The evolutionary origin and diversification of feathers

Progress on the evolutionary origin and diversification of feathers has been hampered by conceptual problems and by the lack of plesiomorphic feather fossils. Recently, both of these limitations have been overcome by the proposal of the developmental theory of the origin of feathers, and the discovery of primitive feather fossils on nonavian theropod dinosaurs. The conceptual problems of previous theories of the origin of feathers are reviewed, and the alternative developmental theory is presented and discussed. The developmental theory proposes that feathers evolved through a series of evolutionary novelties in developmental mechanisms of the follicle and feather germ. The discovery of primitive and derived fossil feathers on a diversity of coelurosaurian theropod dinosaurs documents that feathers evolved and diversified in nonavian theropods before the origin of birds and before the origin of flight. The morphologies of these primitive feathers are congruent with the predictions of the developmental theory. Alternatives to the theropod origin of feathers are critique and rejected. Hypotheses for the initial function of feathers are reviewed. The aerodynamic theory of feather origins is falsified, but many other functions remain developmentally and phylogenetically plausible. Whatever their function, feathers evolved by selection for a follicle that would grow an emergent tubular appendage. Feathers are inherently tubular structures. The homology of feathers and scales is weakly supported. Feathers are composed of a suite of evolutionary novelties that evolved by the duplication, hierarchical organization, interaction, dissociation, and differentiation of morphological modules. The unique capacity for modular subdivision of the tubular feather follicle and germ has fostered the evolution of numerous innovations that characterize feathers. The evolution of feather keratin and the molecular basis of feather development are also discussed.     

Shh-Bmp2 signaling module and the evolutionary origin and diversification of feathers

To examine the role of development in the origin of evolutionary novelties, we investigated the developmental mechanisms involved in the formation of a complex morphological novelty-branched feathers. We demonstrate that the anterior-posterior expression polarity of Sonic hedgehog (Shh) and Bone morphogenetic protein 2 (Bmp2) in the primordia of feathers, avian scales, and alligator scales is conserved and phylogenetically primitive to archosaurian integumentary appendages. In feather development, derived patterns of Shh-Bmp2 signaling are associated with the development of evolutionarily novel feather structures. Longitudinal Shh-Bmp2 expression domains in the marginal plate epithelium between barb ridges provide a prepattern of the barbs and rachis. Thus, control of Shh-Bmp2 signaling is a fundamental component of the mechanism determining feather form (i.e., plumulaceous vs. pennaceous structure). We show that Shh signaling is necessary for the formation and proper differentiation of a barb ridge and that it is mediated by Bmp signaling. BMP signaling is necessary and sufficient to negatively regulate Shh expression within forming feather germs and this epistatic relationship is conserved in scale morphogenesis. Ectopic SHH and BMP2 signaling leads to opposing effects on proliferation and differentiation within the feather germ, suggesting that the integrative signaling between Shh and Bmp2 is a means to regulate controlled growth and differentiation of forming skin appendages. We conclude that Shh and Bmp signaling is necessary for the formation of barb ridges in feathers and that Shh and Bmp2 signaling constitutes a functionally conserved developmental signaling module in archosaur epidermal appendage development. We propose a model in which branched feather form evolved by repeated, evolutionary re-utilization of a Shh-Bmp2 signaling module in new developmental contexts. Feather animation Quicktime movies can be viewed at http://fallon.anatomy.wisc.edu/feather.html.     

