A new caudipterid from the Lower Cretaceous of China with information on the evolution of the manus of Oviraptorosauria

Caudipteridae is a basal clade of Oviraptorosauria, all known species from the Early Cretaceous Jehol Biota of northeastern China. They were one of the first feathered dinosaur groups discovered, and possessed avian-like pennaceous remiges and rectrices. Their discovery provided significant information on early oviraptorosaurian evolution and the origins of birds and feathers. Here we describe a new caudipterid species Xingtianosaurus ganqi gen. et sp. nov. from the Lower Cretaceous Yixian Formation of Liaoning Province, China. This new taxon differs from other caudipterids by a small pleurocoel close to the dorsal edge of the lateral surface of the dorsal vertebrate centrum, a humerus longer than the scapula, a proportionally long ulna, a relatively small radiale angle, and a relatively short metacarpal I. The phylogenetic results shows X. ganqi is an early diverging caudipterid. It exhibits a mosaic morphology, providing new morphological information on early manual evolution of Oviraptorosauria, and giving new light on the evolution of radiale angle among Coelurosauria.

www.nature.com/scientificreports www.nature.com/scientificreports/ anteroposterior length of the centrum is slightly longer than its height. The ventral margin shows a constriction. Based on the preserved chevrons, at last 18~19 caudals are preserved on Xingtianosaurus ganqi. Because the distal most caudals are not preserved, the certain number of caudal vertebrate and whether the distal caudals fused into a pygostyle, as in Similicaudipteryx 7 and Nomingia 9 , is unknown. As in other oviraptorosaurs, an obvious transition point is absent 1 . The ratio between the length and height of the vertebrae gradually increases from proximal to distal. However, on the distal most preserved caudals, this ratio is reduced. The long and slender prezygapophyses of middle caudals extend anteriorly, and are longer than the half length of the corresponding centrum. The postzygapophyses are much shorter than the prezygapophyses, and only slightly extend past the posterior articular faces of the centra. The first six chevrons are dorsoventrally elongated and flattened mediolaterally. The middle chevrons are distinctly shortened in height. All chevrons with a preserved distal end show an anterior expansion, which creates a boot-shaped end. As in Nomingia 9 , the proximal end of each chevron is divided into three prominent processes. The anterior and posterior processes articulated with the previous and succeeding centrum respectively, and the middle process inserts between the two centra. The dorsal ribs are scattered. The neck separating the capitulum and tuberculum has a concave dorsal margin. The scapular blade is straight and strap-like (Fig. 3b), unlike the slightly bowed scapula of Similicaudipteryx 7 . It is shorter than the humerus, in contrast to other oviraptorosaurs 1 but similar to paraves 12 . The lateral surface of shaft is strongly concave, making a sharp rim at the dorsal and ventral margins. This concavity extends nearly to the distal end and has a round posterior margin. The dorsal and ventral margins of the scapula are subparallel at mid-shaft and distinctly expanded at the distal end. The distal end is slightly rugose, for the attachment of M. deltoideus scapularis 13 . The acromion is not as prominent as other oviraptorosaurs outside of Caudipteryx 1 . It projects anteriorly and slightly dorsally (Fig. 3c).
One sternal plate is preserved but is mostly covered by other bones. It is more than 25% length of femur. This ratio is more similar to oviraptorids such as Khaan 11 and Citipati 14 , rather than the small sternum of C. zoui (20.69%) 6 and C. dongi (16.45%) 5 . The anterior margin of the sternum is slightly convex for articulation with the coracoid. The sternum bears anterolateral and xiphoid process as Oviraptoridae 11,14 (Fig. 3e-g) and Caenagnathidae 15 (Fig. 3h), unlike the two oval sternal plates in Caudipteryx 3,5 (Fig. 3d). The differences between the sternum of Xingtianosaurus and Caudipteryx are unlikely to be the result of ontogeny for the following reasons: the sternum of Caudipteryx is connected with the sternal ribs, with no space for the existence of cartilage 3,5 ; and the fusion of the centra and neural arches, the well-ossified wrist and ankle bones, absence of pits and grooves on the surface of bones indicate the adult nature of Caudipteryx 3,5 . The sternum of Xingtianosaurus has a wrinkled surface for attachment of M. pectoralis 13 .
