Adaptation to the sky: Defining the feather with integument fossils from mesozoic China and experimental evidence from molecular laboratories

In this special issue on the Evo-Devo of amniote integuments, Alibardi has discussed the adaptation of the integument to the land. Here we will discuss the adaptation to the sky. We first review a series of fossil discoveries representing intermediate forms of feathers or feather-like appendages from dinosaurs and Mesozoic birds from the Jehol Biota of China. We then discuss the molecular and developmental biological experiments using chicken integuments as the model. Feather forms can be modulated using retrovirus mediated gene mis-expression that mimics those found in nature today and in the evolutionary past. The molecular conversions among different types of integument appendages (feather, scale, tooth) are discussed. From this evidence, we recognize that not all organisms with feathers are birds, and that not all skin appendages with hierarchical branches are feathers. We develop a set of criteria for true avian feathers: 1) possessing actively proliferating cells in the proximal follicle for proximo-distal growth mode; 2) forming hierarchical branches of rachis, barbs, and barbules, with barbs formed by differential cell death and bilaterally or radially symmetric; 3) having a follicle structure, with mesenchyme core during development; 4) when mature, consisting of epithelia without mesenchyme core and with two sides of the vane facing the previous basal and supra-basal layers, respectively; and 5) having stem cells and dermal papilla in the follicle and hence the ability to molt and regenerate. A model of feather evolution from feather bud --> barbs --> barbules --> rachis is presented, which is opposite to the old view of scale plate --> rachis --> barbs --> barbules (Regal, '75; Q Rev Biol 50:35).     

Sexually dimorphic melanin‐based colour polymorphism,feather melanin content,and wing feather structure in the barn owl (Tyto alba)

Feathers confer protection against biophysical agents and determine flying ability. The geometry and arrangement of the barbs, together with the keratin and pigments deposited in the feathers, determine the mechanical stability of the vane, and its stiffness and resistance to abrasive agents. In colour‐polymorphic species, individuals display alternative colour morphs, which can be associated with different foraging strategies. Each morph may therefore require specific flying abilities, and their feathers may be exposed to different abrasive agents. Feathers of differently coloured individuals may thus have a specific structure, and colour pigments may help resist abrasive agents and improve stiffness. We examined these predictions in the barn owl (Tyto alba), a species for which the ventral body side varies from white to dark reddish pheomelanic, and in the number and size of black spots located at the tip of the feathers. White and reddish birds show different foraging strategies, and the size of black feather spots is associated with several phenotypic attributes. We found that birds displaying a darker reddish coloration on the ventral body side deposit more melanin pigments in their remiges, which also have fewer barbs. This suggests that wear resistance increases with darkness, whereas feathers of lighter coloured birds may bend less easily. Accordingly, individuals displaying a lighter reddish coloration on the ventral body side, and those displaying larger black spots, displayed more black transverse bars on their remiges: as larger‐spotted individuals are heavier and longer‐winged birds also have more transverse bars, these bars may reduce feather bending when flying. We conclude that differently coloured individuals produce wing feathers of different strengths to adopt alternative behavioural and life history strategies. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 562–573.     

Morphometry of auricular feathers of barn owls (Tyto alba)

In all owl species, the facial plumage forms a parabolic dish, the facial ruff, which is most conspicuous in the the barn owl (Tyto alba). The center of the ruff is formed by auricular feathers. Such feathers are also found on the preaural flaps which cover the ear openings, and in the region of the beak. In this study, we compare the different types of auricular feathers of the barn owl with contour feathers from the neck. Auricular feathers are characterised by an open vane structure and fewer barbs as compared to contour feathers. Auricular feathers also have fewer distal and proximal barbules than contour feathers. The open vane of the auricular feather results from an acute angle between the barb and the basis of the barbules, and from the extension of the pennula parallel to the barbs. These reductions are differently expressed in the three different types of auricular feathers investigated here and correspond with their function (protecting the ruff from dust).     

Feather iridescence of Coeligena hummingbird species varies due to differently organized barbs and barbules

Hummingbirds are perhaps the most exquisite bird species because of their prominent iridescence, created by stacks of melanosomes in the feather barbules. The feather colours crucially depend on the nanoscopic dimensions of the melanosome, and the displayed iridescence can distinctly vary, dependent on the spatial organization of the barbs and barbules. We have taken the genus Coeligena as a model group, with species having feathers that strongly vary in their spatial reflection properties. We studied the feather morphology and the optical characteristics. We found that the coloration of Coeligena hummingbirds depends on both the Venetian-blind-like arrangement of the barbules and the V-shaped, angular arrangement of the barbules at opposite sides of the barbs. Both the nanoscopic and microscopic organization of the hummingbird feather components determine the bird''s macroscopic appearance.     

