ARTICLE
Received 26 Jun 2012 | Accepted 14 Dec 2012 | Published 22 Jan 2013
DOI: 10.1038/ncomms2389
Reduced plumage and flight ability of a new
Jurassic paravian theropod from China
Pascal Godefroit1,2, Helena Demuynck3, Gareth Dyke4, Dongyu Hu5,6, Franc¸ois Escuillié7 & Philippe Claeys3
Feathered theropods were diverse in the Early Cretaceous Jehol Group of western Liaoning
Province, China. Recently, anatomically distinct feathered taxa have been discovered in the
older Middle-Late Jurassic Tiaojishan Formation in the same region. Phylogenetic hypotheses
including these specimens have challenged the pivotal position of Archaeopteryx in bird
phylogeny. Here we report a basal troodontid from the Tiaojishan Formation that resembles
Anchiornis, also from Jianchang County (regarded as sister-taxa). The feathers of Eosinopteryx
are less extensive on the limbs and tail than Anchiornis and other deinonychosaurians. With
reduced plumage and short uncurved pedal claws, Eosinopteryx would have been able to run
unimpeded (with large foot remiges cursorial locomotion was likely problematic for
Anchiornis). Eosinopteryx increases the known diversity of small-bodied dinosaurs in the Jurassic, shows that taxa with similar body plans could occupy different niches in the same
ecosystem and suggests a more complex picture for the origin of flight.
1 Department of Palaeontology, Royal Belgian Institute of Natural Sciences, rue Vautier 29, 1000 Bruxelles, Belgium. 2 Jilin University Geological Museum,
Chaoyang Campus, 6 Ximinzhu Street, Changchun 130062, China. 3 Earth System Science, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium.
4 Ocean and Earth Science, National Oceanography Centre, University of Southampton Waterfront Campus, European Way, Southampton
SO 14 3ZH, UK. 5 Paleontological Institute, Shenyang Normal University, 253 North Huanghe Street, Shenyang 110034, China. 6 Key Laboratory of Vegetation
Ecology, Ministry of Education, Northeast Normal University, 5268 Renmin Street, Changchun 130024, China. 7 Eldonia, 9 avenue des Portes Occitanes,
3800 Gannat, France. Correspondence and requests for materials should be addressed to P.G. (email: pascal.godefroit@naturalsciences.be).
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ARTICLE
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms2389
R
ecent discoveries of feathered theropod dinosaurs in the
Middle-Late Jurassic Tiaojishan Formation of western
Liaoning Province, north-eastern China, have considerably
challenged our understanding of the evolution and biology of the
Paraves (the most-inclusive clade containing Passer domesticus
Linnaeus, 1758 but not Oviraptor philoceratops Osborn, 1924; see
Supplementary information)1–3. Large pennaceous feathers were
already developed on the tail, forelimbs and hindlimbs, and
particularly on the metatarsus and pes, of the troodontid
Anchiornis2. It has been postulated that large pennaceous
feathers first evolved distally on the hindlimbs, as on the
forelimbs and tail, in basal paravian theropods and only spread
proximally at a subsequent stage in theropod evolution2.
Moreover, the organization of the pedal feathers into a
coherent planar surface suggests that they potentially had some
aerodynamic function in Anchiornis2. And adding the new taxa
Xiaotingia and Anchiornis from the Tiaojishan Formation in a
phylogenetic analysis of paravian theropods challenges the pivotal
position of the iconic Archaeopteryx, regarded from its discovery
as the most primitive bird, shifting it to the Deinonychosauria
(the most-inclusive clade containing Dromaeosaurus albertensis
Matthew and Brown, 1922 but not P. domesticus Linnaeus, 1758;
see Supplementary information)3.
Here we describe a new troodontid theropod from the
Tiaojishan Formation of western Liaoning Province. Although
it resembles Anchiornis from an osteological point of view, this
new troodontid is characterized by a reduced plumage, in
comparison with other Middle-Late Jurassic feathered deinonychosaurians: large pennaceous feathers are absent from its tail,
metatarsus and pes. The plumage of paravian theropods was
already diversified by the Late Jurassic, obviously adapted to
different ecological niches.
a
b
sk
cev
ls
rs
fu
dv
cav
lil
rcor
rh
rr
ril
lh
rp ga
lu
lis
rt
ris
rf
lf
ma
rm
ru
lr
lm
lt
rp
lp
4 cm
Results
Systematic palaeontology
Class Theropoda Marsh, 1881
Order Maniraptora Gauthier, 1986
Suborder Troodontidae Gilmore, 1924
Eosinopteryx brevipenna gen. et sp. nov.
Etymology. Eo, Greek for daybreak, dawn; sino, Latin for Chinese; pteryx, Greek for feather, wing; brevi, Latin for short; penna,
Latin for feather.
Holotype. YFGP (Yizhou Fossil & Geology Park)-T5197, a
complete articulated skeleton with associated integumentary
structures (Fig. 1; see Methods for provenance and authenticity of
the holotype specimen).
Locality and horizon. Yaolugou, Jianchang, western Liaoning,
China; Middle-Late Jurassic Tiaojishan Formation1–3.
