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1.  How hollow melanosomes affect iridescent colour production in birds 
Developmental constraints and trade-offs can limit diversity, but organisms have repeatedly evolved morphological innovations that overcome these limits by expanding the range and functionality of traits. Iridescent colours in birds are commonly produced by melanin-containing organelles (melanosomes) organized into nanostructured arrays within feather barbules. Variation in array type (e.g. multilayers and photonic crystals, PCs) is known to have remarkable effects on plumage colour, but the optical consequences of variation in melanosome shape remain poorly understood. Here, we used a combination of spectrophotometric, experimental and theoretical methods to test how melanosome hollowness—a morphological innovation largely restricted to birds—affects feather colour. Optical analyses of hexagonal close-packed arrays of hollow melanosomes in two species, wild turkeys (Meleagris gallopavo) and violet-backed starlings (Cinnyricinclus leucogaster), indicated that they function as two-dimensional PCs. Incorporation of a larger dataset and optical modelling showed that, compared with solid melanosomes, hollow melanosomes allow birds to produce distinct colours with the same energetically favourable, close-packed configurations. These data suggest that a morphological novelty has, at least in part, allowed birds to achieve their vast morphological and colour diversity.
doi:10.1098/rspb.2013.1505
PMCID: PMC3735262  PMID: 23902909
structural colour; morphospace; innovation; sexual selection; proximate mechanism
2.  Discovery of the Elusive Leptin in Birds: Identification of Several ‘Missing Links’ in the Evolution of Leptin and Its Receptor 
PLoS ONE  2014;9(3):e92751.
Leptin is a pleiotropic protein best known for regulation of appetite and fat storage in mammals. While many leptin orthologs have been identified among vertebrates, an authentic leptin in birds has remained elusive and controversial. Here we identify leptin sequence from the Peregrine falcon, Falco peregrinus (pfleptin), and identify sequences from two other birds (mallard and zebra finch), and ‘missing’ vertebrates (elephant shark, alligator, Indian python, Chinese soft-shelled turtle, and coelacanth). The pattern of genes surrounding leptin (snd1, rbm28) is syntenic between the falcon and mammalian genomes. Phylogenetic analysis of all known leptin protein sequences improves our understanding of leptin’s evolution. Structural modeling of leptin orthologs highlights a highly conserved hydrophobic core in the four-helix cytokine packing domain. A docked model of leptin with the leptin receptor for Peregrine falcon reveals several conserved amino acids important for the interaction and possible coevolution of leptin with its receptor. We also show for the first time, an authentic avian leptin sequence that activates the JAK-STAT signaling pathway. These newly identified sequences, structures, and tools for avian leptin and its receptor will allow elucidation of the function of these proteins in feral and domestic birds.
doi:10.1371/journal.pone.0092751
PMCID: PMC3963946  PMID: 24663438
3.  A photonic heterostructure produces diverse iridescent colours in duck wing patches 
The colours of birds are diverse but limited relative to the colours they can perceive. This mismatch may be partially caused by the properties of their colour-production mechanisms. Aside from pigments, several classes of highly ordered nanostructures (thin films, amorphous three-dimensional arrays) can produce a range of colours. However, the variability of any single nanostructural class has rarely been explored. Dabbling ducks are a speciose clade with substantial interspecific variation in the iridescent coloration of their wing patches (specula). Here, we use electron microscopy, spectrophotometry, polarization and refractive index-matching experiments, and optical modelling to examine these colours. We show that, in all species examined, speculum colour is produced by a photonic heterostructure consisting of both a single thin-film of keratin and a two-dimensional hexagonal lattice of melanosomes in feather barbules. Although the range of possible variations of this heterostructure is theoretically broad, only relatively close-packed, energetically stable variants producing more saturated colours were observed, suggesting that ducks are either physically constrained to these configurations or are under selection for the colours that they produce. These data thus reveal a previously undescribed biophotonic structure and suggest that both physical variability and constraints within single nanostructural classes may help explain the broader patterns of colour across Aves.
doi:10.1098/rsif.2012.0118
PMCID: PMC3405756  PMID: 22491981
photonic crystal; Anatidae; iridescence; thin films; sexual selection; nanophotonics
4.  Iridescent colour production in hairs of blind golden moles (Chrysochloridae) 
Biology Letters  2012;8(3):393-396.
