Development of colour-producing β-keratin nanostructures in avian feather barbs (original) (raw)
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Development of colour-producing b-keratin nanostructures in avian feather barbs
2009
The non-iridescent structural colours of avian feather barbs are produced by coherent light scattering from amorphous (i.e. quasi-ordered) nanostructures of b-keratin and air in the medullary cells of feather barb rami. Known barb nanostructures belong to two distinct morphological classes. 'Channel' nanostructures consist of b-keratin bars and air channels of elongate, tortuous and twisting forms. 'Spherical' nanostructures consist of highly spherical air cavities that are surrounded by thin b-keratin bars and sometimes interconnected by tiny passages. Using transmission electron microscopy, we observe that the colour-producing channel-type nanostructures of medullary b-keratin in feathers of the blue-and-yellow macaw (Ara ararauna, Psittacidae) develop by intracellular self-assembly; the process proceeds in the absence of any biological prepattern created by the cell membrane, endoplasmic reticulum or cellular intermediate filaments. We examine the hypothesis that the shape and size of these self-assembled, intracellular nanostructures are determined by phase separation of b-keratin protein from the cytoplasm of the cell. The shapes of a broad sample of colourproducing channel-type nanostructures from nine avian species are very similar to those selfassembled during the phase separation of an unstable mixture, a process called spinodal decomposition (SD). In contrast, the shapes of a sample of spherical-type nanostructures from feather barbs of six species show a poor match to SD. However, spherical nanostructures show a strong morphological similarity to morphologies produced by phase separation of a metastable mixture, called nucleation and growth. We propose that colour-producing, intracellular, spongy medullary b-keratin nanostructures develop their characteristic sizes and shapes by phase separation during protein polymerization. We discuss the possible role of capillary flow through drying of medullary cells in the development of the hollow morphology of typical and spongy feather medullary cells.
Colour producing β-keratin nanofibres in blue penguin feathers
The colours of living organisms are produced by the differential absorption of light by pigments (e.g. carotenoids, melanins) and/or by the physical interactions of light with biological nanostructures, referred to as structural colours. Only two fundamental morphologies of non-iridescent nanostructures are known in feathers, and recent work has proposed that they self-assemble by intracellular phase separation processes. Here, we report a new biophotonic nanostructure in the non-iridescent blue feather barbs of blue penguins (Eudyptula minor) composed of parallel β-keratin nanofibres organized into densely packed bundles. Synchrotron small angle X-ray scattering and two-dimensional Fourier analysis of electron micrographs of the barb nanostructure revealed short-range order in the organization of fibres at the appropriate size scale needed to produce the observed colour by coherent scattering. These two-dimensional quasi-ordered penguin nanostructures are convergent with similar arrays of parallel collagen fibres in avian and mammalian skin, but constitute a novel morphology for feathers. The identification of a new class of β-keratin nanostructures adds significantly to the known mechanisms of colour production in birds and suggests additional complexity in their self-assembly.
Journal of the Royal Society Interface, 2012
Non-iridescent structural colours of feathers are a diverse and an important part of the phenotype of many birds. These colours are generally produced by three-dimensional, amorphous (or quasi-ordered) spongy b-keratin and air nanostructures found in the medullary cells of feather barbs. Two main classes of three-dimensional barb nanostructures are known, characterized by a tortuous network of air channels or a close packing of spheroidal air cavities. Using synchrotron small angle X-ray scattering (SAXS) and optical spectrophotometry, we characterized the nanostructure and optical function of 297 distinctly coloured feathers from 230 species belonging to 163 genera in 51 avian families. The SAXS data provided quantitative diagnoses of the channel-and sphere-type nanostructures, and confirmed the presence of a predominant, isotropic length scale of variation in refractive index that produces strong reinforcement of a narrow band of scattered wavelengths. The SAXS structural data identified a new class of rudimentary or weakly nanostructured feathers responsible for slate-grey, and blue-grey structural colours. SAXS structural data provided good predictions of the singlescattering peak of the optical reflectance of the feathers. The SAXS structural measurements of channel-and sphere-type nanostructures are also similar to experimental scattering data from synthetic soft matter systems that self-assemble by phase separation. These results further support the hypothesis that colour-producing protein and air nanostructures in feather barbs are probably self-assembled by arrested phase separation of polymerizing b-keratin from the cytoplasm of medullary cells. Such avian amorphous photonic nanostructures with isotropic optical properties may provide biomimetic inspiration for photonic technology.