Diagnosis. A small paravian maniraptoran theropod that possesses the following osteological autapomorphies: a short snout,
about 82% the length of the orbit; a lacrimal with a long posterior
process participating in about half the length of the dorsal margin
of the orbit and a vestigial anterior process; a short tail, composed
of 20 caudal vertebrae, 2.7 times the length of the femur; chevrons
reduced to small rod-like elements below the proximal 8th or 9th
caudal; an ilium with a proportionally long, low and distally
tapering postacetabular process (ratio ‘length/height at midlength’ ¼ 5), and pedal unguals shorter than corresponding
penultimate phalanges. The plumage of this taxon is characterized by the absence of rectrices (versus other paravians with
preserved plumage) and feathers on metatarsus and pes (versus
other troodontids with preserved plumage on the hindlimb).
2
Figure 1 | Eosipnopteryx brevipenna YFGP-T5197. (a) Photograph and
(b) line drawing. cav, caudal vertebrae, cev, cervical vertebrae; dv, dorsal
vertebrae; fu, furcula; ga, gastralia; lf, left femur; lh, left humerus; lil, left
ilium; lis, left ischium; lm, left manus, lp, left pes; lr, left radius; ls, left
scapula; lt, left tibia; lu, left ulna; ma, mandible; rcor, right coracoid; rf, right
femur; rh, right humerus; ril, right ilium; ris, right ischium; rm, right manus;
rp, right pes; rr, right radius, rs, right scapula; rt, right tibia; ru, right ulna;
sk, skull.
Description. The holotype of E. brevipenna is small, just 30 cm
long (Fig. 1). The skull has a subtriangular lateral profile produced by a shallow snout and expanded postorbital region
(Fig. 2). Unlike Anchiornis2, the snout of Eosinopteryx is distinctly
shorter (about 82% of orbital length) than its orbit. Both the
rostral plate and the maxillary process of the premaxilla are
particularly short. The posterior process of the lacrimal is
elongated and straight, participating in about half the length of
the dorsal margin of the orbit, whereas the anterior process is
vestigial. The postorbital process of the jugal is broader than in
Anchiornis2, whereas the triradiate postorbital is larger than in
Archaeopteryx4 and forms a complete postorbital bar with the
jugal. There is no trace of a mandibular fenestra. The dentary has
a groove that widens posteriorly and contains a row of foramina
as in Archaeopteryx, Anchiornis, Xiaotingia, troodontids and
some basal dromaeosaurids2,3. The teeth of Eosinopteryx are
unserrated and sharp in contrast to the bulbous teeth of
Xiaotingia3. As characteristic of troodontids5, the premaxillary
and the dentary teeth in the symphyseal region are more closely
packed than are the teeth in the posterior part of the dentary.
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a
b
rpa
rsq
rfr
rq
rsa
rj
scl
rl
rpo
rect
rpal
rna
ra
rmx
rdt
lpm
rpm
1 cm
c
d
prac
ac
1 cm
postac
ac
e
postpr
obt
f
g
mt IV
mt III
mt II
IV-1
IV-2
III-1
II-1
II-2
III-2
IV-3
IV-4
1 cm
IV-5
II-3
III-3
III-4
h
i
1 cm
Figure 2 | Selected skeletal elements and associated feathers of
Eosipnopteryx brevipenna YFGP-T5197. (a) Photograph of skull and
mandible in right lateral view. (b) Line drawing of skull and mandible in right
lateral view. (c) Photograph of pelvis in right lateral view. (d) Line drawing
of right ilium in lateral view. (e) Line drawing of right ischium in lateral view.
(f) Photograph of right metatarsus and pes. (g) Line drawing of right
metatarsus and pes. (h) Detail of secondary remiges. (i) Detail of
plumulaceous feathers under the middle part of the tail. ac, acetabulum;
lpm, left premaxilla; mt, metatarsal; obt, obturator process; postpr,
posterodistal process; prac, preacetabular process; ra, right angular; rdt,
right dentary; rect, right ectopterygoid; rfr, right frontal; rj, right jugal; rl,
right lacrimal; rmx, right maxilla; rna, right nasal; rpa, right parietal; rpal,
right palatine; rpm, right premaxilla; rpo, right postorbital; rq, right quadrate;
rsq, right squamosal; rsa, right surangular; scl, scleral plate.
There are seven postaxial cervical vertebrae in YFGP-T5197.
The cervical ribs are as long as their corresponding centra,
contrasting with the shorter cervical ribs seen in Troodon
formosus5 and the much longer ones of Archaeopteryx6. The
trunk is about 32% the length of the hindlimb, as in Anchiornis2
and Mei7. The middle and posterior dorsals are proportionally
elongate as in Anchiornis, dromaeosaurids and Archaeopteryx8.
