Electron tomography and computer visualisation of a three-dimensional ‘photonic’ crystal in a butterfly wing-scale

Argyros, Alexander; Manos, Steven; Large, M. I.; McKenzie, David R.; Cox, Guy; Dwarte, D.

doi:10.1016/s0968-4328(01)00044-0

Cited by 81 publications

(69 citation statements)

References 8 publications

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“…Ultimately, it will be very productive to conduct 3D Fourier analyses of 3D data sets from high voltage electron microscopy or other tomographic techniques (e.g. Argyros et al, 2002).…”

Section: Uses and Limits Of The Fourier Methodsmentioning

confidence: 99%

Anatomically diverse butterfly scales all produce structural colours by coherent scattering

Prum

Quinn

Torres

2006

Journal of Experimental Biology

199

194

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SUMMARY The structural colours of butterflies and moths (Lepidoptera) have been attributed to a diversity of physical mechanisms, including multilayer interference, diffraction, Bragg scattering, Tyndall scattering and Rayleigh scattering. We used fibre optic spectrophotometry, transmission electron microscopy (TEM) and 2D Fourier analysis to investigate the physical mechanisms of structural colour production in twelve lepidopteran species from four families, representing all of the previously proposed anatomical and optical classes of butterfly nanostructure. The 2D Fourier analyses of TEMs of colour producing butterfly scales document that all species are appropriately nanostructured to produce visible colours by coherent scattering, i.e. differential interference and reinforcement of scattered, visible wavelengths. Previously hypothesized to produce a blue colour by incoherent, Tyndall scattering, the scales of Papilio zalmoxis are not appropriately nanostructured for incoherent scattering. Rather, available data indicate that the blue of P. zalmoxis is a fluorescent pigmentary colour. Despite their nanoscale anatomical diversity, all structurally coloured butterfly scales share a single fundamental physical color production mechanism -coherent scattering. Recognition of this commonality provides a new perspective on how the nanostructure and optical properties of structurally coloured butterfly scales evolved and diversified among and within lepidopteran clades.

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“…Ultimately, it will be very productive to conduct 3D Fourier analyses of 3D data sets from high voltage electron microscopy or other tomographic techniques (e.g. Argyros et al, 2002).…”

Section: Uses and Limits Of The Fourier Methodsmentioning

confidence: 99%

Anatomically diverse butterfly scales all produce structural colours by coherent scattering

Prum

Quinn

Torres

2006

Journal of Experimental Biology

199

194

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“…Systematic application of scanning TEM (STEM) electron tomography (ET) here enables us to obtain sufficiently detailed and reliable real-space spatial data to assert firmly the chirality of the crystallites and the orientation relation of crystallites within single butterfly wing scales of C. rubi. Although individual tomograms have been analyzed for specific biological tissue [including bluebird feathers (24), the butterfly Teinopalpus imperialis (25), and also, C. rubi (8)], our study clearly shows the potential that systematic application of ET holds for understanding the finer but important secondary characteristics, such as chirality or crystallographic texture, for biological matter.…”

Section: Significancementioning

confidence: 99%

Coexistence of both gyroid chiralities in individual butterfly wing scales of Callophrys rubi

Winter

Butz

Dieker

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The wing scales of the Green Hairstreak butterfly Callophrys rubi consist of crystalline domains with sizes of a few micrometers, which exhibit a congenitally handed porous chitin microstructure identified as the chiral triply periodic single-gyroid structure. Here, the chirality and crystallographic texture of these domains are investigated by means of electron tomography. The tomograms unambiguously reveal the coexistence of the two enantiomeric forms of opposite handedness: the left-and right-handed gyroids. These two enantiomers appear with nonequal probabilities, implying that molecularly chiral constituents of the biological formation process presumably invoke a chiral symmetry break, resulting in a preferred enantiomeric form of the gyroid structure. Assuming validity of the formation model proposed by Ghiradella H (1989) J Morphol 202(1): 69-88 and Saranathan V, et al. (2010) Proc Natl Acad Sci USA 107(26):11676-11681, where the two enantiomeric labyrinthine domains of the gyroid are connected to the extracellular and intra-SER spaces, our findings imply that the structural chirality of the single gyroid is, however, not caused by the molecular chirality of chitin. Furthermore, the wing scales are found to be highly textured, with a substantial fraction of domains exhibiting the <001> directions of the gyroid crystal aligned parallel to the scale surface normal. Both findings are needed to completely understand the photonic purpose of the single gyroid in gyroid-forming butterflies. More importantly, they show the level of control that morphogenesis exerts over secondary features of biological nanostructures, such as chirality or crystallographic texture, providing inspiration for biomimetic replication strategies for synthetic self-assembly mechanisms.electron tomography | chirality | crystallographic texture | photonic crystal | butterfly wing scales A lthough the formation of chiral structures is fascinating, their occurrence can often be rationalized by simple energy or free energy considerations without a need to resort to their possible biological origin. For example, handed structures are observed in the simplest models of phyllotaxis (1) and self-assembly of biological fibers (2). In such models, there is no energetic distinction between and hence, a balance of the two enantiomers [that is, the right-handed (RH) and left-handed (LH) versions of the chiral structure]. Chiral symmetry breaking, the process by which one enantiomer occurs exclusively or with prevalence, is commonly observed in biological materials on a range of scales from molecular dimensions and the structure of DNA to the macroscopic size of snails (3). The dominance of one enantiomer is driven by the presence of a force or molecular building block that favors one enantiomer over the other; constituent chiral molecules (4), genetically controlled molecular pathways (3), and biological generation of torque (5) are possible causes.Here, we investigate the chiral symmetry breaking of the singlegyroid structure, a complex network-lik...

