The Quarterly Review of Biology 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 critiqued and rejected. Hypotheses for the 262 Volume 77 THE QUARTERLY REVIEW OF BIOLOGY 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. F are the most complex integumentary appendages found in vertebrates (Lucas and Stettenheim 1972; Bereiter-Hahn et al. 1986). They have complex branched structure, and grow from their bases by a unique mechanism (Figures 1 and 2). The evolutionary origin of feathers has been a persistent and intractable question for more than 140 years (Lucas and Stettenheim 1972; Dyck 1985; Feduccia 1999; Maderson and Homberger 2000). Two important sources have contributed to the fundamental difficulty of studying this problem: the intellectual limitations of available models, and the lack of any antecedent fossil feather structures. Over the last few years, both problems have been addressed in ways that have fundamentally changed our conception of and answers to these evolutionary questions. Recent proposals of the developmental theory (Prum 1999; Brush 2000), and startling new paleontological discoveries of primitive feathers in nonavian theropod dinosaurs (Chen et al. 1998; Ji et al. 1998; Xu et al. 1999a, 1999b, 2000, 2001; Ji et al. 2001), have made it possible to make the first concrete conclusions about the evolutionary origin of feathers. The earliest known feathers appear in the fossil record in Archaeopteryx lithographica, known from the 140 million-year-old Solnhofen Limestone of Germany (de Beer 1954). The discovery of these spectacular fossils in the 1860s stunned scientists because of their mosaic of primitive reptilian and modern avian features, including essentially modern feathers (Griffiths 1996; Martin and Czerkas 2000). Most specimens of Archaeopteryx are preserved with impressions of the remiges and rectrices (flight feathers of the wings and tail, respectively) that exhibit asymmetrical, closed pennaceous vanes indicative of advanced flight capability. The closed pennaceous structure of the remiges and rectrices of Archaeopteryx demonstrates an entirely modern morphology, however, including differentiated distal and proximal barbules that interlock between neighboring barbs to create the planar vane of modern feathers (Griffiths 1996; Martin and Czerkas 2000). Thus, the oldest known fossil feathers give no more clues as to the ancestral morphology and ultimate origin of feathers than do the feathers of extant birds. (In this paper, the terms Aves, birds, and avian refer to members of the most inclusive clade including Archaeopteryx and modern birds. For a discussion of alternatives, see Gauthier and de Queiroz 2001.) Research on the origin of feathers requires a backward extrapolation from the complex, entirely modern feathers of Archaeopteryx and modern birds to propose plausible ancestral feather morphologies. Unfortunately, the development of a heuristic theory of the origin of feathers has been limited by many of the same conceptual problems faced by macroevolutionary biology over the last century. Early workers attempted to reconstruct primitive feather morphologies based on variations in feather structures found among “primitive” lineages of extant birds (reviewed in Dyck 1985). In absence of an explicit concept of phylogeny, these theories overlooked the fact that all modern birds share a common ancestor with Archaeopteryx that already had fully modern feathers. Therefore, extant variations were derived, secondarily simplified feather morphologies. Since 1950, many theories focused on constructing functional theories for the origin of feathers (reviewed in Dyck 1985; Feduccia 1999). These theories used speculations about the plausible function of ancestral feathers to predict their morphology, despite the paucity of evidence about the biology of avian ancestors. FuncSeptember 2002 263 EVOLUTION AND DIVERSIFICATION OF FEATHERS Figure 1. The Branched Structure of a Pennaceous Feather (A) The structure of a typical pennaceous contour feather with afterfeather, from Lucas and Stettenheim (1972). (B) Cross section of two adjacent feather barbs from the closed pennaceous portion of a feather vane (orientation as in the labeled barbs in A). Distal barbules are oriented toward the tip of the feather (extending right) and the proximal barbules are oriented toward the base of the feather (extending left). The hooked pennulae of the ends of the distal barbules extend over the obverse (upper) surface of the vane to interlock with the grooved dorsal flanges of the bases of the proximal barbules of the adjacent barbs to form the closed pennaceous vane. The distal barbules of open pennaceous feathers lack hooked pennulae. Both illustrations are from Lucas and Stettenheim (1972). 