Evolution of plumage coloration in the crow family (Corvidae) with a focus on the color-producing microstructures in the feathers: a comparison of eight species

Plumage coloration has been the subject for a variety of questions that comprise the center of modern evolutionary biology. Unlike carotenoids that the concentration directly influences the intensity of the color, melanin, in addition to produce brown or black colors, is often involved in producing the structural coloration such as glossiness or iridescence. As the melanin granules can be located in the barbs or the barbules, we aim to (i) discern if the colors observed at macro scale comes from the barbs, the barbules or both in a series of related species and (ii) estimate the evolutionary history of the color-producing mechanisms in the family Corvidae that are known to have melanin-based coloration. From a preliminary comparative analysis on eight representative species, we found three coloration schemes in Corvidae; (1) matte colors of brown or black that were produced in barbs and barbules; (2) non-iridescent structural colors such as blue, bluish gray and white, that were produced in the barbs and (3) iridescent structural colors that were produced only in distal barbules. Comparative character analysis of these coloration schemes suggests that the ancestral state among these species were the colors produced in the barbs and that the color produced in the distal barbules is a derived character. The evolution of iridescence seems tightly linked to the evolution of the colors produced in the distal barbules. Data from more species should be incorporated in order to grasp a full picture on the evolutionary history of plumage coloration in this group of birds.     

ON THE NATURE AND ORIGIN OF THE FEATHER COLOURATION IN THE GREAT WHITE PELICAN PELECANUS ONOCROTALUS ROSEUS IN ETHIOPIA

The yellow or orange-brown colour on the breast feathers and to a lesser extent on other feathers of the Great White Pelican in a breeding colony on an island in Lake Shala, Ethiopia, is due to the presence of ferric oxide.
The feathers most probably become stained when the birds are in the water, and the source of the ferric oxide may be iron–rich silt carried into the lake by the Gidu River.     

Structural coloration in a fossil feather

Investigation of feathers from the famous Middle Eocene Messel Oil Shale near Darmstadt, Germany shows that they are preserved as arrays of fossilized melanosomes, the surrounding beta-keratin having degraded. The majority of feathers are preserved as aligned rod-shaped eumelanosomes. In some, however, the barbules of the open pennaceous, distal portion of the feather vane are preserved as a continuous external layer of closely packed melanosomes enclosing loosely aligned melanosomes. This arrangement is similar to the single thin-film nanostructure that generates an iridescent, structurally coloured sheen on the surface of black feathers in many lineages of living birds. This is, to our knowledge, the first evidence of preservation of a colour-producing nanostructure in a fossil feather and confirms the potential for determining colour differences in ancient birds and other dinosaurs.     

BREEDING OF THE WHITE-BACKED AND RÜPPELL'S GRIFFON VULTURES, GYPS AFRICANUS AND G. RUEPPELLII

The breeding season of two species of griffon vultures are described. Rüppell's Griffon Vulture lays 2–3 months earlier than the White-backed Griffon. Young birds were hand-reared to determine their food requirements during growth; these estimates were combined with the food requirements of adult birds to make an estimate of the amount of food a parent bird needs to obtain when it is rearing young. The amount of food actually obtained by a group of birds was recorded from the size of the crops of birds returning to the breeding colony in the afternoon. The comparison of the estimates of the food obtained and the food required through the breeding season suggested that there may be a period during rearing when there was insufficient food available to satisfy the food requirements of both chick and adult. Chicks were found to have a very high survival rate and were probably receiving sufficient food. Presumably adult birds were not therefore receiving sufficient food, and the examination of a sample of adult birds for body condition through the breeding season showed a clear decline in their fat deposits. It was considered that in both species, breeding was timed so that the young left the nest at a period in the year when food conditions were good and the young birds could feed with little competition from adults. The parent birds therefore had to rear young during a season in the year when food conditions were not always adequate and they had to rely on utilising fat reserves. The food conditions for vultures during this study were probably favourable and during years of food shortage breeding may become impossible, or restricted to the most aggressive and dominant individuals.     