Development and evolutionary origin of feathers

Avian feathers are a complex evolutionary novelty characterized by structural diversity and hierarchical development. Here, I propose a functionally neutral model of the origin and evolutionary diversification of bird feathers based on the hierarchical details of feather development. I propose that feathers originated with the evolution of the first feather follicle-a cylindrical epidermal invagination around the base of a dermal papilla. A transition series of follicle and feather morphologies is hypothesized to have evolved through a series of stages of increasing complexity in follicle structure and follicular developmental mechanisms. Follicular evolution proceeded with the origin of the undifferentiated collar (stage I), barb ridges (stage II), helical displacement of barb ridges, barbule plates, and the new barb locus (stage III), differentiation of pennulae of distal and proximal barbules (stage IV), and diversification of barbule structure and the new barb locus position (stage V). The model predicts that the first feather was an undifferentiated cylinder (stage I), which was followed by a tuft of unbranched barbs (stage II). Subsequently, with the origin of the rachis and barbules, the bipinnate feather evolved (stage III), followed then by the pennaceous feather with a closed vane (stage IV) and other structural diversity (stages Va-f). The model is used to evaluate the developmental plausibility of proposed functional theories of the origin of feathers. Early feathers (stages I, II) could have functioned in communication, defense, thermal insulation, or water repellency. Feathers could not have had an aerodynamic function until after bipinnate, closed pennaceous feathers (stage IV) had evolved. The morphology of the integumental structures of the coelurisaurian theropod dinosaurs Sinosauropteryx and Beipiaosaurus are congruent with the model's predictions of the form of early feathers (stage I or II). Additional research is required to examine whether these fossil integumental structures developed from follicles and are homologous with avian feathers. J. Exp. Zool. (Mol. Dev. Evol.) 285:291-306, 1999.Copyright 1999 Wiley-Liss, Inc.     

Feather function and the evolution of birds

The ability of feathers to perform many functions either simultaneously or at different times throughout the year or life of a bird is integral to the evolutionary history of birds. Many studies focus on single functions of feathers, but any given feather performs many functions over its lifetime. These functions necessarily interact with each other throughout the evolution and development of birds, so our knowledge of avian evolution is incomplete without understanding the multifunctionality of feathers, and how different functions may act synergistically or antagonistically during natural selection. Here, we review how feather functions interact with avian evolution, with a focus on recent technological and discovery-based advances. By synthesising research into feather functions over hierarchical scales (pattern, arrangement, macrostructure, microstructure, nanostructure, molecules), we aim to provide a broad context for how the adaptability and multifunctionality of feathers have allowed birds to diversify into an astounding array of environments and life-history strategies. We suggest that future research into avian evolution involving feather function should consider multiple aspects of a feather, including multiple functions, seasonal wear and renewal, and ecological or mechanical interactions. With this more holistic view, processes such as the evolution of avian coloration and flight can be understood in a broader and more nuanced context.     

A hierarchical model of plumage: morphology,development, and evolution

Plumage is a complex component of the avian phenotype. The plumage of an individual is composed of numerous hierarchically arranged developmental and morphological modules. We present a hierarchical model of plumage that provides an intellectual framework for understanding the development and evolution of feathers. Independence, covariation, and interaction among plumage modules create numerous opportunities for developmental and evolutionary diversification of feather complexity and function. The hierarchical relationships among plumage modules are characterized by both top-down and bottom-up effects in which properties of modules at one level of the hierarchy determine or influence the properties of modules at lower or higher levels of the hierarchy. Plumage metamodules are created by covariation or interaction among modules at different levels of the hierarchy.     

