A Jurassic ornithischian dinosaur from Siberia with both feathers and scales

See allHide authors and affiliations

Science  25 Jul 2014:
Vol. 345, Issue 6195, pp. 451-455
DOI: 10.1126/science.1253351

Feathers, not just for the birds?

Theropod dinosaurs, thought to be the direct ancestors of birds, sported birdlike feathers. But were they the only feathery dino group? Godefroit et al. describe an early neornithischian dinosaur with both early feathers and scales. This seemingly feathery nontheropod dinosaur shows that feathers were not unique to the ancestors of birds and may even have been quite widespread.

Science, this issue p. 451


Middle Jurassic to Early Cretaceous deposits from northeastern China have yielded varied theropod dinosaurs bearing feathers. Filamentous integumentary structures have also been described in ornithischian dinosaurs, but whether these filaments can be regarded as part of the evolutionary lineage toward feathers remains controversial. Here we describe a new basal neornithischian dinosaur from the Jurassic of Siberia with small scales around the distal hindlimb, larger imbricated scales around the tail, monofilaments around the head and the thorax, and more complex featherlike structures around the humerus, the femur, and the tibia. The discovery of these branched integumentary structures outside theropods suggests that featherlike structures coexisted with scales and were potentially widespread among the entire dinosaur clade; feathers may thus have been present in the earliest dinosaurs.

The origin of birds is one of the most-studied diversification events in the history of life. Principal debates relate to the origin of key avian features such as wings, feathers, and flight (19). Numerous finds from China have revealed that diverse theropods possessed feathers and various degrees of flight capability (49). The identification of melanosomes in non-avian theropods (10, 11) confirms that fully birdlike feathers originated within Theropoda at least 50 million years before Archaeopteryx.

But were feathers more widespread among dinosaurs? Quill-like structures have been reported in the ornithischians Psittacosaurus (12) and Tianyulong (13), but whether these were true feathers, or some other epidermal appendage, is unclear. Bristlelike epidermal appendages occur in pterosaurs, some early theropods (14), and extant mammals (“hairs”), and so the Psittacosaurus and Tianyulong filaments might have evolved independently of the feathers of theropods.

Here we report a new ornithischian dinosaur, Kulindadromeus zabaikalicus, with diverse epidermal appendages, including grouped filaments that we interpret as avianlike feathers. This suggests that all Dinosauria could have had feathers and that feathers arose for purposes of insulation and signaling and were only later co-opted for flight (10, 11).

The new dinosaur comes from the Kulinda locality (Cherynyshevsky District of Chita Region, southeastern Siberia, Russia; fig. S1), from the base of the Ukureyskaya Formation, dated as Middle to Late Jurassic (15). The dinosaur bones are associated with abundant, well-preserved fossils of plants, insect larvae, and freshwater crustaceans that suggest deposition in a low-energy, probably lacustrine, freshwater environment. The sequence includes tuff deposits and ignimbrites that indicate local volcanic activity (15).

The description of Kulindadromeus zabaikalicus (15) is based on six partial skulls and several hundred disarticulated skeletons unearthed from two neighboring monospecific bone beds. Each individual skeletal element is represented by a single morphotype, and all of the observed morphological differences can easily be explained by ontogenetic and intraspecific variation, as confirmed by the detailed study of the partial skeletons (15). Therefore, there is no indication that more than one basal ornithischian is present. Many of the bones are strongly iron-stained, suggesting partial replacement during diagenesis.

Kulindadromeus zabaikalicus is differentiated from all other dinosaurs by the following characters (Fig. 1, and figs. S4 to S7): maxilla with rostral ascending process much lower than caudal ascending process and maxillary fenestra larger than antorbital fenestra; jugal with notched postorbital ramus; postorbital with dorsoventrally expanded caudal ramus; dorsoventrally slender postacetabular process on ilium; and deep extensor fossae on metatarsals II to IV (15).

Fig. 1 Skeletal anatomy of Kulindadromeus zabaikalicus.