Adaptive allocation of stress-induced deformities on bird feathers

Physiological stress during ontogeny is known to cause abnormalities in keratin structures of vertebrates, but little is known about if and how organisms have evolved mechanisms to reduce the negative effects of these abnormalities. Stress experienced during avian feather growth is known to lead to the formation of fault bars, and thereby to the weakening of feathers because of shortage and slimming of barbules. Here we propose and test a new hypothesis (the 'fault bar allocation hypothesis') according to which birds should have evolved adaptive strategies to counteract this evolutionary pressure. In particular, we predicted and tested the idea that in flying birds, natural selection should have selected for mechanisms to reduce fault bar load on feathers with high strength requirements during flight. Data on the growth of feathers of nestling white storks (Ciconia ciconia) revealed a consistent allocation of more, and more intense, fault bars in innermost than in outermost wing feathers as predicted by our hypothesis. Moreover, the same pattern emerged from feathers of adult storks. We discuss the generality of our results, and suggest avenues for further investigations in this area.     

An alternate and reversible method for flight restraint of cranes

Flight restraint is important for zoos, safaris, and breeding centers for large birds. Currently used techniques for flight restraint include both surgical and non-surgical approaches. Surgical approaches usually cause permanent change to or removal of tendon, patagial membrane, or wing bones, and can cause pain and inflammation. Non-surgical approaches such as clipping or trimming feathers often alter the bird's appearance, and can damage growing blood feathers in fledglings or cause joint stiffness. We observed microstructure of primary feathers of the red-crowned crane (Grus japonensis) and found that the width of barbs is a determinative factor influencing vane stiffness and geometric parameters. We hypothesized that partial longitudinal excision of barbs on the ventral surface of the primary feathers would reduce the stiffness of the vane and render the feathers unable to support the crane's body weight during flight. Furthermore, we hypothesized that this modification of barbs would also change the aerodynamic performance of feathers such that they could not generate sufficient lift and thrust during flapping to enable the bird to fly. We tested this hypothesis on a red-crowned crane that had normal flight capability by excising the ventral margin of barbs on all 10 primaries on the left wing. The bird was unable to take off until the modified feathers were replaced by new ones. Removal of barbs proved to be a simple, non-invasive, low-cost and reversible method for flight restraint. It is potentially applicable to other large birds with similar structural characteristics of primary feathers.     

Vulture Genomes Reveal Molecular Adaptations Underlying Obligate Scavenging and Low Levels of Genetic Diversity

Obligate scavenging on the dead and decaying animal matter is a rare dietary specialization that in extant vertebrates is restricted to vultures. These birds perform essential ecological services, yet many vulture species have undergone recent steep population declines and are now endangered. To test for molecular adaptations underlying obligate scavenging in vultures, and to assess whether genomic features might have contributed to their population declines, we generated high-quality genomes of the Himalayan and bearded vultures, representing both independent origins of scavenging within the Accipitridae, alongside a sister taxon, the upland buzzard. By comparing our data to published sequences from other birds, we show that the evolution of obligate scavenging in vultures has been accompanied by widespread positive selection acting on genes underlying gastric acid production, and immunity. Moreover, we find evidence of parallel molecular evolution, with amino acid replacements shared among divergent lineages of these scavengers. Our genome-wide screens also reveal that both the Himalayan and bearded vultures exhibit low levels of genetic diversity, equating to around a half of the mean genetic diversity of other bird genomes examined. However, demographic reconstructions indicate that population declines began at around the Last Glacial Maximum, predating the well-documented dramatic declines of the past three decades. Taken together, our genomic analyses imply that vultures harbor unique adaptations for processing carrion, but that modern populations are genetically depauperate and thus especially vulnerable to further genetic erosion through anthropogenic activities.     

Continent-wide variation in feather colour of a migratory songbird in relation to body condition and moulting locality

Understanding the causes of variation in feather colour in free-living migratory birds has been challenging owing to our inability to track individuals during the moulting period when colours are acquired. Using stable-hydrogen isotopes to estimate moulting locality, we show that the carotenoid-based yellow-orange colour of American redstart (Setophaga ruticilla) tail feathers sampled on the wintering grounds in Central America and the Caribbean is related to the location where feathers were grown the previous season across North America. Males that moulted at southerly latitudes were more likely to grow yellowish feathers compared with males that moulted more orange-red feathers further north. Independent samples obtained on both the breeding and the wintering grounds showed that red chroma-an index of carotenoid content-was not related to the mean daily feather growth rate, suggesting that condition during moult did not influence feather colour. Thus, our results support the hypothesis that feather colour is influenced by ecological conditions at the locations where the birds moulted. We suggest that these colour signals may be influenced by geographical variation in diet related to the availability of carotenoids.     