Review: cornification,morphogenesis and evolution of feathers

Feathers are corneous microramifications of variable complexity derived from the morphogenesis of barb ridges. Histological and ultrastructural analyses on developing and regenerating feathers clarify the three-dimensional organization of cells in barb ridges. Feather cells derive from folds of the embryonic epithelium of feather germs from which barb/barbule cells and supportive cells organize in a branching structure. The following degeneration of supportive cells allows the separation of barbule cells which are made of corneous beta-proteins and of lower amounts of intermediate filament (IF)(alpha) keratins, histidine-rich proteins, and corneous proteins of the epidermal differentiation complex. The specific protein association gives rise to a corneous material with specific biomechanic properties in barbules, rami, rachis, or calamus. During the evolution of different feather types, a large expansion of the genome coding for corneous feather beta-proteins occurred and formed 3–4-nm-thick filaments through a different mechanism from that of 8–10 nm IF keratins. In the chick, over 130 genes mainly localized in chromosomes 27 and 25 encode feather corneous beta-proteins of 10–12 kDa containing 97–105 amino acids. About 35 genes localized in chromosome 25 code for scale proteins (14–16 kDa made of 122–146 amino acids), claws and beak proteins (14–17 kDa proteins of 134–164 amino acids). Feather morphogenesis is periodically re-activated to produce replacement feathers, and multiple feather types can result from the interactions of epidermal and dermal tissues. The review shows schematic models explaining the translation of the morphogenesis of barb ridges present in the follicle into the three-dimensional shape of the main types of branched or un-branched feathers such as plumulaceous, pennaceous, filoplumes, and bristles. The temporal pattern of formation of barb ridges in different feather types and the molecular control from the dermal papilla through signaling molecules are poorly known. The evolution and diversification of the process of morphogenesis of barb ridges and patterns of their formation within feathers follicle allowed the origin and diversification of numerous types of feathers, including the asymmetric planar feathers for flight.     

The evolution of eyes and visually guided behaviour

The morphology and molecular mechanisms of animal photoreceptor cells and eyes reveal a complex pattern of duplications and co-option of genetic modules, leading to a number of different light-sensitive systems that share many components, in which clear-cut homologies are rare. On the basis of molecular and morphological findings, I discuss the functional requirements for vision and how these have constrained the evolution of eyes. The fact that natural selection on eyes acts through the consequences of visually guided behaviour leads to a concept of task-punctuated evolution, where sensory systems evolve by a sequential acquisition of sensory tasks. I identify four key innovations that, one after the other, paved the way for the evolution of efficient eyes. These innovations are (i) efficient photopigments, (ii) directionality through screening pigment, (iii) photoreceptor membrane folding, and (iv) focusing optics. A corresponding evolutionary sequence is suggested, starting at non-directional monitoring of ambient luminance and leading to comparisons of luminances within a scene, first by a scanning mode and later by parallel spatial channels in imaging eyes.     

Evolution of median fin modules in the axial skeleton of fishes

Detailed examples of how hierarchical assemblages of modules change over time are few. We found broadly conserved phylogenetic patterns in the directions of development within the median fins of fishes. From these, we identify four modules involved in their positioning and patterning. The evolutionary sequence of their hierarchical assembly and secondary dissociation is described. The changes in these modules during the evolution of fishes appear to be produced through dissociation, duplication and divergence, and co-option. Although the relationship between identified median fin modules and underlying mechanisms is unclear, Hox addresses may be correlated. Comparing homologous gene expression and function in various fishes may test these predictions.The earliest actinopterygians likely had dorsal and anal fins that were symmetrically positioned via a positioning module. The common patterning (differentiation) of skeletal elements within the dorsal and anal fins may have been set into motion by linkage to this positioning module. Frequent evolutionary changes in dorsal and anal fin position indicate a high level of dissociability of the positioning module from the patterning module. In contrast, the patterning of the dorsal and anal fins remains linked: In nearly all fishes, the endo- and exoskeletal elements of the two fins co-differentiate. In all fishes, the exoskeletal fin rays differentiate in the same directions as the endoskeletal supports, indicating complete developmental integration. In acanthopterygians, a new first dorsal fin module evolved via duplication and divergence. The median fins provide an example of how basic modularity is maintained over 400 million years of evolution.     