264 Volume 77 THE QUARTERLY REVIEW OF BIOLOGY September 2002 265 EVOLUTION AND DIVERSIFICATION OF FEATHERS tional theories of the origin of feathers have failed to establish a consensus on either the original function or original morphology of feathers. Over the last half of the 20th century, neoDarwinian approaches to the origin of feathers, exemplified by Bock (1965), have hypothesized a microevolutionary and functional continuum between feathers and a hypothesized antecedent structure (usually an elongate scale). Feathers, however, are hierarchically complex assemblages of numerous evolutionary novelties—the feather follicle, tubular feather germ, feather branched structure, interacting differentiated barbules—that have no homolog in any antecedent structures (Brush 1993, 1996, 2000; Prum 1999). Genuine evolutionary novelties are distinct from simple microevolutionary changes in that they are qualitatively or categorically different from any antecedent or homonomous structure (Nitecki 1990; Müller and Wagner 1991; Raff 1996). Consequently, Wagner (2000; Wagner et al. 2000; Chiu and Wagner 2001) has argued that macroevolutionary research on homology and the origins of evolutionary novelties should ask different questions that are focused on uncovering the mechanisms that generate morphological novelties. Traditional neo-Darwinian approaches to the origin of feathers have focused on creating theoretical continuity with antecedent structures, and as a consequence, few of these theories have adequately appreciated the many novel aspects of feather morphology and feather development, and none have formulated adequately detailed hypotheses about the origin and evolution of these morphological and developmental novelties. In contrast to neo-Darwinian approaches, and in congruence with a macroevolutionary concept of novelty, the developmental theory of feather origins is focused specifically on reconstructing the transition of developmental novelties required for the origin and diversification of feathers (Prum 1999). Another conceptual problem has been the tendency to propose complex evolutionary scenarios as intellectual “package deals” that include correlated and interdependent hypotheses about the origins of birds, avian flight, and feathers. One package features birds as an early nondinosaurian lineage of archosaurs, the arboreal theory of the origin of flight, and the aerodynamic theory of the origin of feathers (e.g., Feduccia 1999). An alternative package offers birds as a lineage of theropod dinosaurs, the cursorial theory of the origin of flight, and the thermal insulation theory of the origin of feathers (e.g., Ostrom 1974). These two packages have been promoted inaccurately as reflecting “ornithological” and “paleontological” schools of thought, respectively (e.g., Feduccia 1999). Clearly, the solutions to these complex questions are ultimately interrelated (i.e., there is only one history of life). But the fundamental problem with these combined scenarios is that they conflate the analysis of these complex issues and eliminate many plausible combinations. These macroevolutionary questions can only be productively and rigorously pursued independent from one another. By approaching the questions of phylogenetic relationships and evolutionary functional morphology independently, emergent historical patterns can be used to test hypotheses of morphological homology and evolutionary process (Lauder and Liem 1989; Larson and Losos 1996). Perhaps unsurprisingly, the recent theoretical Figure 2. Schematic Diagram of Helical Growth of Barb Ridges of a Pennaceous Feather The branched structure of the barbs and the rachis of a feather form by helical growth and fusion of barb ridges within the tubular feather germ. Feathers grow from the base. Barb ridges form at the new barb locus on the posterior midline of the collar and grow helically around the collar toward the anterior midline where they fuse to form the rachis ridge. Subsequent barb ridges fuse to the rachis ridge. In feathers with an afterfeather, the new barb locus divides into two laterally displaced new barb loci. Subsequently, new barb ridges grow helically both anteriorly to the main rachis and posteriorly to form the hyporachis and vane of the afterfeather. The main vane and the afterfeather form separate vanes united within a single feather by the calamus (Figure 1A). Pennaceous feathers obtain their planar form only after emerging from the cylindrical feather sheath when growth is complete. The obverse (upper) and reverse (lower) surfaces of the vane develop from the outer and inner surfaces of the cylindrical feather germ. Illustration based on Lucas and Stettenheim