JOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 285:291–306 (1999) - PDF document

JOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 285:291–306 (1999)© 1999 WILEY-LISS, INC.Department of Ecology & Evolutionary Biology, and Natural HistoryAvian feathers are a complex evolutionary novelty characterized by structuraldrical epidermal invagination around the base of a dermal papilla. A transition series of folliclequently, with the origin of the rachis and barbules, the bipinnate feather evolved (stage III), followedVa–f). The model is used to evaluate the developmental plausibility of proposed functional theo-defense, thermal insulation, or water repellency. Feathers could not have had an aerodynamic andare congruent with the model’s predictions of the form of early feathers (stage I orII). Additional research is required to examine whether these fossil integumental structures devel-J. Exp. Zool. (Mol. Dev. Evol.) 285:291–© 1999 Wiley-Liss, Inc. Received 9 June 1999; Accepted 3 September 1999Avian feathers are a premier example of a com-plex evolutionary novelty. The evolutionary ori-gin of by the lack of any known ancestral feather mor-pletely modern form (de Beer, ’54; Griffiths, ’96).lack of consensus about the morphology of the ear-feather morphology.Subsequently, theories about the origin of feath- 292R.O. PRUM(Mayr, ’60), and water repellency (Dyck, ’85).create the novelty (Müller and Wagner, ’91)? A richcomplex mechanisms of feather development. Al-themselves Recently, Brush (’93, ’96) emphasized the dif--keratins, feather morphology, and feather devel-genomic, molecular, developmental, and morpho-logical levels. Subsequently, Brush (’99a,b,c) hascomplexity. Brush (’99a,b,c) proposes that feath-classes of feather morphology.novelties in the history of feather evolution. Thevelopment are inferred from the hierarchical or-ganization of events in feather development, or,in some instances, by the physical necessity of aevents (Müller and Wagner, ’91). In the discus-mentally plausible. Also, I discuss the congruenceOVERVIEW OF FEATHER STRUCTURETHER STRUCTUREnology, morphology, and development is based onadditional details are specifically referenced.] Athe feather. The primary branches of the rachis DEVELOPMENT AND ORIGIN OF FEATHERS293cells of the base and ending with a series of longer,proximal barbules, respectively.pennulae of the distal barbules and the simpler,such as plants, feathers do not grow from bifur-later, and, ultimately, the calamus is producedcommunication between the dermis and epider-mis (Sengel, ’76; Wolpert, ’98). With few excep-a bird’s life develop during the first 12 days of lifefrom the epidermal placode produces a finger-likean outer dermal layer, an outer epidermal layer,a follicle cavity or lumen between the two epider-mal layers, an inner epidermal layer, and the der-Virtually all feather growth takes place within Fig. 1.(feather with afterfeather. ( 294R.O. PRUM Earlier Position of New Barb Locus Rachis Later Two Laterally Displaced out of the collar by younger, more basal cells pro-liferating below. Gradually, older, more superficialmature feather.by differentiation within the follicle collar. Thesheath of the emerging feather. The inner layerof the growing feather.older, more superficial cells. Rather, they are dis- feather placodeepidermisdermis dermal condensationepidermisdermal papillafollicular cavitydermal pulpepidermal collarepidermisdermisdermisdermis of follicleepidermis of folliclefollicular cavitydermal pulpepidermal collar BCD Fig. 2.Schematic diagram of the development of a feathera series of tissue layers (from peripheral to central): the der-mis of the follicle, the epidermis of the follicle (outer epider-of the feather takes place in the follicular collar.Fig. 3.Diagram of helical displacement of barb ridgesafterfeather (from Lucas and Stettenheim, ’72). Initially, barbthe collar and are gradually displaced, as they grow, aroundto form the rachis and vane of the afterfeather. A mature DEVELOPMENT AND ORIGIN OF FEATHERS295tation of the vane of the mature feather.] As afollicle where they fuse to the largest, anterior-comes the rachis of the emerging feather. NewAs new barb ridges are formed, the follicle may in-crease in diameter. From the new barb locus, barbwithin tral axis. The peripheral cells in the paired bar-vertical displacement, the distal cells of the bar-the barbules grow.the follicle decreases in diameter, and