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Coloration Mechanisms and Phylogeny of Morpho Butterflies M © 2016. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2016) 219, 3936-3944 doi:10.1242/jeb.148726 RESEARCH ARTICLE Coloration mechanisms and phylogeny of Morpho butterflies M. A. Giraldo1,*, S. Yoshioka2, C. Liu3 and D. G. Stavenga4 ABSTRACT scales (Ghiradella, 1998). The ventral wing side of Morpho Morpho butterflies are universally admired for their iridescent blue butterflies is studded by variously pigmented scales, together coloration, which is due to nanostructured wing scales. We performed creating a disruptive pattern that may provide camouflage when the a comparative study on the coloration of 16 Morpho species, butterflies are resting with closed wings. When flying, Morpho investigating the morphological, spectral and spatial scattering butterflies display the dorsal wing sides, which are generally bright- properties of the differently organized wing scales. In numerous blue in color. The metallic reflecting scales have ridges consisting of previous studies, the bright blue Morpho coloration has been fully a stack of slender plates, the lamellae, which in cross-section show a attributed to the multi-layered ridges of the cover scales’ upper Christmas tree-like structure (Ghiradella, 1998). This structure is not laminae, but we found that the lower laminae of the cover and ground exclusive to Morpho butterflies and has also been found in other scales play an important additional role, by acting as optical thin film butterfly species, for instance pierids, reflecting in the blue and/or reflectors. We conclude that Morpho coloration is a subtle UV wavelength range (Ghiradella et al., 1972; Rutowski et al., combination of overlapping pigmented and/or unpigmented scales, 2007; Giraldo et al., 2008). In Morpho, with their thickness and ∼ multilayer systems, optical thin films and sometimes undulated scale spacing being in the 100 nm range, the lamellae create a multilayer surfaces. Based on the scales’ architecture and their organization, that strongly reflects blue light. The number of layers, which five main groups can be distinguished within the genus Morpho, determines the reflection intensity, varies with the species and type largely agreeing with the accepted phylogeny. of scale (Gralak et al., 2001; Kinoshita et al., 2002; Plattner, 2004; Berthier et al., 2006). The multilayered scales are classified as KEY WORDS: Wing scales, Spectrophotometry, Scatterometry, iridescent because the reflectance spectrum depends on the angle of Multilayers, Thin films, Butterfly phylogeny illumination. The margins of the Morpho’s blue dorsal wings are commonly brown–black, because of pigmentary colored scales INTRODUCTION containing concentrated melanin pigment (Berthier, 2007). Butterflies of the Neotropics and particularly the genus Morpho have In our previous study, we investigated three characteristic for centuries intrigued scientific researchers as well as laymen because Morpho species, M. epistrophus, M. helenor and M. cypris, and of their striking colors and gracious flight (DeVries et al., 2010). concluded that their brilliant iridescence is due to both a thin film Considerable insight into the evolution of Morpho has been gained by lower lamina and a multilayered upper lamina (Giraldo and phylogenetic studies (Penz and DeVries, 2002; Penz et al., 2012; Stavenga, 2016). Here we present a comparative study on 16 of Cassildé et al., 2012; Blandin and Purser, 2013). Furthermore, detailed the 30 accepted Morpho species (Blandin and Purser, 2013; Chazot anatomical and optical investigations of the scales that cover the wings et al., 2016). We specifically focus on the spectral and have yielded substantial knowledge of the physical basis of the morphological scale characteristics, at both a macroscopical and a brilliant-blue colored wings (Ghiradella, 1984; Vukusic et al., 1999; microscopical level, by applying microscopy, spectrophotometry Yoshioka and Kinoshita, 2004; Berthier, 2007; Kinoshita, 2008). and imaging scatterometry. The assembled data indicate a distinct Butterfly wing scales basically consist of two laminae connected classification of the investigated species. We have come to identify by pillar-like structures, the trabeculae (Ghiradella, 1989). The five groups according to the overlapping of ground scales by cover lower lamina is commonly a smooth membrane that can act as an scales, which appears to be in fair agreement with the recently optical thin-film reflector (Yoshioka and Kinoshita, 2004; Stavenga deduced phylogeny of the Morphinae (Blandin and Purser, 2013). et al., 2014; Giraldo and Stavenga, 2016). The upper lamina is a much more intricate structure, consisting of an array of ridges MATERIALS AND METHODS parallel to the longitudinal axis of the scale and an array of cross-ribs Animals at right angles to the former. We studied specimens of 16 butterfly species belonging to the genus The wings of butterflies are shingled on both the ventral and Morpho Fabricius 1807. Morpho achilles, M. aega, M. cypris, dorsal side by a regular lattice of overlapping ground and cover M. deidamia, M. epistrophus, M. godarti, M. helenor helenor, M. marcus, M. menelaus didius, M. menelaus menelaus, M. portis, M. rhetenor, M. sulkowskyi, M. theseus and M. zephyritis were 1Biophysics Group, Institute of Physics, University of Antioquia, Calle 70 #52-21, AA purchased from commercial suppliers. Dr Marta Wolff, Entomology 1226, Medellıń 050010, Colombia. 