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“…The three-dimensional crystalline complexity of papilionid and lycaenid butterfly scales has been appreciated since the 1970s (8,11,(15)(16)(17)(18)(19)(20)(21)(22)(23)(24). However, most studies have used 2D electron microscopy (EM) to characterize these 3D photonic nanostructures, which is not sufficient to completely resolve their mesoscale features.…”

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confidence: 99%

“…More recently, Michielsen et al (20) provided further support for their identification of the gyroid nanostructure in Callophrys rubi (Lycaenidae) by showing congruence between a finite difference time domain model of light scattering by a single gyroid structure and single scale reflectance measurements. Argyros et al (23) used tilt-series electron tomography to model the nanostructure of Teinopalpus imperialis (Papilionidae) and concluded that it was a distorted, chiral, tetrahedral structure with an underlying triclinic lattice. Poladian et al (19) and Michielsen and Stavenga (18) respectively suggest a distorted diamond and gyroid morphology for T. imperialis.…”

mentioning

confidence: 99%

“…Poladian et al (19) and Michielsen and Stavenga (18) respectively suggest a distorted diamond and gyroid morphology for T. imperialis. Although electron tomography may be promising, sample shrinkage and other artifacts may alter the nanostructure and its three-dimensional connectivity (23,25). Thus, fundamental uncertainty remains about the precise nanoscale organization of 3D photonic crystals in butterfly wing scales.…”

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confidence: 99%

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Structure, function, and self-assembly of single network gyroid ( I 4 ₁ 32) photonic crystals in butterfly wing scales

Saranathan

Osuji

Mochrie

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

441

412

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Complex three-dimensional biophotonic nanostructures produce the vivid structural colors of many butterfly wing scales, but their exact nanoscale organization is uncertain. We used small angle X-ray scattering (SAXS) on single scales to characterize the 3D photonic nanostructures of five butterfly species from two families (Papilionidae, Lycaenidae). We identify these chitin and air nanostructures as single network gyroid (I4 1 32) photonic crystals. We describe their optical function from SAXS data and photonic band-gap modeling. Butterflies apparently grow these gyroid nanostructures by exploiting the self-organizing physical dynamics of biological lipid-bilayer membranes. These butterfly photonic nanostructures initially develop within scale cells as a core-shell double gyroid (Ia3d), as seen in block-copolymer systems, with a pentacontinuous volume comprised of extracellular space, cell plasma membrane, cellular cytoplasm, smooth endoplasmic reticulum (SER) membrane, and intra-SER lumen. This double gyroid nanostructure is subsequently transformed into a single gyroid network through the deposition of chitin in the extracellular space and the degeneration of the rest of the cell. The butterflies develop the thermodynamically favored double gyroid precursors as a route to the optically more efficient single gyroid nanostructures. Current approaches to photonic crystal engineering also aim to produce single gyroid motifs. The biologically derived photonic nanostructures characterized here may offer a convenient template for producing optical devices based on biomimicry or direct dielectric infiltration.biological meta-materials | organismal color | biomimetics | biological cubic mesophases

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Electron tomography and computer visualisation of a three-dimensional ‘photonic’ crystal in a butterfly wing-scale

Cited by 81 publications

References 8 publications

Anatomically diverse butterfly scales all produce structural colours by coherent scattering

Anatomically diverse butterfly scales all produce structural colours by coherent scattering

Coexistence of both gyroid chiralities in individual butterfly wing scales of Callophrys rubi

Structure, function, and self-assembly of single network gyroid ( I 4 ₁ 32) photonic crystals in butterfly wing scales

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Electron tomography and computer visualisation of a three-dimensional ‘photonic’ crystal in a butterfly wing-scale

Cited by 81 publications

References 8 publications

Anatomically diverse butterfly scales all produce structural colours by coherent scattering

Anatomically diverse butterfly scales all produce structural colours by coherent scattering

Coexistence of both gyroid chiralities in individual butterfly wing scales of Callophrys rubi

Structure, function, and self-assembly of single network gyroid ( I 4 1 32) photonic crystals in butterfly wing scales

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Structure, function, and self-assembly of single network gyroid ( I 4 ₁ 32) photonic crystals in butterfly wing scales