(A) Composite skeletal reconstruction; photograph (B) and line drawing (C) of the holotype skull (INREC K3/109) in right lateral view; (D) proximal portion of right scapula (INREC K3/204) in lateral view; (E) right scapula (INREC K3/134) in caudolateral view; (F) left ulna (INREC K3/205) in medial view; (G) right tibia (INREC K3/207) in caudal view; (H) right femur (INREC K3/206) in cranial view; (I) right ischium (INREC K3/124) in lateral view; (J) distal caudal vertebra (INREC K3/202) in right lateral view; (K) mirror image of left ilium (INREC K3/113) in lateral view; (L) dorsal vertebra (INREC 3/112) in right lateral view; (M) mirror image of left pubis (INREC K3/114) in lateral view. Scale bars, 10 mm. Abbreviations: ac, acetabulum; acp, acromial process; an, angular; aof, antorbital fossa; art, articular; cor, coracoid facet; dpc, deltopectoral crest; drf, distal radial facet; dt, dentary; fh, femoral head; fr, frontal; gl, glenoid; ilpd, iliac peduncle; imal, inner malleolus; ispd, ischial peduncle; iss, ischial shaft; j, jugal; l, lacrimal; lcd, lateral condyle; mcd, medial condyle; mf, maxillary fenestra; mx, maxilla; na, nasal; obn, obturator notch; obpr, obturator process; ns, neural spine; ol, olecranon process; omal, outer malleolus; p, parietal; pap, palpebral; pm, premaxilla; po, postorbital; poac, postacetabular process; poc, paroccipital process; poz, postzygapophysis; pr, prefrontal; prac, preacetabular process; prf, proximal radial facet; prpu, prepubic process; prz, prezygapophysis; pupd, pubic peduncle; pus, pubic shaft; q, quadrate; qj, quadratojugal; rap, rostral ascending process; rcd, radial condyle; sa, surangular; sac, supraacetabular crest; sq, squamosal; ucd, ulnar condyle; 4tr, fourth trochanter.

It was a small, 1.5-m-long bipedal herbivore, with a short skull, plant-eating teeth, elongate hindlimbs, short forelimbs, and an elongate tail (Fig. 1). Phylogenetic analysis (figs. S10 and S11) (15) recovers Kulindadromeus as a basal member of Neornithischia [all genasaurians more closely related to Parasaurolophus walkeri than to Ankylosaurus magniventris or Stegosaurus stenops (16)] and the sister taxon for Cerapoda [Parasaurolophus walkeri, Triceratops horridus, their most recent common ancestor, and all descendants (16)].

The key features of Kulindadromeus relate to its integument. Numerous, varied, exceptionally preserved integumentary features are associated, often in direct connection, with the bones and vary in morphology among different body regions. They comprise three types of scales and three types of featherlike structures. Small (<3.5 mm long) imbricated and hexagonal scales, resembling the scutella in modern birds (17), are associated with the distal parts of the tibiae in Kulindadromeus (Fig. 2A and fig. S8E). Smaller (<1 mm) rounded and nonoverlapping scales occur around the manus, tarsus (Fig. 2A and fig. S8E), metatarsus, and pes (fig. S8F), resembling the reticula along the plantar face of the pes in modern birds (17). The tail of Kulindadromeus is covered by at least five longitudinal rows of slightly arched scales (Fig. 2, B and C, and fig. S8, A to D). The largest scales (~20 mm long and 10 mm wide) occur along the proximal part of the tail. The caudal scales of Kulindadromeus are thin (<100 μm), unornamented, and slightly imbricated, each scale covering part of the adjacent distal one (Fig. 2C and fig. S8, B to D). They are clearly different from the thicker, sculptured, and nonoverlapping osteoderms in thyreophoran ornithischians (18) and from the proportionally thicker and smaller scales in iguanodontian ornithopods (19), more closely resembling epidermal scales. The preservation of the scales as carbonaceous remains suggests that they are unlikely to be osteoderms, because the bones (which also comprise calcium phosphate in vivo) display a quite different preservational pathway. Each scale forms a triangular anterior spur that covers the preceding one, so that adjacent elements are interconnected by a clip-like system. Proximally, at the level of the base of the tail (Fig. 2C), the scales become progressively smaller and more rounded and do not overlap.

Fig. 2 Epidermal scales and featherlike structures of Kulindadromeus zabaikalicus.

(A) Scales around the distal tibia and the tarsus (INREC K4/57); (B) double row of scales above the proximal part of the tail (INREC K4/94) in dorsal view; (C) close-up of the left row of caudal scales (INREC K4/117) in dorsal view; (D) partial skull (INREC K4/22) in right lateral view, with (E and F) detail of areas indicated in (D) and (E) showing filamentous structures; (G) left part of ribcage (INREC K4/33), with (H and I) detail of areas indicated in (G) and (H) showing filamentous structures.

Monofilaments are widely distributed around the thorax (Fig. 2, G to I), on the back, and around the head (Fig. 2, D to F). Those above the head are thin (~0.15 mm in diameter), short (10 to 15 mm long), and curved, with no preferred orientation. The thoracic and abdominal filaments are wider (0.2 to 0.3 mm) and longer (20 to 30 mm). These monofilaments are shorter and thinner than the long bristlelike structures on the proximal part of the tail in Psittacosaurus (12) and the filamentous structures in Tianyulong (13). They more closely resemble the monofilaments in the basal coelurosaur Sinosauropteryx (20) and are similar to morphotype 1 in a recent evolutionary model of feathers (21).

