Nanostructural self-assembly of iridescent feather barbules through depletion attraction of melanosomes during keratinization

Abstract

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.

Dietary protein level affects iridescent coloration in Anna's hummingbirds, Calypte anna

“…Currently, we do not know how the iridescent nanostructures themselves were affected by protein level in the diet and regrowth during the study, and future microscopic work is needed to examine the mechanisms by which different levels of dietary protein affected the organization or size of melanin or keratin nanostructural elements that produce the iridescent color that we measured spectrophotometrically. Higher concentrations of keratin or melanosomes or larger-sized melanosomes could lead to enhanced self-assembly and greater nanostructural organization (Maia et al, 2012). Spacing of certain nanostructural elements have been correlated with color differences among feathers in satin bowerbirds [Ptilonorhynchus violaceus (Doucet et al, 2006)], abdomens in damselflies (Fitzstephens and Getty, 2000) and wing scales in butterflies (Kemp et al, 2006), but changes in nanostructural organization as a result of experimental manipulation of a key component of feather nanostructure, i.e.…”

“…However, the size and concentration of melanosomes and the concentration of keratin molecules as well as costs associated with 'setting the stage' for self-assembly (e.g. cellular pH, hormones and availability of materials) likely represent costs for producing iridescent colors (Maia et al, 2012).…”

“…It may also affect the thickness or number of melanosomes because melanin production requires the amino acid tyrosine as a precursor (Fox, 1976). Keratin concentration and melanosome size and concentration could both affect self-assembly of iridescent nanostructures in feather barbules (Maia et al, 2012). Tyrosine can be obtained via protein in the diet or be synthesized from phenylalanine, which is an essential amino acid that must be derived from dietary protein.…”

“…costly to obtain, cannot be produced de novo, boost health (McGraw, 2006)], but it has been suggested that Protein affects hummingbird coloration producing precisely spaced, sized and aligned optical nanostructures may also be expensive in terms of materials and energy (reviewed in McGraw, 2008;Prum, 2006). New research on the development of iridescent feather barbules shows that the final organization of melanosomes within a keratin matrix is the result of entropic selfassembly (Maia et al, 2012). However, the size and concentration of melanosomes and the concentration of keratin molecules as well as costs associated with 'setting the stage' for self-assembly (e.g.…”

A window on the past: male ornamental plumage reveals the quality of their early-life environment

“…It is reasonable to expect a link between developmental environment and colourful traits. The long-term effects of developmental nutrition on morphology, physiology and metabolism can influence adult ability to assimilate the dietary pigments necessary for pigment-based coloration [9,10], and potentially also to form feather nanostructures necessary for structural coloration [11]. A number of studies have considered the immediate effects of developmental environment on nestling plumage colour [12 -15], demonstrating, for example, the importance of maternally invested egg yolk carotenoids for yellow plumage in nestling blue tits [16].…”