As in caudipterids, the humerus is half the length of the femur. The humeral head is pronounced and domed at its proximal end. The deltopectoral crest is broken but extends less than one-third of the shaft. The internal tuberosity is located in nearly the same plane as the humeral head and extends a short distance. All that can be said about the distal end is that is slightly expanded and has a nearly round lateral condyle. The ulna is subequal in length to the humerus, which differs from most maniraptors but is shared with some avialae 16 . The olecranon process is weakly developed and smaller than the coronoid processes. The shaft bows posteriorly, which is a synapomorphy of Maniraptora 17 . The distal end shows no dorsoventral expansion, and is almost as wide as the mid-shaft, in contrast to a pointed end in Khaan 11 and Anzu 18 . The radius is slightly bowed anteriorly, this condition could also be seen in some derived oviraptorosaurs 11,14 but is usually absent in Caudipteridae. The shaft expands in width distally from about 40% of the way from the proximal end.
There are three carpals preserved in extensor view (Fig. 4). The radiale is wedge-shaped in dorsal view. It is relatively large, similar in size to the semilunate carpal. The radiale angle 19 is about 39°. This angle is much smaller than other oviraptorosaurs including Caudipteryx, but similar to some deinonychosaurids 19 . There is a small carpal locates between the ulna and radius, articulating with the radiale and metacarpal II, but it is hard to determine whether it is the ulnare or intermedium. As in other oviraptorosaurs 11,15,20 except Heyuannia 21,22 , the proximal surface of the semilunate carpal is not strongly convex as paraves. The distal surface covers the entire proximal end of metacarpal I and half of metacarpal II. Metacarpal I is slightly more robust than metacarpal II and less than 40% of the length of the second (Fig. 4). This ratio is smaller than any known oviraptorosaurs (except Gigantoraptor 23 ) where it is approximately 50% in derived species and larger than 40% in Caudipteridae. The proximal end has a slightly concave articular surface for contacting with the semilunate carpal, different from the nearly flat surface of other oviraptorosaurs. The shaft of metacarpal I contacts tightly with metacarpal II for almost its whole length, whereas in Machairasaurus the distal end of metacarpal I is bended and separated from metacarpal II 20 . The distal articular surface is ginglymoid and slightly rotated, making phalanx I-1 point medially when in flexion. The collateral ligament pits are absent on the distal end. The shaft of metacarpal II is nearly straight and the proximal surface is nearly flat. On the distal end, the collateral ligament pit is relatively small and dorsally located. Metacarpal III is more than 90% length of the metacarpal II. The shaft of metacarpal www.nature.com/scientificreports www.nature.com/scientificreports/ III is compressed with a groove on the medial surface for contact with metacarpal II. The proximal end is bended medially and does not reach the proximal end of metacarpal II. Phalanx I-1 is the longest phalanx and has a weakly concave proximal articular surface as other caudipterids. In contrast, derived oviraptorosaurs always have a deep concave surface 5,6,11,14,20,24,25 . Phalanx II-1 is preserved, and it also has a weakly concave articular surface. On all phalanges with a preserved distal end, ligament pits are small and dorsally located. This condition is more similar to derived oviraptorosaurs, while Caudipteridae have a large circular ligament pit near the center. Almost all non-ungual phalanges of digit III are taphonomically missing except the penultimate phalanx on right hand. The shaft of this phalanx is very slender with a relatively large and circular ligament pit. All unguals are strongly curved with a prominent flexor tubercle. The proximodorsal lip is absent.
