. Ingram, A. L., Lousse, V. Vigneron, J. P. & Parker, A. R. Submitted. Structural origin of the blue iridescence on the wings of Hypochrysops polycletus.
41. Jenkins, F. A. & White, H.E 1981. Fundamentals of optics. Singapore: McGraw-Hill International Editions.
42. Jones, R. W. & Tilley, R. J. D. 1999 Colour, ultraviolet reflectivity andiridescent scale structure in Quercusia quercus (1.,1758) and Laeosopis roboris (Esper, 1793) (Lepidoptera: Lycaenidae). Entomol. Gaz. 50, 181-187.
43. Kertész, K., Bálint, Z., Vértesy, Z., Mark, G. I., Lousse, V., Vigneron, J. P. & Biró, L. P. 2006a Photonic crystal type structures of biological origin: structural and spectral characterization. Curr. Appl. Phys. 6, 252-258. (doi:10.1016/j.cap.2005.07.051)
44. Kertész, K., Bálint, Z., Vértesy, Z., Mark, G. I., Lousse, V., Vigneron, J. P., Rassart, M. & Biró, L. P. 2006b Gleaming and dull surface textures from photonic crystal type nanostructures in the butterfly Cyanophrys remus. Phys. Rev. E 74, 15. (doi:10.1103/PhysRevE.74.021922)
45. Kinoshita, S. & Yoshioka, S. 2005 Structural colors in nature: the role of regularity and irregularity in the structure. ChemPhysChem 6, 1442-1459. (doi:10.1002/cphc.200500007)
46. Kinoshita, S., Yoshioka, S. & Kawagoe, K. 2002 Mechanisms of structural colour in the Morpho butterfly: cooperation of regularity and irregularity in an iridescent scale. Proc. R. Soc. B 269, 1417-1421. (doi:10.1098/rspb.2002.2019)
47. Land, M. F. 1972 The physics and biology of animal reflectors. Prog. Biophys. Mol. Biol. 24, 75-106. (doi:10.1016/0079-6107(72)90004-1)
48. Lawrence, C., Vukusic, P. & Sambles, R. 2002 Grazing-incidence iridescence from a butterfly wing. Appl. Opt. 41, 437-441. (doi:10.1364/AO.41.000437)
49. Li, Y. H., Lu, Z. H., Yin, H. W., Yu, X. D., Liu, X. H. & Zi, J. 2005 Structural origin of the brown color of barbules in male peacock tail feathers. Phys. Rev. E 72, 010902. (doi:10.1103/PhysRevE.72.010902)
50. Lippert, W. & Gentil, K. 1951 Elektronenmikroskopische studien uber micellare strukturen bei schmetterlingsschuppen vom Morpho-typ. Z. wiss. Mikr. 61, 95-100.
51. Lippert, W. & Gentil, K. 1959 Uber lamellare feinstrukturen bei den schillerschuppen der schmetterlinge vom Urania und Morpho-typ. Z. Morphol. Okol. Tiere 48, 115-122. (doi:10.1007/BF00407836)
52. Mason, C. W. 1923 Structural colors of feathers. Int. J. Phys. Chem. 27, 201-251. (doi:10.1021/j150228a001)
53. Mason, C. W. 1926 Structural colors in insects. I. Int. J. Phys. Chem. 30, 383-395. (doi:10.1021/j150261a009)
54. Mason, C. W. 1927a Structural colors in insects. II. Int. J. Phys. Chem. 31, 321-354. (doi:10.1021/j150273a001)
55. Mason, C. W. 1927b Structural colors in insects. III. Int. J. Phys. Chem. 31, 1856-1872. (doi:10.1021/j150282a008)
56. Mayer, A. G. 1896 On the color and color-patterns of moths and butterflies. Bull. Museum Comp. Zool. 30, 169-256.
57. Morris, R. B. 1975 Iridescence from diffraction structures in the wing scales of Callophrys rubi, the Green Hairstreak. J. Entomol. 49, 149-154.
58. Moss, M. O. & Gibbs, G. 1997 The wing scales of the common blue butterfly. Quekett J. Microsc. 38, 49-55.
59. Newton, I. 1704 Opticks. London, UK: The Royal Society.
60. Onslow, H. 1921 On a periodic structure in many insect scales, and the cause of their iridescent colours. Phil. Trans. R. Soc. B 211, 1-74. (doi:10.1098/rstb.1923.0001)
61. Overton, J. 1966 Microtubules and microfibrils in morphogenesis of the scale cells of Ephestia kuhniella. J. Cell Biol. 29, 293-305. (doi:10.1083/jcb.29.2.293)
62. Parker, A. R. 1995 Discovery of functional iridescence and its coevolution with eyes in the phylogeny of Ostracoda (Crustacea). Proc. R. Soc. B 262, 349-355. (doi:10.1098/rspb.1995.0216)
63. Parker, A. R. 2006 Conservative photonic crystals imply indirect transcription from genotype to phenotype. Recent Res. Dev. Entomol. 5, 1-10.