Evolving a Protofeather and Feather Diversity

It is likely that feathers evolved from a conical shaped tuberclerather than a plate-like structure. Although the morphologyof the presumably most primitive feather is unknown, minimalconditions for its production include the cellular capacityto synthesize feather proteins (=-keratin) which provides themolecular phenotype, and a follicular mechanism for productionand assembly of molecular and gross structure. Once the minimalstructural element, presumably recognizable as a barb, existed,a variety of phenotypes followed rapidly. A tubercular growthcenter of appropriate size could produce a simple barb-likeelement, with cortex and medulla. This might be recognized externallyas a bristle, but need never existed as a separate morphologicalunit. Rather, if individual placodes gave rise to multiple barbridges that fused proximally, a structure resembling natal downwould have resulted. Subsequent differentiation is controlledby the follicular symmetry, and the feather shape is regulatedby barb length. Barb length is directly related to growth period.As feathers appear to grow at roughly similar, size independentrates, shape is determined by individual barb growth periods.The simple fusion of individual proto-barbs would produce amorphology identifiable as natal down. Although this might bethe simplest feather structure, others could emerge quickly,perhaps simultaneously, a consequence of the same redundantprocessing. Once the machinery existed, broad phenotypic plasticitywas possible. I constructed a feather phylogram based on theseconditions, the fossil record, and ontogeny. I organized thesubsequent changes in morphology by perceived complexity. Thechanges are simply individual responses to similar processesthat might be time (when in ontogeny) and space (where on body)dependent.     

The biology of feather follicles

The feather is a complex epidermal organ with hierarchical branches and represents a multi-layered topological transformation of keratinocyte sheets. Feathers are made in feather follicles. The basics of feather morphogenesis were previously described (Lucas and Stettenheim, 1972). Here we review new molecular and cellular data. After feather buds form (Jiang et al., this issue), they invaginate into the dermis to form feather follicles. Above the dermal papilla is the proliferating epidermal collar. Distal to it is the ramogenic zone where the epidermal cylinder starts to differentiate into barb ridges or rachidial ridge. These neoptile feathers tend to be downy and radially symmetrical. They are replaced by teleoptile feathers which tend to be bilateral symmetrical and more diverse in shapes. We have recently developed a "transgenic feather" protocol that allows molecular analyses: BMPs enhance the size of the rachis, Noggin increases branching, while anti- SHH causes webbed branches. Different feather types formed during evolution (Wu et al., this issue). Pigment patterns along the body axis or intra-feather add more colorful distinctions. These patterns help facilitate the analysis of melanocyte behavior. Feather follicles have to be connected with muscles and nerve fibers, so they can be integrated into the physiology of the whole organism. Feathers, similarly to hairs, have the extraordinary ability to go through molting cycles and regenerate. Some work has been done and feather follicles might serve as a model for stem cell research. Feather phenotypes can be modulated by sex hormones and can help elucidate mechanisms of sex hormone-dependent growth control. Thus, the developmental biology of feather follicles provides a multi-dimension research paradigm that links molecular activities and cellular behaviors to functional morphology at the organismal level.     

The Evolution of Feathers*

Existing hypotheses on the evolution of feathers are reviewed with the assumptions that feather evolved from reptilian scales and that pennaceous feathers evolved before downy feathers. Observations with a scanning electron microscope demonstrate that basic to the structure of pennaceous feathers is the lamelliform structure of barbules, the planes of which are oriented at right angles to the plane of the feather vane. Thus the structure of the vane is more open than generally realized. The airtight vane of flight feathers is assumed a later specialization. Most of the existing hypotheses assume that the feather acts as a relatively solid barrier between the skin of the bird and the exterior and they are therefore not in agreement with the actual structure of feathers. A hypothesis is needed which explains the adaptive value of a pennaceous feather being porous. The hypothesis is put foward that feathers evolved due to selection for a water-repellent integument. For purely physical reasons a porous surface repels water drops more strongly than does a solid surface of the same material. Physicists have pointed out that the structure of feathers conforms closely with the theoretical requirements for water-repellency. Possibly feathers started to evolve on reptiles living at the seashore, where the main advantage of increased water-repellency was to reduce cooling from evaporation of water off a wet integument.     