The ilium is badly preserved (Fig. 5). The anteroventral process does not extend further than the pubic peduncle, unlike in Caudipteryx (IVPP V12430) 6 . The cuppedicus fossa is well-developed, with a somewhat arched ventral margin, unlike the nearly straight margin in Caudipteryx (IVPP V12430) 6 and Nemegtomaia 10 but similar to those of C. dongi, Similicaudipteryx 7 and derived oviraptorosaurs. The pubic peduncle slightly bends anteroventrally, indicating a propubic condition. In contrast to most maniraptors except Similicaudipteryx 7 , the pubic peduncle is constricted at the base and expands anteroposteriorly at the distal ends. Pubis is approximately 86% length of the femur as in Caudipteridae 5,6 . This ratio is about 90% in Caenagnathidae 26,27 and nearly 100% in Oviraptoridae 11,28,29 . The ratio between pubic symphysis to pubis is 57% (Fig. 5), similar to Similicaudipteryx 7 , but larger than 50% in Caudipteryx 5,6 and Microvenator 26 . This ratio in most caenagnathoids with known pubic  www.nature.com/scientificreports www.nature.com/scientificreports/ symphysis is larger than 60% 11,23,28 . The ischium is plate-like. The dorsal margin is strongly bowed anteriorly. As in other oviraptorosaurs, a large triangular obturator process is located at mid-shaft of ischium. The lateral surface of obturator process is concave for the attachment of M. adductor femoris 1 30 . The dorsal margin of the obturator process is thickened.
The femoral shaft is bowed anteriorly in lateral view. The proximal end of the femur is broken and it is difficult to observe any details. There is no fourth trochanter. The tibia is approximately 125% the femoral length. On the posterior surface, the lateral and medial condyle are well-developed and slightly point upwards. Both condyles are large and round, and are separated by a shallow groove. A pronounced fibular crest is preserved on the lateral surface of tibia, about 26% of the way down the shaft of the tibia from the proximal end. This ratio is shorter than Gigantoraptor and Khaan. The mid-shaft of tibia is compressed lateromedially but the distal end expands to be plate-like. The tibia is not fused with the astragalus. The medial surface of fibula is concave for contact with the lateral condyle of tibia. The tubercle for the insertion of M. iliofibularis is not obvious, but is located a quarter way down the shaft. As in other neotheropods, the concavity turns into a narrow groove along the medial surface of fibula 14,[31][32][33] . The groove expands below the iliofibularis tubercle, offering an attachment for the interosseous membrane between tibia and fibula.
The distal tarsals are not fused with the metatarsals. Metatarsal I is strongly reduced, and located three-quarters of the way down metatarsal II. Metatarsal III is the longest, then II and IV, respectively. The proximal end of metatarsal II expands both anteroposteriorly and transversely. Most of the shaft is straight, but the distal quarter is bent medially. Metatarsal III is strongly compressed along more than half of its length. The proximal end of metatarsal III is slightly anteroposterior expanded. The anterior and posterior margins are subparallel to be strap-like, with no obvious proximal constriction, which is seen in Chirostenotes, Leptorhynchos or some troodontids 34 . Because the proximal end of metatarsal II and IV are not articulated, whether a true arctometatarsal exists is doubtful. The lateral margin of metatarsal IV is constricted to make a sharp ridge. The metatarsal V extends less than one-third of length of metatarsal III, and its shaft is bowed. Metatarsal II to IV bear large and deep ligament fossae on the distal end. The joints of all non-ungual phalanges bear shallow or no ginglymous articular surface. On the distal end of each phalanx there is a deep ligament fossa on both sides. Each phalanx is longer than the distal one, except the fourth phalanx of digit IV, as an adaptation for terrestrial locomotion 35 . The pedal unguals are only slightly curved. A vascular groove extends from proximal end to the tip near the mid-line on both sides, whereas it is more ventrally locates in Caudipteryx (IVPP V12430).
