BIO 554/754
Ornithology

Feather evolution

Among the various integumentary structures of vertebrates, feathers are the most complex. Feathers are unique in their complex branching and impressive variation in size, shape, color, and texture (Prum 1999, Prum and Williamson 2001; Figure 1). Feathers were long considered the defining anatomical feature of birds. However, many specimens of non-avian dinosaurs have been discovered in China that show that feathers are not restricted to birds (Figure 2). Specifically, most non-avian coelurosaurian theropods appeared to have feathers, with coelurosaurs being relatively small (2 – 3 m long), carnivorous dinosaurs that occurred from the mid-Triassic through the early Jurassic (230 – 200 million years ago).

Figure 1. The two basic feather types are pennaceous and plumulaceous (or downy). Both types have a calamus. The pennaceous feather also has a rachis (or shaft) from which branches the barbs. Branching off of the barbs (upper right) are barbules. The hooklets of the barbules on the distal side of barbs interlock with the barbules on the proximal side of adjacent barbs. The ‘interlocked’ barbs on each side of the rachis form the feather vanes. The plumulaceous feather has numerous non-interlocked barbs extending from the calamus (From: Prum and Brush 2003).

Figure 2. Relationships among theropods, coelurosaurs (feathered dinosaurs), and present-day birds
(Source: http://www.zoology.ubc.ca/~bio336/Bio336/Lectures/Lecture5/Overheads.html).

In taxa more distantly related to birds, such as Sinosauropteryx (Figure 3 below), multiple tufts projecting a few millimeters from the skin have been discovered that resemble hypothesized early stages in avian feather development. These filamentous ‘feathers’ (or ‘protofeathers’; there is some disagreement concerning whether or not these integumentary structures were true feathers, e.g., Unwin 1998, Lingham-Soliar et al. 2007) were about 20 (5-40) mm long and appear to be rather homogenous over the body rather than originating in specific tracts. To some investigators, the filaments appear to be like down feathers and were probably used for insulation. They were hollow, and appeared to have a short shaft with barbs, but no barbules. In 2009, a fossil of another feathered dinosaur, Beipiaosaurus (a coelurosaurian theropod), with even simpler feathers was reported (Xu et al. 2009; Figures 4 and 5 below). These feathers consisted of single broad (about 2 mm wide) filament, were 10 to 15 centimeters long, and only present on the head, neck and tail. In taxa more closely related to birds, such as the oviraptorid Caudipteryx and dromaeosaurid Sinornithosaurus, elongate pinnate wing and tail feathers, structurally identical to the feathers of present-day birds and comprised of a central rachis, branching barbs, and barbules, have been found. In addition, fossils of a Dromaeosaurid (Microraptor) have revealed asymmetrically veined pennaceous feathers on both the forelimbs and hindlimbs (Clarke and Middleton 2006).

Figure 3. Restoration of a Sinosauropteryx (Sinosauropteryx prima) with its body covered with feathers that were likely important for thermoregulation
(From: Chuong et al. 2001, and based on Chen et al. 1998).

Figure 4. The elongated, single filament feathers of Beipiaosaurus. The yellow arrows point to feathers on the head and neck (right) and tail (above)
(From: Xu et al. 2009).

Figure 5. Artist’s conception of Beipiaosaurus, a dinosaur with broad, single-filament feather
(Image: Zhao Chuang and Xing Lida; source: http://blogs.discovermagazine.com/80beats/2009/01/13/to-attract-mates-this-dino-may-have-shaken-a-tail-feather/).

Cladogram illustrating the relationship of birds with major groups of non-avian coelurosaurian theropods. The numbers in circles at each branching node indicate the first appearance of feathers and other key morphological characters. 1, unbranched feathers; 2, uncinate processes on ribs; 3, true branched feathers; 4, retroverted pubis; 5, reversed hallux; 6, asymmetrical flight feathers; 7, pygostyle; 8, horny beak; 9, alula (bastard wing); 10, large, keeled sternum. Taxa indicated with an asterisk are known to have possessed either protofeathers or true feathers (From: Zhou et al. 2003).