64. Parker, A. R. & Hegedus, Z. 2003 Diffractive optics in spiders. J. Opt. A: Pure Appl. Opt. 5, S111-S116. (doi:10.1088/1464-4258/5/4/ 364)
65. Parker, A. R. & Townley, H. E. 2007 Biomimetics of photonic nanostructures. Nat. Nanotechnol. 2, 347-353. (doi:10.1038/nnano. 2007.152)
66. Parker, A. R., McKenzie, D. R. & Ahyong, S. T. 1998 A unique form of light reflector and the evolution of signalling in Ovalipes (Crustacea: Decapoda: Portunidae). Proc. R. Soc. B 265, 861-867. (doi:10.1098/rspb.1998.0371)
67. Parker, A. R., McPhedran, R. C., McKenzie, D. R., Botten, L. C. & Nicorovici, N. A. P. 2001 Photonic engineering - Aphrodite's iridescence. Nature 409, 36-37. (doi:10.1038/35051168)
68. Parker, A. R., Welch, V. L., Driver, D. & Martini, N. 2003 Structural colour - opal analogue discovered in a weevil. Nature 426, 786-787. (doi:10.1038/426786a)
69. Paweletz, N. & Schlote, F.-W. 1964 Die entwicklung der schmetterlingsschuppe bei Ephestia kuhniella zeller. Zeitschrift fur Zellforschung 63, 840-870. (doi:10.1007/BF00336225)
70. Plattner, L. 2004 Optical properties of the scales of Morpho rhetenor butterflies: theoretical and experimental investigation of the back-scattering of light in the visible spectrum. J. R. Soc. Interface 1, 49-59. (doi:10.1098/rsif.2004.0006)
71. Prum, R. O., Torres, R., Williamson, S. & Dyck, J. 1999 Two-dimensional Fourier analysis of the spongy medullary keratin of structurally coloured feather barbs. Proc. R. Soc. B 266, 13-22. (doi:10.1098/rspb.1999.0598)
72. Prum, R. O., Quinn, T. & Torres, R. H. 2006 Anatomically diverse butterfly scales all produce structural colours by coherent scattering. J. Exp. Biol. 209, 748-765. (doi:10.1242/jeb.02051)
73. Rutowski, R. L. 1981 Sexual discrimination using visual cues in the checkered white butterfly (Pieris protidice). Z. Tierpsychol. 55, 325-334.
74. Saito, A., Yoshioka, S. & Kinoshita, S. 2004 Reproduction of the Morpho butterfly's blue: arbitration of contradicting factors. In Optical systems degradation, contamination and stray light: effects, measurements and control (eds P. T. C. Chen, J. C. Fleming & M. G. Dittman), pp. 188-194. Bellingham, WA: SPIE.
75. Silberglied, R. E. & Taylor, O. R. 1973 Ultraviolet differences between the sulphur butterflies, Colias eurytheme and C. philodice, and a possible isolating mechanism. Nature 241, 406-408. (doi:10.1038/241406a0)
76. Stavenga, D. G., Stowe, S., Siebke, K., Zeil, J. & Arikawa, K. 2004 Butterfly wing colours: scale beads make white pierid wings brighter. Proc. R. Soc. B 271, 1577-1584. (doi:10.1098/rspb.2004.2781)
77. Suffert, F. 1924 Morphologie und optik der schmetterlingsschuppen. Z. Morphol. Okol. Tierre 1, 171-308. (doi:10.1007/BF00403572)
78. Suffert, F. 1942 Elektronenmikroskopische untersuchung des feinbaues schillernder leisten von Morpho-schuppen. Zeitschr. Morphol. Okol. Tierre 38, 344-355. (doi:10.1007/BF01434120)
79. Tabata, H., Kumazawa, K., Funakawa, M., Takimoto, J. & Akimoto, M. 1996 Microstructures and optical properties of scales of butterfly wings. Opt. Rev. 3, 139-145. (doi:10.1007/s10043-996-0139-x)
80. Tada, H., Mann, S. E., Miaoulis, I. N. & Wong, P. Y. 1998 Effects of a butterfly scale microstructure on the iridescent color observed atdifferent angles. Appl. Opt. 37, 1579-1584.
81. Tilley, R. J. D. 1988 Scale structure and blue colour in the chalkhill blue butterfly, Lysandra coridon (Poda): (Lepidoptera: Lycaenidae). Entomologist 107, 82-89.
82. Tilley, R. J. D. 2000 Further considerations of the colour of the green scales on the underside of the wings of the butterflies Callophrys rubi (Linnaeus, 1758) and C. avis (Chapman, 1909). Entomol. Gazette 51, 191-193.