Some imprints and fragments of pennaceous feathers are preserved posterior to the forearm and metacarpals (Fig. 4a). The feathers are perpendicular to the ulna and covered the distal half of the forearm. The attachment of remiges is different from known Caudipteryx specimens, which possess pennaceous feathers only on the metacarpals 3,5,6 . Details of the plumage are hard to verify because of the bad preservation. systematics of Xingtianosaurus ganqi. Because the skull is not preserved, we first investigated the systematic position of Xingtianosaurus ganqi by adding it to a coelurosaurian matrix 36 (Fig. 6a). The analysis produced 74 most parsimonious trees of 3374 steps (Consistency Index = 0.32, Retention Index = 0.776). The result supports its location at the base of Oviraptorosauria, close to Caudipteryx. This position is consistent with the primitive morphological features: the tail is proportionally short with fewer than 26 caudals; the humerus is relatively short, about half the length of the femur; metacarpal I is shorter than 50% length of the second; the proximal articular surface of manual phalanx I-1 is slightly concave; and the proximal portion of metatarsal III is compressed transversely.
In order to determine the relationship of Xingtianosaurus ganqi gen. et sp. nov. relative to other oviraptorosaurs, we conducted a phylogenetic analysis using an oviraptorosaurian data metrics modified from combination of Osmólska et al. 1 , Lamanna et al. 18 , and Funston & Currie 15 . The analysis results in 2 most parsimonious trees of 581 steps (Consistency Index = 0.513, Retention Index = 0.691). The strict consensus of the most parsimonious trees confirms that Xingtianosaurus ganqi belongs to Caudipteridae (Fig. 6b). In this result, Caudipteridae is only supported by one character: Preacetabular process expanded ventrally well below the level of the dorsal acetabular margin (character 138). However, this analysis gives less information about the relationship between Caudipteryx, Similicaudipteryx and Xingtianosaurus ganqi, which are recovered in a polytomy.

Discussion
Manus evolution in oviraptorosauria. Caudipteryx can be easily distinguished from other oviraptorosaurs by its bizarre manual characters: 5,6 a strongly reduced manual digit III with only two short phalanges whose combined length is slightly longer than half the length of phalanx manual II-1; a large ligament pit on the manual phalanges; and an only shallowly concave proximal articular surface of manual phalanx I-1. The hand of Xingtianosaurus ganqi provides important information that reduces the morphological gap between Caudipteryx and other oviraptorosaurs. As in Caudipteryx, the proximal articular surface of phalanx I-1 in Xingtianosaurus ganqi is weakly concave, but it shares with derived oviraptorosaurs a relatively small ligament pit. Unlike Caudipteryx, but like all other oviraptorosaurs, the manus of Xingtianosaurus ganqi preserves three unguals. The large two belong to digit I and II, while the relatively small one belongs to digit III. Although the full digit III is not preserved, the remaining bones are slender, as in other oviraptorosaurs.
The study of the hand of Xingtianosaurus ganqi also gives new understanding of the evolution of hand of oviraptorosaurs (Fig. 7). In both Caudipteridae and Caenagnathidae, the combined length of manual phalanx II-1 and II-2 is 1.5 times longer than metacarpal II. But the second digit of Xingtianosaurus ganqi is relatively shorter than the combined length of phalanx II-1 and II-2 is about 1.1 times longer than metacarpal II, closer to the ratio of Oviraptoridae, except "Ingeniinae". This indicates that the primitive condition in Oviraptorosauria is non-ungual phalanges of the second digit subequal in length to metacarpal II. The elongated conditions in Caudipteridae and Caenagnathidae are independently evolved.
www.nature.com/scientificreports www.nature.com/scientificreports/ Some studies have regarded Caudipteryx as a kind of secondarily flightless avian [37][38][39] according to some features shared with birds, such as the third manual digit strongly reduced, the propatagium on the forelimb, and the absence of a supracetabular crest of ilium. The features of the manus of Xingtianosaurus indicate the specialized hand of Caudipteryx is derived from other oviraptorosaurs. In addition, the absence of a supracetabular crest can be found not only in Caudipteryx and paraves, but also in many oviraptorosaurs and some non-pennaraptoran coelurosaurs such as Huaxiagnathus (Compsognathidae) 40 . A propatagium is existence on forelimb of Microraptor 38 , and is not a synapomorphy of avians. These result support Caudipteryx as a true dinosaur, rather than a flightless avian.