Relative to other metazoans, the mammalian integument is thought to be limited in colour. In particular, while iridescence is widespread among birds and arthropods, it has only rarely been reported in mammals. Here, we examine the colour, morphology and optical mechanisms in hairs from four species of golden mole (Mammalia: Chrysochloridae) that are characterized by sheens ranging from purple to green. Microspectrophotometry reveals that this colour is weak and variable. Iridescent hairs are flattened and have highly reduced cuticular scales, providing a broad and smooth surface for light reflection. These scales form multiple layers of light and dark materials of consistent thickness, strikingly similar to those in the elytra of iridescent beetles. Optical modelling suggests that the multi-layers produce colour through thin-film interference, and that the sensitivity of this mechanism to slight changes in layer thickness and number explains colour variability. While coloured integumentary structures are typically thought to evolve as sexual ornaments, the blindness of golden moles suggests that the colour may be an epiphenomenon resulting from evolution via other selective factors, including the ability to move and keep clean in dirt and sand.
doi:10.1098/rsbl.2011.1168
PMCID: PMC3367760  PMID: 22279154
structural colour; biophotonics; hair
5.  Nanostructural self-assembly of iridescent feather barbules through depletion attraction of melanosomes during keratinization 
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.
doi:10.1098/rsif.2011.0456
PMCID: PMC3284138  PMID: 21865251
Asakura–Oosawa depletion model; biophotonics; honest signalling; sexual selection; thin-films
6.  Melanin Concentration Gradients in Modern and Fossil Feathers 
PLoS ONE  2013;8(3):e59451.
In birds and feathered non-avian dinosaurs, within-feather pigmentation patterns range from discrete spots and stripes to more subtle patterns, but the latter remain largely unstudied. A ∼55 million year old fossil contour feather with a dark distal tip grading into a lighter base was recovered from the Fur Formation in Denmark. SEM and synchrotron-based trace metal mapping confirmed that this gradient was caused by differential concentration of melanin. To assess the potential ecological and phylogenetic prevalence of this pattern, we evaluated 321 modern samples from 18 orders within Aves. We observed that the pattern was found most frequently in distantly related groups that share aquatic ecologies (e.g. waterfowl Anseriformes, penguins Sphenisciformes), suggesting a potential adaptive function with ancient origins.
doi:10.1371/journal.pone.0059451
PMCID: PMC3608712  PMID: 23555675
7.  Colour-producing β-keratin nanofibres in blue penguin (Eudyptula minor) feathers 
Biology Letters  2011;7(4):543-546.
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.
doi:10.1098/rsbl.2010.1163
PMCID: PMC3130216  PMID: 21307042
structural colour; nanofibres; biophotonics
8.  What makes a feather shine? A nanostructural basis for glossy black colours in feathers 
Colours in feathers are produced by pigments or by nanostructurally organized tissues that interact with light. One of the simplest nanostructures is a single layer of keratin overlying a linearly organized layer of melanosomes that create iridescent colours of feather barbules through thin-film interference. Recently, it has been hypothesized that glossy (i.e. high specular reflectance) black feathers may be evolutionarily intermediate between matte black and iridescent feathers, and thus have a smooth keratin layer that produces gloss, but not the layered organization of melanosomes needed for iridescence. However, the morphological bases of glossiness remain unknown. Here, we use a theoretical approach to generate predictions about morphological differences between matte and glossy feathers that we then empirically test. Thin-film models predicted that glossy spectra would result from a keratin layer 110–180 nm thick and a melanin layer greater than 115 nm thick. Transmission electron microscopy data show that nanostructure of glossy barbules falls well within that range, but that of matte barbules does not. Further, glossy barbules had a thinner and more regular keratin cortex, as well as a more continuous underlying melanin layer, than matte barbules. Thus, their quasi-ordered nanostructures are morphologically intermediate between matte black and iridescent feathers, and perceived gloss may be a form of weakly chromatic iridescence.
doi:10.1098/rspb.2010.1637
PMCID: PMC3107640  PMID: 21123257
biophotonics; iridescence; plumage colour; structural colour
9.  A Natural Experiment on the Condition-Dependence of Achromatic Plumage Reflectance in Black-Capped Chickadees 
PLoS ONE  2011;6(10):e25877.
