Pointillist structural color in Pollia fruit

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...

Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

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

Winter

Butz

Dieker

et al. 2015

“…Structural coloration is widespread in nature and can be observed in butterflies (10,26), beetles (27)(28)(29)(30), fruits (31,32), as well as fish (33,34). Obviously, the control of the color of the reflected light as well as of the directional distribution is likely to be a behaviorally linked, key characteristic of many iridescent animals (35,36).…”

Section: Discussionmentioning

confidence: 99%

Sparkling feather reflections of a bird-of-paradise explained by finite-difference time-domain modeling

Wilts

Michielsen²,

Raedt

et al. 2014

111

121

Birds-of-paradise are nature's prime examples of the evolution of color by sexual selection. Their brilliant, structurally colored feathers play a principal role in mating displays. The structural coloration of both the occipital and breast feathers of the bird-of-paradise Lawes' parotia is produced by melanin rodlets arranged in layers, together acting as interference reflectors. Light reflection by the silvery colored occipital feathers is unidirectional as in a classical multilayer, but the reflection by the richly colored breast feathers is threedirectional and extraordinarily complex. Here we show that the reflection properties of both feather types can be quantitatively explained by finite-difference time-domain modeling using realistic feather anatomies and experimentally determined refractive index dispersion values of keratin and melanin. The results elucidate the interplay between avian coloration and vision and indicate tuning of the mating displays to the spectral properties of the avian visual system. biophotonics | body colors | courtship | signaling | reflectance B irds-of-paradise are best known for their magnificent coloration. Living isolated on Papua New Guinea and its satellite islands (1), the absence of predators has allowed these birds to become extremely specialized for female sexual selection (2). Male birds-of-paradise have evolved extravagant ornamental traits, with intricate sounds and ritualized sets of dance steps and movements accompanied by simultaneous elaborate feather movements, all combined in beautiful displays to win the favor of females (1-4). Among the 39 species of birds-of-paradise almost all colors of the rainbow can be found, and often the males advertise themselves with brilliant, vivid colors framed within a jet-black background. The females on the other hand have dull brownish plumage which has remained in its ancestral color state (1, 2).Whereas the biological purpose of the colorful displays is relatively well understood (1, 2), the coloration mechanisms of the birds' displays and the connection to the visual system of the animals are poorly explored. Feather coloration can be generally categorized in two forms: pigmentary and structural. Randomly arranged, inhomogeneous media containing pigments are colored, because the pigments absorb the diffusely scattered light in a restricted wavelength range. For instance, carotenoids cause the colorful yellow or red feathers of many songbirds (5), and the ubiquitous, broad-band absorbing pigment melanin causes feathers to be black (6). Structural colors occur in feather barbs due to quasiordered spongy structures, and in feather barbules due to melanosomes--nanosized, melanin-containing granules--regularly arranged in layers within a keratin matrix, resulting in directional reflections because of constructive interference (7-11). Differences in the morphology of the structural colored feathers, i.e., in the dimensions of the spongy structured barbs or the melanosome multilayers in the barbules, can modify the color of the ...

“…A lthough structural color is widespread across both the animal and plant kingdoms (1)(2)(3)(4), there are very few cases in which the photonic structures are tunable and adaptive (5)(6)(7). Many cephalopods exhibit iridescence, but only a few squid species can tune this iridescence for adaptive camouflage and communication (8,9) by modulating the periodicity of multilayer reflectors (7) in specialized cells classically called iridocytes.…”

Section: Doryteuthis Opalescens | Iridophore | Structural Colormentioning

confidence: 99%

Membrane invaginations facilitate reversible water flux driving tunable iridescence in a dynamic biophotonic system

DeMartini

Krogstad

Morse

2013

101

132

Squids have used their tunable iridescence for camouflage and communication for millions of years; materials scientists have more recently looked to them for inspiration to develop new "biologically inspired" adaptive optics. Iridocyte cells produce iridescence through constructive interference of light with intracellular Bragg reflectors. The cell's dynamic control over the apparent lattice constant and dielectric contrast of these multilayer stacks yields the corresponding optical control of brightness and color across the visible spectrum. Here, we resolve remaining uncertainties in iridocyte cell structure and determine how this unusual morphology enables the cell's tunable reflectance. We show that the plasma membrane periodically invaginates deep into the iridocyte to form a potential Bragg reflector consisting of an array of narrow, parallel channels that segregate the resulting high refractive index, cytoplasmic protein-containing lamellae from the lowindex channels that are continuous with the extracellular space. In response to control by a neurotransmitter, the iridocytes reversibly imbibe or expel water commensurate with changes in reflection intensity and wavelength. These results allow us to propose a comprehensive mechanism of adaptive iridescence in these cells from stimulation to color production. Applications of these findings may contribute to the development of unique classes of tunable photonic materials. Doryteuthis opalescens | iridophore | structural colorA lthough structural color is widespread across both the animal and plant kingdoms (1-4), there are very few cases in which the photonic structures are tunable and adaptive (5-7). Many cephalopods exhibit iridescence, but only a few squid species can tune this iridescence for adaptive camouflage and communication (8,9) by modulating the periodicity of multilayer reflectors (7) in specialized cells classically called iridocytes.[Earlier workers have referred to these cells variously as iridocytes, iridophores, or reflective cells. We use here the unambiguous convention of contemporary cell biology, referring to them as iridocytes (literally "iridescent cells"), with no specific photonic mechanism implied.] For this reason, the tunable photonics of squids have long been a source of intrigue and inspiration to materials scientists (10-12). Although it is known that the neurotransmitter acetylcholine (ACh) activates a signal-transduction cascade to drive the changes in periodicity of the reflectors (7, 13), and the nerve cells delivering this signal recently have been identified (14), details of the molecular mechanisms and cellular architectures governing the biophotonic processes themselves have remained elusive.Morphology of cephalopod iridocytes has traditionally been interrogated by light microscopy ( Fig. 1 A and B) and transmission electron microscopy (TEM) (Fig. 1 C and D), revealing the membrane-bound subcellular lamellae that constitute a Bragg reflector. Whereas these analyses by optical imaging are fundamentally limited because t...