83. Vértesy, Z., Bálint, Z., Kertesz, K., Mehn, D., Kiricsi, I., Lousse, V., Vigneron, J.-P. & Biró, L. P. 2004 Modifications to wing scale microstructures in lycaenid butterflies. Microsc. Anal. 18, 25-27.
84. Vigneron, J. P., Colomer, J. F., Vigneron, N. & Lousse, V. 2005 Natural layer-by-layer photonic structure in the squamae of Hoplia coerulea (Coleoptera). Phys. Rev. E 72, 061 904. (doi:10.1103/PhysRevE.72.061904)
85. Vigneron, J. P., Colomer, J. F., Rassart, M., Ingram, A. L. & Lousse, V. 2006 Structural origin of the colored reflections from the black-billed magpie feathers. Phys. Rev. E 73, 021 914. (doi:10.1103/PhysRevE. 73.021914)
86. Vukusic, P. & Hooper, I. 2005 Directionally controlled fluorescence emission in butterflies. Science 310, 1151. (doi:10.1126/science. 1116612)
87. Vukusic, P., Sambles, J. R., Lawrence, C. R. & Wootton, R. J. 1999 Quantified interference and diffraction in single Morpho butterfly scales. Proc. R. Soc. B 266, 1403-1411. (doi:10.1098/rspb.1999. 0794)
88. Vukusic, P., Sambles, J. R. & Lawrence, C. R. 2000 Structural colour - colour mixing in wing scales of a butterfly. Nature 404, 457. (doi:10.1038/35006561)
89. Vukusic, P., Sambles, J. R., Lawrence, C. R. & Wootton, R. J. 2002 Limited-view iridescence in the butterfly Ancyluris meliboeus. Proc. R. Soc. B 269, 7-14. (doi:10.1098/rspb.2001.1836)
90. Vukusic, P., Sambles, J. R. & Lawrence, C. R. 2004 Structurally assisted blackness in butterfly scales. Proc. R. Soc. B 271, S237-S239. (doi:10.1098/rsbl.2003.0150)
91. Welch, V. L. 2005 Photonic crystals in biology. In Structural colors in biological systems (eds S. Kinoshita & S. Yoshioka), pp. 53-71. Osaka, Japan: Osaka University Press.
92. Welch, V. L. & Vigneron, J. P. 2007 Beyond butterflies-the diversity of biological photonic crystals. Opt. Quant. Electron 39, 295-303. (doi:10.1007/s11082-007-9094-4)
93. Welch, V. L., Vigneron, J. P. & Parker, A. R. 2005 The cause of colouration in the ctenophore Beroe cucumis. Curr. Biol. 15, R985-R986. (doi:10.1016/j.cub.2005.11.060)
94. Welch, V., Vigneron, J. P., Lousse, V. & Parker, A. 2006 Optical properties of the iridescent organ of the comb-jellyfish Beroe cucumis (Ctenophora). Phys. Rev. E 73, 0 419 161-0 419 167. (doi:10.1103/PhysRevE.73.041916)
95. Wickham, S., Large, M. C. J., Poladian, L. & Jermiin, L. 2006 Exaggeration and suppression of iridescence: the evolution of two-dimensional butterfly structural colours. J. R. Soc. Interface 3, 99-109. (doi:10.1098/rsif.2005.0071)
96. Wiklund, C. 2003 Sexual selection and the evolution of butterfly mating systems. In Butterflies: ecology and evolution taking flight (eds C. L. Boggs, W. B. Watt & P. R. Ehrlich), pp. 67-90. Chicago, IL: The University of Chicago Press.
97. Yablonovitch, E. 1987 Inhibited spontaneous emission in solid-state physics and electronics. Phys. Rev. Lett. E 58, 2059-2062. (doi:10.1103/PhysRevLett.58.2059)
98. Yablonovitch, E. 1999 Liquid versus photonic crystals. Nature 401, 539-541. (doi:10.1038/44038)
99. Yoshioka, S. & Kinoshita, S. 2004 Wavelength-selective and anisotropic light-diffusing scale on the wing of the Morpho butterfly. Proc. R. Soc. B 271, 581-587. (doi:10.1098/rspb.2003.2618)
100. Yoshioka, S. & Kinoshita, S. 2006 Single-scale spectroscopy of structurally colored butterflies: measurements of quantified reflectance and transmittance. J. Opt. Soc. Am. A: Opt. Image Sci. Vis. 23, 134-141. (doi:10.1364/JOSAA.23.000134)
101. Yoshioka, S. & Kinoshita, S. 2007 Polarization-sensitive color mixing in the wing of the Madagascan sunset moth. Opt. Express 15, 2691-2701. (doi:10.1364/OE.15.002691)
102. Zi, J., Yu, X., Li, Y., Hu, X., Xu, C., Wang, X., Lui, X. & Fu, M. 2003 Colouration strategies in peacock feathers. Proc. Natl Acad. Sci. USA 100, 12 576-12 578. (doi:10.1073/pnas.2133313100)