Honest advertisement models posit that only individuals in good health can produce and/or maintain ornamental traits. Even though disease has profound effects on condition, few studies have experimentally tested its effects on trait expression and even fewer have identified a mechanistic basis for these effects. Recent evidence suggests that black and white, but not grey, plumage colors of black-capped chickadees (Poecile atricapillus) are sexually selected. We therefore hypothesized that birds afflicted with avian keratin disorder, a condition that affects the beak and other keratinized tissues, would show reduced expression of black and white, but not grey, color. UV-vis spectrometry of black-capped chickadees affected and unaffected by avian keratin disorder revealed spectral differences between them consistent with this hypothesis. To elucidate the mechanistic bases of these differences, we used scanning electron microscopy (SEM), electron-dispersive x-ray spectroscopy (EDX) and a feather cleaning experiment. SEM showed extreme feather soiling in affected birds, and EDX revealed that this was most likely from external sources. Experimentally cleaning the feathers increased color expression of ornamental feathers of affected, but not unaffected, birds. These data provide strong evidence that black and white color is an honest indicator in chickadees, and that variation in feather dirtiness, likely due to differences in preening behavior is a mechanism for this association.
doi:10.1371/journal.pone.0025877
PMCID: PMC3185041  PMID: 21991378
10.  Differential deposition of antimicrobial proteins in blue tit (Cyanistes caeruleus) clutches by laying order and male attractiveness 
Behavioral Ecology and Sociobiology  2010;64(6):1037-1045.
Female birds can influence offspring fitness by varying the relative quantities of egg components they deposit within and between clutches. Antimicrobial proteins (lysozyme, ovotransferrin, and avidin) are significant components of the avian albumen and likely aid in defense of embryos from microbial infection. Within clutches, females may enhance antimicrobial defense of early-laid eggs to protect them from the high risk of infection incurred before the onset of incubation. Among entire clutches, females may invest more resources in young sired by more attractive males because they have higher reproductive value. We tested these hypotheses by quantifying antimicrobial protein distribution within and among clutches in blue tit eggs. Contrary to our hypothesis, clutches showed no differential deposition of lysozyme or avidin within clutches, but eggs laid in the middle of the sequence had higher concentrations of ovotransferrin than eggs in the beginning and end. Consistent with our second hypothesis, we found that females produced eggs with higher concentrations of lysozyme (although not ovotransferrin or avidin) when mated to more attractive (more UV-reflective) males. Furthermore, females mated to polygynous males deposited less lysozyme than those mated to monogamous males. These data suggest that allocation of lysozyme at the clutch level may be a maternal effect mediated by male qualities.
doi:10.1007/s00265-010-0919-y
PMCID: PMC2854352  PMID: 20414331
Maternal effects; Antimicrobial proteins; Differential allocation; Egg infection
11.  A protean palette: colour materials and mixing in birds and butterflies 
Journal of the Royal Society Interface  2009;6(Suppl 2):S221-S231.
While typically classified as either ‘structural’ or ‘pigmentary’, bio-optical tissues of terrestrial animals are rarely homogeneous and typically contain both a structural material such as keratin or chitin and one or more pigments. These base materials interact physically and chemically to create colours. Combinations of structured base materials and embedded pigment molecules often interact optically to produce unique colours and optical properties. Therefore, to understand the mechanics and evolution of bio-optical tissues it is critical to understand their material properties, both in isolation and in combination. Here, we review the optics and evolution of coloured tissues with a focus on their base materials, using birds and butterflies as exemplar taxa owing to the strength of our current knowledge of colour production in these animals. We first review what is known of their base materials, and then discuss the consequences of these interactions from an optical perspective. Finally, we suggest directions for future research on colour optics and evolution that will be invaluable as we move towards a fuller understanding of colour in the natural world.
doi:10.1098/rsif.2008.0459.focus
PMCID: PMC2706479  PMID: 19141430
structural colour; pigments; photonics; refractive index
12.  Electron tomography, three-dimensional Fourier analysis and colour prediction of a three-dimensional amorphous biophotonic nanostructure 
Journal of the Royal Society Interface  2009;6(Suppl 2):S213-S220.
