A new feather type in a nonavian theropod and the early evolution of feathers

Discussion

All reported feathers in nonavian theropods are composite structures formed by multiple slender filaments (1, 5–7), which are morphologically congruent with relatively advanced stages in feather evolution predicted by recently proposed developmental models of the evolutionary origin of feathers (14, 15). However, no adduced fossil evidence has unambiguously demonstrated the presence of monofilamentous feathers in a nonavian theropod, even though such feathers would correspond to the phylogenetically most basal feather morphotype (stage I) predicted by these developmental models (14, 15). Although the EBFFs in the basal therizinosaur Beipiaosaurus differ from the predicted stage I morphology in some features, such as their somewhat planar form, their discovery nevertheless documents an unbranched feather morphology in nonavian theropods and thus completes the array of fossil evidence for the morphological series predicted by the developmental models.

The planar form of the EBFFs, as they are preserved on the slab, deserves special note. Because feathers are essentially tubular structures, the EBFFs are probably hollow, at least basally. Their relatively great width indicates, however, that they are unlikely to be subcircular in cross-section. It is more probable that the filaments developed as stiff large tubes with an elliptical cross-section. Interestingly, not only are modern feathers planar in their overall form, but their individual rami and barbules are also somewhat flattened (16). In this respect, avian feathers differ significantly from hairs, which represent the other major category of filamentous integumentary structures in tetrapods and have a subcircular cross-section. However, the undifferentiated, somewhat planar EBFFs are unlikely to represent the plesiomorphic condition for feathers because the feathers of more basal coelurosaurs are all made up of slender filaments that are subcircular in cross-section (5). Based on the ontogeny of feathers in modern birds (14), it is probable that the composite feathers of a typical feathered coelurosaur each grew from a collar of epidermal tissue that became differentiated into multiple barb ridges, each of which produced one of the filaments. By contrast, each EBFF on the body of Beipiaosaurus presumably grew from an epidermal collar that never underwent differentiation, so that subsequent growth produced a monofilamentous feather. The cross-section of the epidermal collar was probably elliptical, rather than subcircular, a condition that would explain the planar appearance of the preserved EBFFs of Beipiaosaurus. The presence of EBFFs could represent an autapomorphy of Beipiaosaurus or a slightly more inclusive clade.

It is difficult to infer the primary function of the EBFFs, as is the case for many other structures known only in extinct animals, but flight and thermoregulation can be excluded from the list of possibilities given the morphology of the feathers and their distribution on the body. The third most common function for feathers, visual display, is more acceptable for the EBFFs of Beipiaosaurus because of their relatively great length, apparent flexural stiffness, and localized distribution. The EBFFs are much longer than normal filamentous feathers (Table S1) and are inferred to have been very flexurally stiff. They occur only on portions of the head, neck, and tail, body areas that commonly bear integumentary display structures in extant birds (16) and mammals (17). These features suggest that the EBFFs might have been used in display, whereas other types of filamentous feathers in nonavian theropods are more likely to have functioned in thermoregulation (2, 11, 12). Integumentary display using highly modified pennaceous feathers has been documented in basal avians (18) and even in nonavian maniraptorans (19), but no filamentous feathers have been shown to function in display. The EBFFs of Beipiaosaurus provide the first evidence supporting the occurrence of integumentary display using filamentous feathers among nonavian theropods. Because pennaceous feathers have not been reported in therizinosaurs and more basal coelurosaurian groups, EBFFs are thus inferred to have appeared phylogenetically at a more basal point than did feathers of modern aspect. This indicates that integumentary display using feathers evolved at an earlier stage than flight, which is associated with pennaceous feather types.

Finally, the EBFFs share some striking similarities with the filamentous integumentary structures seen in the ornithischian Psittacosaurus (20) and some pterosaurs (21–23), including unbranched morphology, thickness, and apparent flexural stiffness. These points of resemblance suggest a potential primary homology among the integumentary features of these three disparate taxa. This reinforces the intriguing possibility, mentioned by some recent studies (1), that monofilamentous integumentary structures might have evolved early in archosaurian evolution and might characterize a clade far more inclusive than the Coelurosauria. The known ornithodiran fossil record would thus likely push the origin of monofilamentous integumentary structures into the Middle Triassic at least (24).