Cytochemical and molecular characteristics of the process of cornification during feather morphogenesis

Feathers are the most complex epidermal derivatives among vertebrates. The present review deals with the origin of feathers from archosaurian reptiles, the cellular and molecular aspects of feather morphogenesis, and focus on the synthesis of keratins and associated proteins. Feathers consist of different proteins among which exists a specialized group of small proteins called beta-keratins. Genes encoding these proteins in the chick genome are distributed in different chromosomes, and most genes encode for feather keratins. The latter are here recognized as proteins associated with the keratins of intermediate filaments, and functionally correspond to keratin-associated proteins of hairs, nails and horns in mammals. These small proteins possess unique properties, including resistance and scarce elasticity, and were inherited and modified in feathers from ancestral proteins present in the scales of archosaurian progenitors of birds. The proteins share a common structural motif, the core box, which was present in the proteins of the reptilian ancestors of birds. The core box allows the formation of filaments with a different molecular mechanism of polymerization from that of alpha-keratins. Feathers evolved after the establishment of a special morphogenetic mechanism gave rise to barb ridges. During development, the epidermal layers of feathers fold to produce barb ridges that produce the ramified structure of feathers. Among barb ridge cells, those of barb and barbules initially accumulate small amounts of alpha-keratins that are rapidly replaced by a small protein indicated as “feather keratin”. This 10 kDa protein becomes the predominant form of corneous material of feathers. The main characteristics of feather keratins, their gene organization and biosynthesis are similar to those of their reptilian ancestors. Feather keratins allow elongation of feather cells among supportive cells that later degenerate and leave the ramified microstructure of barbs. In downfeathers, barbs are initially independent and form plumulaceous feathers that rest inside a follicle. Stem cells remain in the follicle and are responsible for the regeneration of pennaceous feathers. New barb ridges are produced and they merge to produce a rachis and a flat vane. The modulation of the growth pattern of barb ridges and their fusion into a rachis give rise to a broad variety of feather types, including asymmetric feathers for flight. Feather morphogenesis suggests possible stages for feather evolution and diversification from hair-like outgrowths of the skin found in fossils of pro-avian archosaurians.     

Size,plumage, moult and supposed hybrids of African Goshawks (Accipiter tachiro/toussenelii group) in DR Congo

Parapatric A. tachiro sparsimfasciatus and A. toussenelii canescens are in a size cline from large east African to small west African birds. While their plumage colour is different, the pattern of spotting (juvenile) and barring (adult) of the breast feathers is similar. No general hybridisation is found in the contact region in Kivu: the plumage of some aberrant individuals can be due to great age or to individual variation. One supposed hybrid was obtained far from the contact region. I consider them as paraspecies. Based on direct evidence and on annual moult I conclude that the breeding period is prolonged in both taxa in equatorial DR Congo, and that it is seasonal in tachiro sparsimfasciatus in southern DR Congo. In the latter population, the postjuvenile moult starts probably just before the age of one year but it lasts many months, leaving the juvenile upper tail coverts in place for one more year. Plumage characteristics are related to habitat. The female of the woodland sparsimfasciatus is cryptically coloured, with individual variation, possibly helpful for 'image avoidance'. The male is even more variable in colour, in part age related: a 'sepia' morph is described for the first adult plumage. Older birds are grey with reddish flanks, becoming darker with age. The adult evergreen forest canescens shows enforcement of colourful advertising plumage and loss of sexual plumage dimorphism. The first adult is advertised by the late moult of the barred juvenile flank feathers in both sexes. Its juvenile is peculiar; it lacks breast spots, suggesting image avoidance, but possibly also character displacement or mimicry.     

The louse Trinoton anserinum (Amblycera: Phthiraptera), an intermediate host of Sarconema eurycerca (Filarioidea: Nematoda), a heartworm of swans

The role of the louse Trinoton anserinum (F) as an intermediate host of Sarconema eurycerca (Wehr) was investigated in swans. 8.3% of healthy swans carried one to twelve lice per bird, dispersed contagiously. Injured and lead-poisoned swans were more heavily infected. The mouthparts appear designed to penetrate the hosts' skin; the mandibles are robust and asymmetric, and the maxillae have a serrated intercutting surface. 22% fed exclusively on blood and 33% on both blood and feather. All life-cycle stages fed upon blood and the barbs and barbules from down feathers; hooklets from contour feathers were only found in adults. 9% of lice were infected with developing nematode larvae in the head, thorax or abdomen. Lice labelled with Technetium 99 m moved towards the scapulas and the wings. Lice were found to be highly active and were mobile.     

