Frane Babarović

Structural coloration is widespread in animals, yet we know relatively little about its evolution and development. While previous studies have explored adaptive functions of structural color, a key gap is our lack of understanding of how historical contingency (path-dependency of biological processes) influences the loss and gain of this complex trait. We shed light on this question by describing feather nanostructures responsible for plumage colors in the cuckoos (family Cuculidae), a group with widespread occurrence of shiny, metallic plumage (metallic luster). The melanosomes found in feathers with metallic luster have specialized shapes: hollow rods, thin solid rods, hollow platelets, or solid platelets. In contrast, it is generally assumed that drably colored feathers possess thick, rod-shaped melanosomes. However, we uncover that this assumption is unfounded in cuckoos. We describe metallic luster in the plumages of 126 cuckoo species and map its phylogenetic distribution. This reveals that metallic luster is widespread in cuckoos but has likely been lost several times. We then use transmission electron microscopy to describe the feather nanostructures of 21 cuckoo species. Surprisingly, the drab feathers of many cuckoo species contain melanosomes with specialized shapes. We propose that historical contingency greatly influences nanostructure diversity in cuckoos. Specialized melanosome shapes can be retained in the plumages of drab species, potentially making it easier for metallic luster to evolve again in the future. This discovery supports the idea that historical contingency plays a key role in shaping the evolution of plumage color diversity.

3.1 Birds are one of the most colourful animal groups in the world and there are multiple ways by which they achieve this feature. Mechanisms of colour production range from pigmentary (pigment deposition) to structural (nanostructural arrangements), or the combination of both. Despite the huge breadth of colour gamut, the basic components of feathers are shared across all of them (keratin, air and presence of pigments in accordance with the colour produced). It has been shown that in some instances, colour evolution between pigmentary and structural colours can proceed by rearrangement of the nano-structural elements of feathers. Here, we investigated evolutionary transitions between pigmentary grey and non-iridescent structural blue. We focus on the Thraupidae (tanagers and allies) that display a variety of blues and greys including a potential transition state that we refer to as slate. We used digitally calibrated images of birds to quantify colour and determine the distinctiveness of slate colour in colourspace. Following, we identify the most likely pathway for the evolution of the colour blue: from grey via slate colour. Our research reveals a new pathway in the evolution of blue colour.

What drives the evolution of plumage color in birds? Bird color is likely to be under both natural and sexual selection where natural selection may favor evolution toward crypsis or camouflage whereas sexual selection may favor evolution toward conspicuousness. The responses to selection are predicted to relate to species’ ecology, behavior, and life history. Key hypotheses have focused on habitat and light environment, breeding strategy, territoriality, and hunting behavior. We tested these potential causes of color variation in the Coraciiformes, a colorful clade of non-passerine birds, using phylogenetic comparative methods and data on chromatic and achromatic properties of plumage coloration measured from museum specimens. We found that correlates of color evolution in Coraciiformes vary across body regions and depend on the focal color property (chromatic or achromatic properties of plumage coloration). While the light environment showed widespread effects on coloration in multiple body regions for both color properties, selection pressures related to behavioral characteristics had more spatially localized effects (e.g. territoriality on achromatic properties of wing feathers and hunting strategy on chromatic properties of belly feathers). Our results reveal both general patterns that may hold across other bird clades and more nuanced effects of selection that are likely to be mediated through the visual ecology of the signaler and receiver and the behavioral characteristics of Coraciiform species.

Non-iridescent structural colour in avian feathers is produced by coherent light scattering through quasi-ordered nanocavities in the keratin cortex of the barbs. To absorb unscattered light, melanosomes form a basal layer underneath the nanocavities. It has been shown that throughout Aves, melanosome morphology reflects broad categories of melanin-based coloration, as well as iridescence, allowing identification of palaeocolours in exceptionally preserved fossils. However, no studies have yet investigated the morphology of melanosomes in non-iridescent structural colour. Here, we analyse a wide sample of melanosomes from feathers that express non-iridescent structural colour from a phylogenetically broad range of extant avians to describe their morphology and compare them with other avian melanosome categories. We find that investigated melanosomes are typically wide (approx. 300 nm) and long (approx. 1400 nm), distinct from melanosomes found in black, brown and iridescent feathers, but overlapping significantly with melanosomes from grey feathers. This may suggest a developmental, and perhaps evolutionary, relationship between grey coloration and non-iridescent structural colours. We show that through analyses of fossil melanosomes, melanosomes indicative of non-iridescent structural colour can be predicted in an Eocene stem group roller ( Eocoracias : Coraciiformes) and with phylogenetic comparative methods the likely hue can be surmised. The overlap between melanosomes from grey and non-iridescent structurally coloured feathers complicates their distinction in fossil samples where keratin does not preserve. However, the abundance of grey coloration relative to non-iridescent structural coloration makes the former a more likely occurrence except in phylogenetically bracketed specimens like the specimen of Eocoracias studied here.