Because birds evolved from reptiles and the integument of present-day reptiles (and most extinct reptiles including most dinosaurs) is characterized by scales, early hypotheses concerning the evolution of feathers began with the assumption that feathers developed from scales, with scales elongating, then growing fringed edges and, ultimately, producing hooked and grooved barbules (Figure 6 below). The problem with that scenario is that scales are basically flat folds of the integument whereas feathers are tubular structures. A pennaceous feather becomes ‘flat’ only after emerging from a cylindrical sheath (Prum and Brush 2002). In addition, the type and distribution of protein (keratin) in feathers and scales differ (Sawyer et al. 2000). The only feature shared by feathers and scales is that they both begin development as a morphologically distinct placode – an epidermal thickening above a condensation, or congregation, of dermal cells (see Figure 8 below). Feathers, then, are not derived from scales, but, rather, are evolutionary novelties with numerous unique features, including the feather follicle, tubular feather germ (an elevated area of epidermal cells), and a complex branching structure (Prum and Brush 2002; Figure 7 below).

Figure 6. Hypothetical intermediate stage in the evolution of feathers from scales, with ‘cracks’ separating sections of a large scales into smaller, lateral plates, or protobarbs (From: Regal 1975).

Feathers are branched structures. The main branch of a typical feather is the rachis, and barbs, consisting of a barb ramus and projections called barbules, branch off the rachis (Figure above from Prum and Brush 2003). Feathers grow from the base and the different branches are generated by various mechanisms in the feather follicle. Feather growth depends on nutrients provided via the follicular cavity (dermal pulp), and the feather structure develops on the follicular (or follicle) collar (inner epidermal layer; Figure 8 below). The production of the complex branched structure involves the interaction of several processes of cellular differentiation that occurs on the follicle collar (Calcott 2009). Among present-day birds, variation in the shape and structure of the rachis, barbs, and barbules generates a variety of feather types, including flight (contour) feathers, semiplumes, bristles, down feathers, filoplumes, and powder downs (Figure 7 below).

Figure 7. Various types of feathers of present-day birds, including the contour feather (left) plus filoplumes, semiplumes, down feathers, and bristles
(From: Lucas and Stettenheim 1972).

Figure 8. Schematic diagram of the development of a feather follicle. (A) Development of the epidermal feather placode and the dermal condensation. (B) Development of a feather papilla (or elongate feather bud) via the proliferation of dermal cells. (C) Formation of the feather follicle by the invagination of a cylinder of epidermal tissue around the base of the feather papilla. (D) Cross-section of the feather follicle as indicated by the dashed line in C. The follicle consists of a series of tissue layers (from peripheral to central), including the dermis of the follicle, the epidermis of the follicle (outer epidermal layer), the follicle cavity or lumen (the space between epidermal layers), the follicle (epidermal) collar (or inner epidermal layer), and the dermal pulp (tissue at the center of the follicle). The proliferation of feather keratinocytes and most of the growth of the feather occurs in the follicle, or epidermal, collar (From: Prum 1999).

Based on fossil evidence, we know that the first non-avian theropods with simple, single-filament feathers lived about 190 million years ago, and that non-avian theropods with feathers having a complex branching structure like those of present-day birds (pennaceous feathers) existed about 135 million years ago. This fossil evidence raises two important questions. First, if not derived from scales, how did feathers evolve and, second, how did simple, single-filament feathers evolve to become much more complex pennaceous feathers? Of course, a related question is, given that non-avian theropods did not fly, what function or functions did these feathers serve?

Both fossil and developmental evidence suggests that feathers evolved through a series of transitional stages, each the result of a developmental evolutionary novelty or, in other words, a new mechanism of growth (Prum 1999, Prum and Brush 2002, 2003). The first feathers, like those of Beipiaosaurus , were unbranched, hollow cylinders that developed from the tubular elongation (the feather germ) of a placode (Figure 9 below). The advantage of a tubular feather germ is that growth of a structure (in this case, a feather) can occur without an increase in the size of the skin itself (in contrast to, for example, scales; Prum 2005). An important step in the evolution of the first feathers was a change in characteristics of the placode. Both scales and feathers begin development from placodes, but feather development, in contrast to scale development, requires generation of suprabasal cell populations (dermal condensations) to form the follicle (see Figure 8 above). The development of placodes where dermal condensations occur, an evolutionary novelty, required changes in gene expression and timing. However, such changes are known to be an important mechanism in the origin of morphological innovations in many other organisms (True and Carroll 2002, Prum 2005).

Figure 9. The first feathers were likely hollow cylinders (Stage I) with undifferentiated collars that developed from an evolutionary novel follicle collar
(From: Prum and Brush 2003).