On silver wings: a fragile structural mechanism increases plumage conspicuousness

We report for the first time the existence of a structural mechanism of feathers different from iridescence that makes plumage conspicuous. By using electron and light microscopy, we show that the mechanism consists of special lengthened and twisted distal barbules that are very susceptible to damage. The dorsal side of these barbules is translucent, which creates a distinctive sheen colouration to feathers that otherwise would be dark. When distal sheen barbules are broken, the black proximal barbules are exposed, thus generating a conspicuous difference between abraded and non-abraded areas. Total and ultraviolet reflectance of sheen (non-abraded) areas are strikingly higher than in abraded areas. We propose that this mechanism represents a case of convergent evolution in species that are limited in developing colourful plumage patches. Future studies should explore the potential of this colour mechanism to act as a signal of individual quality or identity.     

Variability and phylogenetic significance of detachable nodes in feathers of tinamous, galliforms and turacos

The occurrence of detachable nodal structures in the downy barbules of many birds was studied with light- and scanning electron microscopy. Anuli are the only type of nodal structure that may break loose and slide along the barbules to form dual or multiple nodes. Considerable variation exists in the occurrence of this feature. Multiple nodes are more frequently present in tail-coverts than in breast feathers. This is the first report of the presence of detachable anuli in feathers of Cracidae, Numididae and Musophagidae. The suggestion by earlier workers that these structures are characteristic for all galliforms is not confirmed, since megapodes never show detached nodes. The downy barbules of Afropavo resemble those of other phasianids in all respects, while those of Opisthocomus are strikingly different from both galliforms and cuckoos. Outgroup comparison indicates that multiple nodes may be synapomorphic for Tinamidae, Cracidae, Tetraonidae, Phasianidae, Numididae, Meleagridae and Musophagidae together, but, considering the incongruence of this hypothesis with recently proposed phylogenies, alternative explanations for the structural similarities between the downy barbules of tinamous, turacos and galliforms are discussed.     

Dramatic colour changes in a bird of paradise caused by uniquely structured breast feather barbules

The breast-plate plumage of male Lawes' parotia (Parotia lawesii) produces dramatic colour changes when this bird of paradise displays on its forest-floor lek. We show that this effect is achieved not solely by the iridescence--that is an angular-dependent spectral shift of the reflected light--which is inherent in structural coloration, but is based on a unique anatomical modification of the breast-feather barbule. The barbules have a segmental structure, and in common with many other iridescent feathers, they contain stacked melanin rodlets surrounded by a keratin film. The unique property of the parotia barbules is their boomerang-like cross section. This allows each barbule to work as three coloured mirrors: a yellow-orange reflector in the plane of the feather, and two symmetrically positioned bluish reflectors at respective angles of about 30°. Movement during the parotia's courtship displays thereby achieves much larger and more abrupt colour changes than is possible with ordinary iridescent plumage. To our knowledge, this is the first example of multiple thin film or multi-layer reflectors incorporated in a single structure (engineered or biological). It nicely illustrates how subtle modification of the basic feather structure can achieve novel visual effects. The fact that the parotia's breast feathers seem to be specifically adapted to give much stronger colour changes than normal structural coloration implies that colour change is important in their courtship display.     

Population dynamics of the bearded vulture Gypaetus barbatus in southern Africa

The essential features of mortality and survivorship of bearded vultures Gypaetus barbatus in southern Africa were deduced from age class plumage characteristics. The population consisted of about 204 adult pairs within a breeding range of about 35,000 sq km. Pairs bred every year and produced, on average, about 0·9 young per pair per year. Young birds made up about 37% of the population, subadults 3·5% and adults 60%. About 182 fledged young were recruited to the population each year. The proportion of young birds in the population in different areas was inversely related to the breeding density of adult birds (range 24–47%). Young bird mortality over the four years to subadult age was 87%, the survival rate of adults was 94% and the mean lifespan of birds surviving to adulthood was 21·4 years. This study demonstrates the need to understand the relationship between adult breeding density and young bird numbers in different parts of their range to accurately deduce population dynamics characteristics.