Radiale angle evolution in oviraptorosauria. The radiale angle was first proposed as a useful character by Sullivan et al. 19 (Fig. 6a). It is the angle between the articular surface for the radius and semilunate carpal, and it is related to the flexibility of the manus. A large radiale angle is an osteological correlate of a greater range of abduction of the manus. In Coelurosauria, a small radiale angle is the primitive state and it becomes enlarged in maniraptorans. The enlarged radiale angle of maniraptorans means not only a more flexible manus, but also a capability to protect long plumage on their forearm.
Sullivan et al. 19 interpreted the radiale angle in oviraptorosaur as unusually large, even greater than basal Avialae. This is because the oviraptorosaur taxon Sullivan et al. chose to represent the entire group is Caudipteryx, which has a radiale angle of 76°. To verify the condition of the radiale angle in Oviraptorosauria, we measured other oviraptorosaurs with a well-preserved radiale. Only angles measured from a radiale preserved in the three-dimension or two-dimensional radiale with at least partially exposed articular surface are reliable. The www.nature.com/scientificreports www.nature.com/scientificreports/ result shows that the radiale angle is 93° in Hagryphus (Caenagnathidae), 62° in Khaan, 49° in Machairasaurus (Oviraptoridae). Thus, all measurements of the radiale angle of oviraptorosaurs are relatively larger than other non-avian maniraptorans. But it should be noted that Caudipteryx is an extremely specialized species, and the other measured species are derived, so they do not adequately represent the basal condition of Oviraptorosauria. As a primitive species, the radiale angle of Xingtianosaurus is more representative of the basal condition. Its low radiale angle coincides with the evolutionary trend of radiale angle increase in Coelosauria (Fig. 6b). This measurement indicates, like many other characters such as toothless jaws, short nasals, and a rod-like jugal bar 28 , a large radiale angle similar to birds evolved independently in derived oviraptorosaurs.
Most oviraptorosaurs with preserved radiales show a large angle. But the radiale of derived "Ingeniinae" is quite different from other oviraptorosaur groups 21,22,41,42 . Their radiale is small, less than one-third of the size of the semilunate carpal in Heyuannia and even less than one-fourth in Jiangxisaurus, whereas radiale is larger than half the size of the semilunate carpal in other oviraptorosaurs. The radiale of "Ingeniinae" is quadrilateral, rather than wedge-shaped like in most maniraptorans. The function of the manus in these dinosaurs may be changed from other theropods.

Methods
The phylogenetic analysis of Coelurosauria is from a large recently published data matrix 34 (853 characters and 153 taxa). The oviraptorosaurian matrix (252 characters and 39 taxa) is modified from combination of Osmólska et al. 1 , Lamanna et al. 18 , and Funston & Currie 15 , with 3 added characters as following: 251. Ratio of width of metacarpal III to metacarpal II: more than 0.5 (0); less than 0.5 (1). 252. Ligament pit on manual phalanges: small and dorsally located (0); large and covering most distal end (1). 253. Proximal articular surface of first phalanx of digit I: slightly concave (0); obviously concave (1). We analyzed both datasets with Tree Analysis Using New Technology (TNT) version 1.1 43 . The coelurosaurian analysis used the "New Technology" search options, with sectorial search, ratchet, tree drift and tree fusion, recovering a minimum tree length in 10 replicates. In oviraptorosaurian analysis, we used traditional search with tree bisection-reconnection (TBR) swapping algorithm with random seeds of 1,000 and 1,000 replicates, saving ten trees per replication.