Theory of the development of curved barbs and their effects on feather morphology

Feathers exhibit an extraordinary diversity of shapes, which are used by birds to accomplish a diverse set of functions. Pennaceous feathers have a double branched morphology that develops from a tube of epidermis, and variation in branch geometry determines feather shape. Feather development is both complex (i.e., a simple developmental modification can have multiple effects on mature feather shape), and redundant (i.e., different developmental modifications can create the same shape). Due to this, it is not readily apparent how different feather shapes develop. In many feathers, barbs are not straight, but instead curve in toward, or away, from the feather tip. Barb curvature can affect the shape of mature feathers but the development of curved barbs is unknown. Previous research has hypothesized that barb curvature could develop either during the helical growth of barb ridges in the tubular feather germ, or during barb angle expansion as the feather unfurls from the sheath. To better understand the development of curved barbs and their effects on mature feathers we present a theoretical model of curved barb development and test the model with empirical investigations of feathers. We find that curved barbs affect many aspects of feather morphology including vane width, barb length, and barb spacing. In real feathers, curved barbs can develop both during helical barb ridge growth and during barb angle expansion, with most of the observed curvature due to barb angle expansion. Our results demonstrate that barb angle expansion as a feather unfurls from the sheath is a complex and dynamic process that plays an important role in determining the shape and structure of mature feathers. Curved barbs create heterogeneity in barb geometry within the feather vane, which could have important implications for aerodynamic function and the development of within feather pigmentation patterns. J. Morphol. 277:995–1013, 2016. © 2016 Wiley Periodicals, Inc.     

Molecular biology of feather morphogenesis: a testable model for evo-devo research

Darwin's theory describes the principles that are responsible for evolutionary change of organisms and their attributes. The actual mechanisms, however, need to be studied for each species and each organ separately. Here we have investigated the mechanisms underlying these principles in the avian feather. Feathers comprise one of the most complex and diverse epidermal organs as demonstrated by their shape, size, patterned arrangement and pigmentation. Variations can occur at several steps along each level of organization, leading to highly diverse forms and functions. Feathers develop gradually during ontogeny through a series of steps that may correspond to the evolutionary steps that were taken during the phylogeny from a reptilian ancestor to birds. These developmental steps include 1) the formation of feather tract fields on the skin surfaces; 2) periodic patterning of the individual feather primordia within the feather tract fields; 3) feather bud morphogenesis establishing anterio-posterior (along the cranio-caudal axis) and proximo-distal axes; 4) branching morphogenesis to create the rachis, barbs and barbules within a feather bud; and 5) gradual modulations of these basic morphological parameters within a single feather or across a feather tract. Thus, possibilities for variation in form and function of feathers occur at every developmental step. In this paper, principles guiding feather tract formation, distributions of individual feathers within the tracts and variations in feather forms are discussed at a cellular and molecular level.     

Origin of feathers: Feather beta (beta) keratins are expressed in discrete epidermal cell populations of embryonic scutate scales

The feathers of birds develop from embryonic epidermal lineages that differentiate during outgrowth of the feather germ. Independent cell populations also form an embryonic epidermis on scutate scales, which consists of peridermal layers, a subperiderm, and an alpha stratum. Using an antiserum (anti-FbetaK) developed to react specifically with the beta (beta) keratins of feathers, we find that the feather-type beta keratins are expressed in the subperiderm cells of embryonic scutate scales, as well as the barb ridge lineages of the feather. However, unlike the subperiderm of scales, which is lost at hatching, the cells of barb ridges, in conjunction with adjacent cell populations, give rise to the structural elements of the feather. The observation that an embryonic epidermis, consisting of peridermal and subperidermal layers, also characterizes alligator scales (Thompson, 2001. J Anat 198:265-282) suggests that the epidermal populations of the scales and feathers of avian embryos are homologous with those forming the embryonic epidermis of alligators. While the embryonic epidermal populations of archosaurian scales are discarded at hatching, those of the feather germ differentiate into the periderm, sheath, barb ridges, axial plates, barbules, and marginal plates of the embryonic feather filament. We propose that the development of the embryonic feather filament provides a model for the evolution of the first protofeather. Furthermore, we hypothesize that invagination of the epidermal lineages of the feather filament, namely the barb ridges, initiated the formation of the follicle, which then allowed continuous renewal of the feather epidermal lineages, and the evolution of diverse feather forms.     