Based on Prum’s (1999) model of feather evolution, the next step after the origin of the feather follicle was the differentiation of the follicle collar into barb ridges to generate barbs (Stage II; Figure 10 below). The resulting feather would consist of a tuft of barbs extending from the calamus (Figure 10 below). Such a feather is hypothesized to have evolved before the origin of the rachis (Stage IIIA) because the rachis is initially formed by the fusion of barb ridges. In addition, barbs are hypothesized to evolve before barbules because barbules develop within layers of pre-existing barb ridges (Prum 1999). Feathers comparable in structure to hypothesized Stage II feathers have been reported from fossils of non-avian theropods, such as Sinornithosaurus mellenii (Figures 11 and 12 below; Xu et al. 2001, Norell and Xu 2005).

Figure 10. The next step in feather evolution (Stage II) involved the differentiation of the follicle collar into barb ridges to generated unbranched barbs (From: Prum and Brush 2003).

Figure 11. Filamentous integumental structure of Sinornithosaurus millenii with compound structures composed of multiple filaments. These structures exhibit two types of branching structure unique to avian feathers: the filaments are joined in a basal tuft, and the filaments are joined at their bases in series along a central filament. a, Arrows indicate the distal tips of some component filaments . b , Illustrated reconstruction of the appendage showing the positions of the observed filaments (lines) and the inferred outline of the appendage (shading). Asterisk, the proximal end of the appendage. The curved position of the appendage reveals its compound structure. Each filament converges on the centre of the appendage at its base. Scale bar, 5 mm (From: Xu et al. 2001).

Figure 12. Sinornithosaurus millenii , based on this skeletal drawing by Marco Auditore and others
(Source: Wikipedia; http://en.wikipedia.org/wiki/File:Sinornithosaurus.jpg).

The next step in feather evolution could have involved either the development of a rachis via fusion of barbs or the development of barbules that branched from the tufts of barbs. Perrichot et al. (2008) discovered feathers from the Early Cretaceous (and preserved in amber; Figure 15 below) that had shafts (rachis) consisting of incompletely fused, still distinguishable, partially superimposed barbs. This represents an intermediate stage between Prum’s (1999) stages II and IIIa and suggests the possibility that rachis development may have preceded barbule development (Figures 13 and 14 below).

Figure 13. Hypothesized stages I–III of feather evolution. Stage I of this model assumes an unbranched, hollow filament, which developed from a cylindrical invagination of the epidermis around a papilla. In stage II, a tuft was formed by fusion of several filaments at their bases. Stage III represents the formation of a central rachis and development of serially fused barbs (III A) — to which, at a slightly later stage (III B), secondary barbs (barbules) were added. The two other stages, IV (bipinnate feathers with elaborate barbules and a closed vane) and V (the asymmetrical flight feathers of modern flying birds), are not shown (From: Sues 2001).

Figure 14. The next step in feather evolution (Stage III) could have involved either the development of a rachis via fusion of barbs (3a) or the development of barbules that branched from the tufts of barbs (3b; From: Prum and Brush 2003). The discovery of feathers from the Early Cretaceous that had shafts (rachis) consisting of incompletely fused, still distinguishable, partially superimposed barbs suggests that that rachis development (3a) may have preceded barbule development (3b).

Figure 15. Three-dimensional virtual reconstruction of a fossil feather from the Early Cretaceous (about 100 million years ago) preserved in amber. This feather could be from either a bird or a non-avian theropod. (a-c) long barbs form two vanes on each side of a relatively flattened shaft; (d) the shaft is flattened and composed of incompletely fused bases of the barbs, a stage in feather evolution that was hitherto unknown in fossil records and corresponding to an intermediate stage between the very distinct stages II and IIIa defined by Prum (1999). Scale bars, 100 µm (From: Perrichot et al. 2008).

With the development of the rachis, the next stage in feather evolution would likely have been the development of barbules (without hooklets) to generate a bipinnate, open pennaceous structure (Stage 3a + b; Figure 16 below). Subsequent evolution of differentiated proximal and distal barbules would then generate the first closed, pennaceous vane, with distal barbules growing hooklets to attach to the simpler, grooved proximal barbules of the adjacent barb (Stage 4; Figure 16 below). Finally, lateral displacement of the new barb locus by differential new barb ridge addition to each side of the follicle led to the growth of a closed pennaceous feather with an asymmetrical vane resembling modern remiges (Stage 5; Figure 16 below).