2Tokyo University of Science, Faculty of Science and Technology, Department of Physics, 2641 Yamazaki, Noda-shi, Chiba-ken Group, University of Antioquia (Medellín, Colombia) generously 278-8510, Japan. 3School of Materials Science and Engineering, Georgia Institute supplied M. helenor peleides. of Technology, Atlanta, GA 30332, USA. 4Computational Physics, Zernike Institute for Advanced Materials, University of Groningen, Nijenborgh 4, Groningen NL-9747 AG, The Netherlands. Microphotography Local areas of intact wings and single wing scales were *Author for correspondence ([email protected]) photographed with a Zeiss Universal Microscope (Zeiss, M.A.G., 0000-0003-3437-6308 Oberkochen, Germany) using Zeiss Epiplan objectives (8×/0.2 or 16×/0.35) and a Kappa DX-40 (Kappa Optronics GmbH, Gleichen, Received 25 August 2016; Accepted 4 October 2016 Germany) digital camera. Single wing scales were obtained by Journal of Experimental Biology 3936 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 3936-3944 doi:10.1242/jeb.148726 gently pressing intact wings to a glass microscope slide. The A E I isolated scales were glued to the tip of a glass micropipette, which was mounted on the rotatable stage of the microscope. Imaging scatterometry To investigate the spatial far-field reflection characteristics, we * performed imaging scatterometry on small wing pieces and single scales (Stavenga et al., 2009), which were attached to the tip of a * glass micropipette and positioned at the first focal point of the M. marcus ellipsoidal mirror of the imaging scatterometer. Scatterograms were obtained by focusing a white light beam with a narrow aperture B F J (<5 deg) onto a circular spot with diameter ∼400 µm (wing pieces) or ∼30 µm (isolated scales). The spatial distribution of the far-field scattered light was recorded with an Olympus DP70 digital camera (Olympus, Tokyo, Japan). The red circles in the scatterograms (e.g. Fig. 1I–L) indicate reflection cone angles of 5, 30, 60 and 90 deg. * The scatterograms thus represent the far-field reflection hemisphere. Spectrophotometry M. achilles Reflectance spectra of intact wings were recorded with an C G integrating sphere (AvaSphere-50-Refl; Avantes, Apeldoorn, the G K Netherlands) using a deuterium-halogen lamp [Avantes AvaLight- D(H)-S] and an AvaSpec-2048 spectrometer (Avantes). A white * reflectance standard (WS-2, Avantes) served as a reference. Reflectance spectra were also measured of single scales for both the abwing and adwing sides (ab=away from; ad=toward), i.e. the sides facing the observer and the wing, respectively, with a custom- built microspectrophotometer (MSP), which consists of a Leitz Ortholux epi-illumination microscope connected with a fiber-optic M. zephyritis cable to the AvaSpec-2048 spectrometer. The light source was a D H L xenon arc and the microscope objective was an Olympus LUCPlanFL N 20×/0.45. Owing to the glass optics, the MSP spectra were limited to wavelengths >350 nm. * Scanning electron microscopy A Philips XL-30 scanning electron microscope was used to investigate single scales placed on a carbon stub holder, with either the upper or lower lamina exposed. To reveal the transversal morphology of the scales, scales were trans-sectioned with a razor M. aega blade. Prior to imaging, the samples were sputtered with gold. M 0.6 RESULTS M. marcus Different scale lattices of Morpho butterflies M. achilles M. zephyritis We studied the dorsal wing sides of male butterflies of 16 Morpho M. aega species and classified for each species the lattice organization, the 0.4 morphology of the scales covering the wings, their spectral and spatial optical properties, and the number of lamellae that form the ridges. The experimental results indicated a division of the investigated species into five groups. Reflectance 0.2 In our previous study (Giraldo and Stavenga, 2016), we extensively described the case of M. epistrophus. Its unpigmented cover and ground scales, which have a blueish coloration owing to 0 the scales’ lower laminae acting as an optical thin film, appeared to
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