Morpho-regulation in diverse chicken feather formation: Integrating branching modules and sex hormone-dependent morpho-regulatory modules

Many animals can change the size, shape, texture and color of their regenerated coats in response to different ages, sexes, or seasonal environmental changes. Here, we propose that the feather core branching morphogenesis module can be regulated by sex hormones or other environmental factors to change feather forms, textures or colors, thus generating a large spectrum of complexity for adaptation. We use sexual dimorphisms of the chicken to explore the role of hormones. A long-standing question is whether the sex-dependent feather morphologies are autonomously controlled by the male or female cell types, or extrinsically controlled and reversible. We have recently identified core feather branching molecular modules which control the anterior-posterior (bone morphogenetic orotein [BMP], Wnt gradient), medio-lateral (Retinoic signaling, Gremlin), and proximo-distal (Sprouty, BMP) patterning of feathers. We hypothesize that morpho-regulation, through quantitative modulation of existing parameters, can act on core branching modules to topologically tune the dimension of each parameter during morphogenesis and regeneration. Here, we explore the involvement of hormones in generating sexual dimorphisms using exogenously delivered hormones. Our strategy is to mimic male androgen levels by applying exogenous dihydrotestosterone and aromatase inhibitors to adult females and to mimic female estradiol levels by injecting exogenous estradiol to adult males. We also examine differentially expressed genes in the feathers of wildtype male and female chickens to identify potential downstream modifiers of feather morphogenesis. The data show male and female feather morphology and their color patterns can be modified extrinsically through molting and resetting the stem cell niche during regeneration.     

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.     

Cell organization of barb ridges in regenerating feathers of the quail: implications of the elongation of barb ridges for the evolution and diversification of feathers

This ultrastructural study on the regenerating feathers of quail describes the cellular organization of the barb ridges responsible for the ramification of adult feathers. Bilateral symmetry of the barb ridges determines the organization of feather cells into feather branching. The length of the barb ridges, derived from the number of cells associated to form the barbule plates, determines the length of the barbule branching. Long chains of barb cells form long barbs that branch from the rachis with an increase of feather size. Supportive cells function as spacers between the barbule cells. New cells derive from stem cells localized in the collar region of the feather follicle, as indicated from the re‐organization of collar cells into barb ridges (a morphogenetic process inherited from that of embryonic feathers), production of an embryonic type of keratin (feather keratin), permanence of periderm granules (typical embryonic organelles) in barb vane ridge cells. Variations in the process of barb ridge morphogenesis allow the fusion of ridges into a rachis. The differentiation of hooklets contributes to the origin of planar feathers. Separation between rachis and merging barb ridges is by supportive cells, derived from the marginal plates of the barb ridges. Speculations on the evolution and diversification of feathers are presented.     

Enhancers,development, and evolution

A single-celled fertilized egg develops into a complex, multicellular animal through a series of selection processes of developmental pathways. During these processes, regulatory genes exhibit spatiotemporally restricted expression under the control of the species-specific genetic program, and dictate developmental processes from germ layer formation to cellular differentiation. Elucidation of molecular mechanisms underlying developmental processes and also of mechanistic bases for morphological diversification during evolution is one of the central issues in contemporary developmental biology. Progress has been made due to recent technological innovations, such as high-throughput nucleotide sequencing, live-cell imaging, efficient genetic manipulation, and establishment of the organoid system, opening new avenues to the above issues.