Figure 16. Hypothesized final stages in the evolution of feathers like those of modern-day birds. T he development of barbules (without hooklets) generated a bipinnate, open pennaceous feather (Stage 3a + b), and evolution of differentiated proximal and distal barbules led to the first closed, pennaceous vane, with some barbules having hooklets to firmly attach to grooved barbules of the adjacent barb (Stage 4). Differential new barb ridge addition to each side of the follicle then led to the development of a closed pennaceous feather with an asymmetrical vane (Stage 5) (From: Prum and Brush 2003).

Evolution of feather function

 Early functional hypotheses for the origin of feathers focused on their importance for flight (Steiner 1917, Heilmann 1926). However, the discovery of filamentous (and pennaceous) feathers on flightless non-avian theropods provides clear evidence that feathers evolved before the origin of flight and that the first feathers did not serve an aerodynamic function. The earliest tuft-like feathers could have served a variety of functions, including insulation, heat shielding (Regal 1975), communication (Mayr 1960), crypsis (Prum 1999), water repellency (Dyck 1985), and defense (Prum 1999).

The first cylindrical, filamentous feathers (Stage I) could have provided insulation if they were sufficiently numerous. Feathers similar in morphology to that predicted for Stage I feathers have been found on fossils of Beipiaosaurus (a coelurosaurian theropod; Xu et al. 2009). These primitive feathers consisted of single broad (about 2 mm wide) filaments, about 10 to 15 centimeters long, and were only present on the head, neck and tail. Given their morphology and distribution on the body, these feathers likely did not serve a thermoregulatory function. Rather, their localized distribution and morphology (relatively long and probably rather stiff) suggest that they served as display structures (Xu et al. 2009). However, other types of filamentous feathers in non-avian theropods more likely served a thermoregulatory function (Norell and Xu 2005). For example, the presence of dense filamentous feathers on Sinosauropteryx suggests these theropods were endothermic, and that heat retention was the primary function of the feathers (Chen et al. 1998; Figure 17 below).

Figure 17. a. Fossil of Sinosauropteryx prima. b , Drawing of skeleton and feathers along the dorsal side and tail. Dark pigmentation in the abdominal region might be some soft tissues of the viscera (From: Chen et al. 1998).

The fossil of a pigeon-sized theropod, Epidexipteryx hui, found in sediments from the Middle to Late Jurassic (152 - 168 million years ago) of northern China revealed two pairs of elongate ribbon-like tail feathers that probably served as ornaments (although they could have also helped E. hui maintain balance when moving along tree branches; Figure 18 below). These long feathers had a central shaft (rachis) but, unlike the rectrices of present-day birds, the vanes were not branched into individual filaments. Rather, they consisted of a single ribbon-like sheet. Shorter feathers also covered the body and could have served as insulation (Zhang et al. 2008). At present, Epidexipteryx is the oldest theropod known to have feathers that apparently served a display function.

Figure 18. Artists’ conception of Epidexipteryx hui showing the paired ribbon-like tail feathers that likely served as ornaments and played a role in intra- and intersexual interactions. Illustration Credit: Zhao Chuang, Xing Lida/Nature.

 Pennaceous (or contour) feathers have been reported for a number of theropods, including the maniraptor Protarchaeopteryx (early Cretaceous; 120-122 million years ago), the oviraptorid Caudipteryx, and the dromaeosaurids Sinornithosaurus and Microraptor gui. Both Protarchaeopteryx and Caudipteryx had pennaceous feathers (with barbules) on the forearms and tail (as well as semiplumes and down-like feathers on the rest of the body). However, the arms of these small theropods (about 0.4-0.7 kg) were relatively short and all pennaceous feathers were symmetrical, indicating that these dinosaurs could not fly or glide effectively. Some investigators have suggested that these theropods, with relatively long legs and an elevated hallux, were ground-dwelling runners (Qiang et al. 1998). However, the forelimbs of Protarchaeopteryx and Caudipteryx, although short relative to their hindlimbs, were longer than those of other theropods and some investigators have argued that such elongation (along with other characteristics, including recurved claws) suggests a more (but not exclusive) arboreal lifestyle. For example, Chatterjee and Templin (2004) argued that these theropods were largely arboreal and that their small ‘protowings’ (in combination with the pennaceous feathers on the tail) enhanced arboreal maneuvering and permitted parachuting from branch to branch or from branch to ground (Figure 19 below). Feathers on the ‘protowings’ and tail would increase drag when parachuting and, to some extent, slow the rate of descent, permitting a safer landing. Another possible function of the forearm feathers is that could have been used to increase hindlimb traction in the same manner that some present-day birds, such as Chukar Partridges (Alectoris chukar), flap their wings to improve hindlimb traction when they climb inclined surfaces like the trunk of a tree (i.e., wing-assisted incline running; Dial 2003, Clarke and Middleton 2006).