the last barbridges fuse to the rachis ridge. Ultimately, the col-the emerging feather. The center of the tubularbasilar layer of the epidermal collar. The com-commonly called a pin feather. Only after the cy-obtain its mature planar, pennaceous, orfeather, the hooked pennulae of the distal barbulesof the fully emerged feather, whereas the inter-within the barb ridges of the follicle. Further, thelar. This displacement likely occurs through dif-new barb locus to one side of the follicle collar,since asymmetrical vanes are created by differ-Feathers in many birds also have an after-feather, which is a composed of a second rachisthe barbs of the main feather, whereas barb ridgesfollicle collar, and fuse to form the rachis andEach follicle produces a series of feathers dur- 296R.O. PRUMfeathers is not a consequence of variation in theBird feathers are usually molted once a year, com-monly twice a year, and occasionally once everyother year. With each molt, the follicle resumes ac-tivity, the collar becomes reorganized into a prolif-metry, size, and color emerges. Feathers with a largeand pulp reorganize. However, the structural con-A DEVELOPMENTAL MODEL OFFEATHER EVOLUTIONFig. 4.Developmental model of the origin and diversifi- but both are required before stage IV. Stage IIIa: Origin offerentiation. Stage IV: Origin of differentiated distal andVa: Origin of lateral displacement of the new barb ridge lo- DEVELOPMENT AND ORIGIN OF FEATHERS297The follicle originated with the cylindrical epider-calamus, or sheath, of a modern feather.The inner, basilar layer of the collar differenti-first. Both are required prior to stage IV. The evo-on the anterior midline of the follicle. To create athe posterior new barb locus evolved thereafter. Stage IIIa Stage IIIbStage IIIa+b Stage II Stage Vb Stage Va Stage IV: The origin of differentiated proximal and distal bar-bules created the first closed, pennaceous vane. Distal bar-simpler proximal barbules of the adjacent barb. Stage Va:lical displacement producing a main feather and an after-after stage IV based on modern aftershaft morphology. SeeFig. 5.Developmental model of the origin and diversifi-modern feather. Stage II: The origin of a collar with differen- 298R.O. PRUMIIIb, the feather possessed an open pennaceousTerminally hooked pennulae on the distal barbulesfeather, subsequent developmental novelties gaverise to additional structural diversity. Asymmetri-collar toward either side (stage Va). Vane asym-Va, these asymmetrical feathers could not haveIV, based on modern afterfeather morphology.Additional feather diversity, including filo-feathers that are characterized by elongate bar-within barbule plates (stage Ve). The differentia-tion and programmed death of the axial and mar-(Lucas and Stettenheim, ’72, p 386–387). Avianpinnate barbs evolved. With the evolution of heli- DEVELOPMENT AND ORIGIN OF FEATHERS299to the rest of feather diversity, including asym-metrical flight feathers, the afterfeather, and mostmodern downs (stage Va–f).create the closed pennaceous vane. The after-derived contour feathers of the flightless Australo-the main feather is equal in length to the after-feather. A few novelties, such as the origin of he-, Ardeidae) and birds of paradiseavailable from modern birds. However, the vari-locus, then stage IIIa would have been composedlution of paired barbules. There are, however, noextant feathers that have this morphology. Asym-metrical feather vanes (stage Va) could also havetures grown by modern feather follicles, it wouldelties in the model are congruent with von Baer’srule—the hypothesis that stages that occur ear-(e.g., Gould, ’77). However, the model does not relybirds is usually downy, but because the simplest 300R.O. PRUMplumulaceous feathers. One detail, however, offeather development appears to violate von Baer’spapillae formed (Lucas and Stettenheim, ’72). However, thisthe spatial organization provided by the collar.terestingly, the cylindrical shape of the follicle didnot constrain the morphology of feathers. Rather,however, requires a reevaluation of the homologyan elongate papilla with an established anterior-posterior axis (Fig. 2A, B). However, with the ori-Recently, Alan Brush (’99a,b,c) has investigatedbiochemical, cellular, and developmental view-point. Brush’s analysis independently supportsthe protofeather was a single, unbranched hollowbristle feather. Subsequently, Brush (’99b) pro-based on feather