Organismal colour can be created by selective absorption of light by pigments or light scattering by photonic nanostructures. Photonic nanostructures may vary in refractive index over one, two or three dimensions and may be periodic over large spatial scales or amorphous with short-range order. Theoretical optical analysis of three-dimensional amorphous nanostructures has been challenging because these structures are difficult to describe accurately from conventional two-dimensional electron microscopy alone. Intermediate voltage electron microscopy (IVEM) with tomographic reconstruction adds three-dimensional data by using a high-power electron beam to penetrate and image sections of material sufficiently thick to contain a significant portion of the structure. Here, we use IVEM tomography to characterize a non-iridescent, three-dimensional biophotonic nanostructure: the spongy medullary layer from eastern bluebird Sialia sialis feather barbs. Tomography and three-dimensional Fourier analysis reveal that it is an amorphous, interconnected bicontinuous matrix that is appropriately ordered at local spatial scales in all three dimensions to coherently scatter light. The predicted reflectance spectra from the three-dimensional Fourier analysis are more precise than those predicted by previous two-dimensional Fourier analysis of transmission electron microscopy sections. These results highlight the usefulness, and obstacles, of tomography in the description and analysis of three-dimensional photonic structures.
doi:10.1098/rsif.2008.0374.focus
PMCID: PMC2706473  PMID: 19158016
biophotonics; structural colour; tomography; Fourier analysis; feathers
13.  Avian Incubation Inhibits Growth and Diversification of Bacterial Assemblages on Eggs 
PLoS ONE  2009;4(2):e4522.
Microbial infection is a critical source of mortality for early life stages of oviparous vertebrates, but parental defenses against infection are less well known. Avian incubation has been hypothesized to reduce the risk of trans-shell infection by limiting microbial growth of pathogenic bacteria on eggshells, while enhancing growth of commensal or beneficial bacteria that inhibit or competitively exclude pathogens. We tested this hypothesis by comparing bacterial assemblages on naturally incubated and experimentally unincubated eggs at laying and late incubation using a universal 16S rRNA microarray containing probes for over 8000 bacterial taxa. Before treatment, bacterial assemblages on individual eggs from both treatment groups were dissimilar to one another, as measured by clustering in non-metric dimensional scaling (NMDS) ordination space. After treatment, assemblages of unincubated eggs were similar to one another, but those of incubated eggs were not. Furthermore, assemblages of unincubated eggs were characterized by high abundance of six indicator species while incubated eggs had no indicator species. Bacterial taxon richness remained static on incubated eggs, but increased significantly on unincubated eggs, especially in several families of Gram-negative bacteria. The relative abundance of individual bacterial taxa did not change on incubated eggs, but that of 82 bacterial taxa, including some known to infect the interior of eggs, increased on unincubated eggs. Thus, incubation inhibits all of the relatively few bacteria that grow on eggshells, and does not appear to promote growth of any bacteria.
doi:10.1371/journal.pone.0004522
PMCID: PMC2639702  PMID: 19225566
14.  Evolutionary transitions and mechanisms of matte and iridescent plumage coloration in grackles and allies (Icteridae) 
Iridescent structural colour is found in a wide variety of organisms. In birds, the mechanisms that create these colours are diverse, but all are based on ordered arrays of melanin granules within a keratin substrate in barbules. The feathers of the grackles and allies in the family Icteridae range in appearance from matte black to iridescent. In a phylogenetic analysis of this clade, we identified several evolutionary transitions between these colour states. To describe a possible mechanistic explanation for the lability of plumage coloration, we used spectrometry, transmission electron microscopy and thin-film optical modelling of the feathers of 10 icterid species from five genera, including taxa with matte black or iridescent feathers. In matte black species, melanin was densely packed in barbules, while in iridescent species, melanin granules were arranged in ordered layers around the edges of barbules. The structured arrangement of melanin granules in iridescent species created optical interfaces, which are shown by our optical models to be critical for iridescent colour production by coherent scattering. These data imply that rearrangement of melanin granules in barbules is a mechanism for shifts between black and iridescent colours, and that the relative simplicity of this mechanism may explain the lability of plumage colour state within this group.