Journal of The Royal Society Interface, 2012
Avian plumage colours are model traits in understanding the evolution of sexually selected ornamental traits. Paradoxically, iridescent structural colours, probably the most dazzling of these traits, remain the most poorly understood. Though some data suggest that expression of bright iridescent plumage colours produced by highly ordered arrays of melanosomes and keratin is condition-dependent, almost nothing is known of their ontogeny and thus of any developmental mechanisms that may be susceptible to perturbation. Here, we use light and electron microscopy to compare the ontogeny of iridescent male and non-iridescent female feathers in blue-black grassquits. Feather barbules of males contain a single layer of melanosomes bounded by a thin layer of keratin-producing blue iridescent colour, while those of females contain disorganized melanosomes and no outer layer. We found that nanostructural organization of male barbules occurs late in development, following death of the barbule cell, and is thus unlikely to be under direct cellular control, contrary to previous suggestions. Rather, organization appears to be caused by entropically driven self-assembly through depletion attraction forces that pin melanosomes to the edge of barbule cells and to one another. These forces are probably stronger in developing barbules of males than of females because their melanosomes are (i) larger, (ii) more densely packed, and (iii) more homogeneously distributed owing to the more consistent shape of barbules during keratinization. These data provide the first proposed developmental pathway for iridescent plumage colours, and suggest that any condition dependence of iridescent barbules is likely driven by factors other than direct metabolic cost.
Spatially modulated structural colour in bird feathers
Scientific reports, 2015
Eurasian Jay (Garrulus glandarius) feathers display periodic variations in the reflected colour from white through light blue, dark blue and black. We find the structures responsible for the colour are continuous in their size and spatially controlled by the degree of spinodal phase separation in the corresponding region of the feather barb. Blue structures have a well-defined broadband ultra-violet (UV) to blue wavelength distribution; the corresponding nanostructure has characteristic spinodal morphology with a lengthscale of order 150 nm. White regions have a larger 200 nm nanostructure, consistent with a spinodal process that has coarsened further, yielding broader wavelength white reflectance. Our analysis shows that nanostructure in single bird feather barbs can be varied continuously by controlling the time the keratin network is allowed to phase separate before mobility in the system is arrested. Dynamic scaling analysis of the single barb scattering data implies that the ph...
Nanostructure predicts intraspecific variation in ultraviolet–blue plumage colour
Proceedings of The Royal Society B: Biological Sciences, 2003
Evidence suggests that structural plumage colour can be an honest signal of individual quality, but the mechanisms responsible for the variation in expression of structural coloration within a species have not been identified. We used full-spectrum spectrometry and transmission electron microscopy to investigate the effect of variation in the nanostructure of the spongy layer on expression of structural ultraviolet (UV)-blue coloration in eastern bluebird (Sialia sialis) feathers. Fourier analysis revealed that feather nanostructure was highly organized but did not accurately predict variation in hue. Within the spongy layer of feather barbs, the number of circular keratin rods significantly predicted UV-violet chroma, whereas the standard error of the diameter of these rods significantly predicted spectral saturation. These observations show that the precision of nanostructural arrangement determines some colour variation in feathers.
Understanding the mechanistic bases of natural color diversity can provide insight into its evolution and inspiration for biomimetic optical structures. Metazoans can be colored by absorption of light from pigments or by scattering of light from biophotonic nanostructures, and these mechanisms have largely been treated as distinct. However, the interactions between them have rarely been examined. Captive breeding of budgerigars (Aves, Psittacidae, Melopsittacus undulatus) has produced a wide variety of color morphs spanning the majority of the spectrum visible to birds, including the ultraviolet, and thus they have been used as examples of hypothesized structure–pigment interactions. However, empirical data testing these interactions in this excellent model system are lacking. Here we used ultraviolet–visible spectrometry, light and electron microscopy, pigment extraction experiments and optical modeling to examine the physical bases of color production in seven budgerigar morphs, including grey and chromatic (purple to yellow) colors. Feathers from all morphs contained quasi-ordered air–keratin ʻspongy layerʼ matrices, but these were highly reduced and irregular in grey and yellow feathers. Similarly, all feathers but yellow and grey had a layer of melanin-containing melanosomes basal to the spongy layer. The presence of melanosomes likely increases color saturation produced by spongy layers whereas their absence may allow increased expression of yellow colors. Finally, extraction of yellow pigments caused some degree of color change in all feathers except purple and grey, suggesting that their presence and contribution to color production is more widespread than previously thought. These data illustrate how interactions between structures and pigments can increase the range of colors attainable in birds and potentially in synthetic systems.