growth, biochemistry, and thevery rapidly within evolutionary history.follicle as hypothesized by Brush (’99a). Further-more, Brush’s combined biochemical and morpho-fore they are considered as feathers. Accordingly, could not be de--keratin. Although feather DEVELOPMENT AND ORIGIN OF FEATHERS301Brush’s phylogram of feather diversity (’99b) isdrical form of the earliest feather, that theplumulaceous form preceeded pennaceous mor-phology, and the flight feathers are highly derived.But Brush’s hypothesis describes historical rela-natal down, semiplumes, etc.). As mentioned pre-viously, however, many extant feathers are char-rived pennaceous feathers. To avoid conflating themodern birds. Further, Brush’s (’99a,b) descrip-portions of the collar. Barbs evolved through theters that created the first feather, as implied byever, the presence of complex developmentalply that these mechanisms evolved rapidly, simul-taneously, or as an automatic consequence of theture. We have no evidence regarding how easy ordevelopmental apomorphies that led to the diver-sity of feather morphologies (Figs. 4 and 5). Cur-rent evidence is insufficient to support Brush’svolves the periodic cessation of growth and disor-resumption of growth of a new feather. The emerg-diversity.stage of the evolution of feather complexity. Themodel, however, does make specific predictionsand it is possible to evaluate whether the mor-scales became elongate and planar, then fringed,lection for increasing aerodynamic efficiency. Theaerodynamic hypothesis, however, is basically in-the details of 302R.O. PRUMfunction during all stages of its evolution, from scaleto modern asymmetrical pennaceous flight feather.However, the vane of a pennaceous feather is notsurfaces of the follicle collar, respectively, and can-emergence, all feathers are cylindrical. Any sce-present. Thus, it was impossible for the featherpass through a stage in which a generally undif-ferentiated collar was split along the posteriorformed by fusion of barb ridges, and that differ-licle (stage Va). Feathers evolved an aerodynamiccomplexity.cal nature of the follicle. Further, the bipinnate(stage Va).thin, numerous, and pliable like mammalian hair.shield from excessive solar radiation. As in themechanism. It is conceivable, however, that theWater repellencythrough natural selection for water repellency. The(stage II) could have functioned in that capacity. DEVELOPMENT AND ORIGIN OF FEATHERS303cation (Mayr, ’60). It is also plausible that feathersstripes or longitudinal gradients in color. The more (Chen et al., ’98) has caused consid- have received considerable scru-tiny, but many questions about their morphologyor unbranched filaments; whether they are hol-more recent discovery of similar but much longerin function since common ancestry. Unfortunately,current theories of feather origins directly incor-the origin of the branched or pennaceous feather. indi-ing created by closely adjacent, separate un-branched filaments within the specimens. However,were not internal integumental structures. Addi- and -keratin. Current descriptions of the mor- (Chen et al., ’98) and 304R.O. PRUMand tyrannosaurs. and (Ji etor merely notable depends upon whether these or- are the sister taxa to birds (Ji et al., and were plesio- and to theropod dinosaurs and and areThe proposed model provides a new, coherent, andtesting these hypotheses of homology. In theseWith the discovery of new molecular methods indevelopmental biology, feather development hastigation (Chuong, ’93; Wolpert, ’98). The research genes, arefollicles (Chuong et al., ’90, ’93; Noji et al., ’93;’96; Ting-Berreth and Chuong, ’96; Crowe et al.,Viallet et al., ’98; Wolpert, ’98). The rapid progressWolpert, ’98) developmental research on featherssequently, a great deal of research has focused onwithin the epidermal collar. One exception comesridges, and apparently plays a role in the differ-main to be the feather? How does the plesiomorphic anterior-What physical mechanisms are involved in helical DEVELOPMENT AND ORIGIN OF FEATHERS305tion is discussed in this paper.et al., ’96; Shubin et al., ’97). As more is learnedI thank Alan Brush, Jan Dyck, and Petermental biology. The manuscript benefited fromBostwick, Alan Brush, Michael Christianson, MattHarris, Town Peterson, Mark Robbins, RodolfoTorres, Dave Watson, Scott Williamson, ZhongheLITERATURE CITEDBrush AH. 1993. 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