doi:10.1098/rsif.2006.0131
PMCID: PMC1885357  PMID: 17015306
structural colour; sexual selection; cowbirds; plumage colour; thin-film
15.  An experimental test of the contributions and condition dependence of microstructure and carotenoids in yellow plumage coloration 
A combination of structural and pigmentary components is responsible for many of the colour displays of animals. Despite the ubiquity of this type of coloration, neither the relative contribution of structures and pigments to variation in such colour displays nor the relative effects of extrinsic factors on the structural and pigment-based components of such colour has been determined. Understanding the sources of colour variation is important because structures and pigments may convey different information to conspecifics. In an experiment on captive American goldfinches Carduelis tristis, we manipulated two parameters, carotenoid availability and food availability, known to affect the expression of carotenoid pigments in a full-factorial design. Yellow feathers from these birds were then analysed in two ways. First, we used full-spectrum spectrometry and high-performance liquid chromatography to examine the extent to which variation in white structural colour and total carotenoid content was associated with variation in colour properties of feathers. The carotenoid content of yellow feathers predicted two colour parameters (principal component 1—representing high values of ultraviolet and yellow chroma and low values of violet–blue chroma—and hue). Two different colour parameters (violet–blue and yellow chroma) from white de-pigmented feathers, as well as carotenoid content, predicted reflectance measurements from yellow feathers. Second, we determined the relative effects of our experimental manipulations on white structural colour and yellow colour. Carotenoid availability directly affected yellow colour, while food availability affected it only in combination with carotenoid availability. None of our manipulations had significant effects on the expression of white structural colour. Our results suggest that the contribution of microstructures to variation in the expression of yellow coloration is less than the contribution of carotenoid content, and that carotenoid deposition is more dependent on extrinsic variability than is the production of white structural colour.
doi:10.1098/rspb.2006.3675
PMCID: PMC1639519  PMID: 17015356
American goldfinch; Carduelis tristis; carotenoid pigmentation; diet; honest signalling; sexual selection
16.  Mechanisms of evolutionary change in structural plumage coloration among bluebirds (Sialia spp.) 
Combinations of microstructural and pigmentary components of barbs create the colour displays of feathers. It follows that evolutionary changes in colour displays must reflect changes in the underlying production mechanisms, but rarely have the mechanisms of feather colour evolution been studied. Among bluebirds in the genus Sialia, male rump colour varies among species from dark blue to light blue while breast colour varies from blue to rusty. We use spectrometry, transmission electron microscopy and Fourier analysis to identify the morphology responsible for these divergent colour displays. The morphology of blue rump barbs is similar among the three species, with an outer keratin cortex layer surrounding a medullary ‘spongy layer’ and a basal row of melanin granules. A spongy layer is also present in blue breast barbs of mountain bluebirds Sialia currucoides and in rusty breast barbs of western Sialia mexicana and eastern bluebirds Sialia sialis. In blue barbs melanin is basal to the spongy layer, but is not present in the outer cortex or spongy layer, while in rusty barbs, melanin is present only in the cortex. The placement of melanin in the cortex masks expression of structural blue, creating a rusty display. Such shifts in microstructures and pigments may be widespread mechanisms for the evolutionary changes in the colours of feathers and other reflective structures across colourful organisms.
doi:10.1098/rsif.2006.0111
PMCID: PMC1664640  PMID: 16849249
structural colour; pigmentary colour; Fourier analysis; coherent light scattering
17.  Carotenoids need structural colours to shine 
Biology Letters  2005;1(2):121-124.
The bright colours of feathers are among the most striking displays in nature and are frequently used as sexual signals. Feathers can be coloured by pigments or by ordered tissue, and these mechanisms have traditionally been treated as distinct modes of display. Here we show that some yellow plumage colour is created both by reflection of light from white structural tissue and absorption of light by carotenoids. Thus, structural components of feathers contribute substantially to yellow ‘carotenoid’ displays, but the effect of variation in structural components on variation in colour displays is, to our knowledge, unstudied. The presence of structural colour in some carotenoid-based colour displays will have to be considered in studies of colour signalling.
doi:10.1098/rsbl.2004.0289
PMCID: PMC1626226  PMID: 17148144
plumage colour; nanostructure; sexual selection; honest signalling
18.  Nanostructure predicts intraspecific variation in ultraviolet-blue plumage colour. 
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.
doi:10.1098/rspb.2003.2390
PMCID: PMC1691395  PMID: 12965009

Results 1-18 (18)