Kulindadromeus also shows compound, nonshafted integumentary structures along the humerus and femur (Fig. 3, A to F, and fig. S9). These occur as groups of six or seven filaments that converge proximally and arise from the central regions of a basal plate. Individual filaments are 10 to 15 mm long. Those on the humerus are wider (0.2 to 0.4 mm) and straighter than those on the femur (0.1 to 0.2 mm). These groups of filaments are similar to feather morphotype 3 (21, 22) and resemble the down feathers of some modern chicken breeds, such as the Silkie, which are devoid of barbules (17). The basal plates are also larger on the humerus (3 to 4 mm wide) than on the femur (2 to 3 mm); they are arranged in a hexagonal pattern, but they remain distinctly separated from each other, contrasting with the contiguous distribution of the scales on the distal forelimb, hindlimb, and tail in Kulindadromeus and also with the feathered scales that cover the tarsometatarsus of some living birds (17). Whether the basal plates represent modified scales or calamus-like structures remains unclear and requires further investigation.

Fig. 3 Featherlike structures in Kulindadromeus zabaikalicus.

(A) Right humerus and proximal part of right radius and ulna (INREC K4/115), with detail (B) and interpretative drawing (C) of compound structures around the right humerus; (D and E) compound structures around femur (counterpart of INREC K4/116) with (F) interpretative drawing of (E); (G) ribbonlike structures around proximal part of tibia (INREC K4/44); the inset shows the slab at lower magnification. (H) Detail of area indicated in (G) with interpretive drawing (I) and further details of ribbonlike structures (J); the superficial carbonaceous sheet has been removed during preparation, revealing an internal structure of thin parallel filaments (red arrow). Abbreviation: bpl, basal plate.

An additional integumentary morphotype occurs along the proximal part of the tibia in Kulindadromeus (Fig. 3, G to J): Clusters of six or seven ribbon-shaped elements appear more or less bundled together proximally, close to the bone surface. Each individual element is 15 to 20 mm long and 1.5 to 3 mm wide, with a dark median axis along its length (Fig. 3, H to J). Careful removal of a thin superficial carbonaceous sheet reveals the presence of ~10 thin (50 to 100 μm) internal parallel filaments within each ribbon-shaped element (Fig. 3J). This is an arrangement that has never previously been reported and that could represent a third featherlike morphotype in Kulindadromeus.

The presence of both simple and compound filamentous structures in Kulindadromeus (Fig. 4) supports the hypothesis that the integumentary structures in Ornithischia, already described in Psittacosaurus (12) and Tianyulong (13), could be homologous to the “protofeathers” in non-avian theropods. In any case, it indicates that those protofeather-like structures were probably widespread in Dinosauria, possibly even in the earliest members of the clade. Further, the ability to form simple monofilaments and more complex compound structures is potentially nested within the archosauromorph clade, as exemplified by Longisquama (23), pterosaurs (24), ornithischians, and theropods (including birds).

Fig. 4 Reconstruction of Kulindadromeus zabaikalicus.

A basal ornithopod dinosaur, with feathers and scales, from the Middle to Late Jurassic of southeastern Siberia. [Drawing by Pascale Golinvaux (Royal Belgian Institute of Natural Sciences)]

In Kulindadromeus and most ornithuromorph birds (17, 25), the distal hindlimb is extensively covered by scales and devoid of featherlike structures. This condition might thus be primitive in dinosaurs. Both paleontological and genetic evidence, however, suggests that the pedal scales of ornithuromorph birds are secondarily derived from feathers. In avialan evolution, leg feathers were reduced gradually in a distal-to-proximal direction, with eventual loss of the distal feathers and appearance of pedal scales in ornithuromorphs (25). Further, evo-devo experiments (26, 27) show that feathers in extant birds are the default fate of the avian epidermis, and that the formation of avian scales requires the inhibition of feather development. The local formation of scales requires the inhibition of epidermal outgrowth, regulated by the sonic hedgehog pathway; this inhibition is partially lost in the case of breeds with feathered feet (27). Therefore, it is possible that the extensively scaled distal hindlimbs in Kulindadromeus might be explained by similar local and partial inhibition in the development of featherlike structures. The preservation of featherlike structures and scales in the basal neornithischian Kulindadromeus, and their similarity to structures that are present in diverse theropods and ornithuromorph birds, thus strongly suggest that deep homology mechanisms (28) explain the complex distribution of skin appendages within dinosaurs (23).

Supplementary Materials

Materials and Methods

Supplementary Text

Figs. S1 to S11

References (2955)

References and Notes

  1. See the supplementary materials on Science Online.
  2. Acknowledgments: We thank A. B. Ptitsyn for making fossils available for study; Ph. Claeys, J.-M. Baele, and I. Y. Bolosky for help and comments on the manuscript; and P. Golinvaux, J. Dos Remedios Esteves, C. Desmedt, and A. Vandersypen for the drawings and reconstructions. This study was supported by Belgian Science Policy grant BL/36/62 to P.G. and by Natural Environment Research Council Standard Grant NE/I027630/1 awarded to M.J.B.
View Abstract

Stay Connected to Science

Navigate This Article