Figure 19. Although incapable of powered flight, the pennaceous feather of Protarchaeopteryx may have permitted parachuting, whereas those of Sinornithosaurus likely permitted gliding (From: Chatterjee and Templin 2004).

Other small theropods from the early Cretaceous (124-128 million years ago), including Sinornithosaurus and M. gui, had both plumulaceous and pennaceous feathers. Sinornithosaurus weighed about 1.5 kg, were likely arboreal, and, in contrast to Protarchaeopteryx and Caudipteryx, their forelimbs were as long as their hindlimbs (Figure 12 above) . The longer wings and greater wing surface area, in combination with feathers on the tail (Figure 19 above), may have allowed Sinornithosaurus to glide between perches and from elevated perches to the ground (Chatterjee and Templin 2004).

M. gui was covered by plumulaceous feathers about 25–30 mm long and feathers on the top of the head were up to 40 mm long. Some feathers on the head were pennaceous and probably served a display function. Large, asymmetric pennaceous feathers were also attached to the distal tail, forelimb, and, surprisingly, the hindlimb. Microraptor had both primary and secondary flight feathers. This pattern was mirrored on the hind legs, with flight feathers attached to the upper foot bones as well as the upper and lower leg. When first described, Xu et al. (2003) proposed that Microraptor was arboreal and glided from tree to tree with four ‘wings’ – two forelimb wings and two hindlimb wings. However, Xu et al. (2003) proposed that the legs extended out to the side (Figure 20 below) and other investigators pointed out that such a leg position was unlikely because no known bird or theropod could extend their legs in such a manner without dislocating the hip joint (Padian 2003). Thereafter, Chatterjee and Templin (2007) proposed that the wings of Microraptor gui would have been split-level (like a biplane) and not spread as originally proposed, with the hindlimb flight feathers extending horizontally and able to generate lift along with the forelimb wings (Figure 21 below). Microraptor most likely employed a phugoid (from the Greek, meaning take flight) style of gliding flight - launching itself from a perch, swooping downward in a deep U-shaped curve, and moving upward to land on a perch in another tree (Figure 21 below).

Figure 20. A reconstruction of Microraptor gui in gliding flight (Xu et al. 2003).

 
The Four-winged Dinosaur

Check the PBS website for more information about The Four-winged Dinosaur

Figure 21. Top, teconstruction of M. gui in dorsal view (left) showing the morphology and distribution of hindlimb feathers and orientation of the hindlimb bones (above) during gliding. Above right, cross-section showing relative position of forelimb and hindlimb wings during gliding flight. Below right, a typical staggered biplane (Stearman 75) for comparison with Microraptor; in biplane aircraft of the 1920s, there was much additional drag generated by wires and struts between the two wings, such drag-induced structures were absent in Microraptor (Chatterjee and Templin 2007). Bottom, hypothetical flight path showing a typical undulating phugoid path from an initial take-off launch at a velocity of 3 meters per sec from a perch 20-m high and landing safely at a speed of about 6.4 meters per second (From: Chatterjee and Templin 2004).

 
Possible scenario for the development of feathers leading to the evolution of pennaceous feathers and flight. I and II, simple feathers possibly important for thermoregulation or display; III, with increasingly arboreal lifestyles, body feathers may have provided ancestors of birds with a more aerodynamic shape useful for leaping among branches; IV and V, simple pennaceous feather on the forelimbs may have allowed parachuting; VI, larger pennaceous feathers with symmetrical vanes may have permitted gliding; VII, asymmetrical feathers may have contributed to more efficient gliding; VIII, powered flight (From: Kurochkin and Bogdanovich 2008).

Current ideas about the evolution of feathers are based on dinosaurs (theropods) that actually lived well after Archaeopteryx. Hypothesized steps in the evolution of bird feathers are like those for the evolution of feathers in non-avian theropods (Graphic source: PBS - NOVA).

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