As in the latter, Anchiornis and basal deinonychosaurs, the dorsal
centra do not have distinct pneumatic foramina just shallow
depressions on their lateral surfaces3. Numerous, very slender,
abdominal ribs are preserved in YFGP-T5197, as in
Archaeopteryx6, dromaeosaurids9, the basal pygostylian bird
Confuciusornis10 and many enantiornithines (for example,
Sinornis). The tail of Eosinopteryx is particularly short, 2.7
times the length of the femur (contrasting with 3.2 in Mei7 and
3.9 in the Eichstätt Archaeopteryx6), and only composed of 20
caudal vertebrae (contrasting with 21–23 in Archaeopteryx6, ca.
30 in Anchiornis1 and 24–26 in Microraptor11). The anterior
caudals are proportionally short, their transverse processes longer
than corresponding centra and particularly narrow. Neural spines
are developed only on the anteriormost third or fourth caudals.
As in Anchiornis and Archaeopteryx2,3, the middle and posterior
caudal vertebrae each bear a distinct groove on the lateral surface
near the junction of the centrum and neural arch. The chevrons
are reduced to small rod-like elements and are only present below
the proximal eighth or ninth caudal centra, contrasting with
the larger hook-like proximal chevrons of Anchiornis1 and
with the vertically oriented rectangular proximal chevrons of
Archaeopteryx6.
The subrectangular coracoid of Eosinopteryx bears a distinct
subglenoid fossa and has a wider proximal end than Xiaotingia3
(Supplementary Fig. S1). The scapula (scapula/femur ¼ 0.49) is
proportionally much shorter than in Anchiornis (0.68). The
forelimb of this small paravian (0.73 times hindlimb length) is
slightly shorter than that of Anchiornis (0.8) (ref. 2) and
Archaeopteryx (0.9–1.0) (ref. 6) but is much longer than Mei
(0.5) (ref. 7). The humerus of Eosinopteryx is also shorter (0.8
times) than its femur; the humerus is slightly longer than the
femur in Anchiornis, distinctly longer (1.1–1.2) (ref. 6) in
Archaeopteryx, and is only half the femur length in Mei. As in
Anchiornis, the radius and ulna of Eosinopteryx are straight with
only a narrow gap between them. The manus is slightly longer
than the femur (manus/femur ¼ 1.2), contrasting with the short
hand of Mei (0.8) (ref. 7) and with the proportionally more
elongate hands of Anchiornis (1.55) (ref. 2) and Archaeopteryx
(1.4–1.6) (ref. 6). Metacarpal II is about one third the length of
metacarpal III; in contrast to Xiaotingia3, metacarpal IV is shorter
and is much more slender than metacarpal III (Supplementary
Fig. S2). The phalangeal portion of the manus is also
proportionally shorter, relative to the metacarpus, than in
Xiaotingia3. As in Anchiornis2, the long manual phalanx II-1 of
Eosinopteryx is as robust as the radius; this element is much more
gracile in Sinornithoides12 and Archaeopteryx6. Contrasting with
Xiaotingia3, phalanx III-2 is shorter than metacarpal III, whereas
the manual unguals of Eosinopteryx, sheathed by long keratinous
claws, are less curved than in Archaeopteryx6, Anchiornis1 and
Xiaotingia3.
The ilium of Eosinopteryx is characterized by a long, low and
distally tapering postacetabular process, with a ratio ‘length/
height at mid-length’ of 5 (Fig. 2). The ischium is particularly
short, about 28% the femur length. With its distally displaced
obturator process and its long and pointed posterodistal process,
this element closely resembles that of Anchiornis1,2 (Fig. 2). The
tibiotarsus of Eosinopteryx (1.4 femur length) is proportionally
shorter than Anchiornis (1.60), whereas pes (metatarsus þ
phalanges) proportions (1.3 femur length) are similar to
those of Mei7 and shorter than Anchiornis (1.56) (ref. 2). The
proximal end of metatarsal III is transversely compressed,
suggesting a subarctometatarsalian condition. Pedal digit I lies
on the medioplantar side of metatarsal II (Fig. 2), as in
Archaeopteryx6,13,14, but contrasts with the position of pedal
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ARTICLE
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Period
Epoch
Age/stage
Maastrichtian
70
Saurornithoides
Troodon
Zanabazar
Dromaeosauridae
Ma
Discussion
Preliminary phylogenetic analysis places E. brevipenna sister to
Anchiornis huxleyi at the base of Troodontidae (Fig. 3) (subject to
change in subsequent analyses; see Supplementary Methods for
details). Both taxa share a dorsally curved ilium shaft, a pubis
moderately oriented posteriorly and a straight ulna that is not
bowed away from the humerus. Archaeopteryx and Wellnhoferia
form an unresolved polytomy at the base of Deinonychosauria in
the strict consensus tree, supporting the hypothesis that
Archaeopteryx is a deinonychosaurian theropod instead of a
primitive bird3 (Fig. 3). Note, however, that this phylogeny
remains only weakly supported presumably due to the numerous
homoplasies
widely
distributed
across
coelurosaurian
phylogeny3,17 (Supplementary Fig. S3).
The almost complete plumage of Eosinopteryx is less developed
than that of other known Middle-Late Jurassic deinonychosaurians. The complete absence of rectrices on the tail cannot be
explained by taphonomic factors (that is, more fragile plumulaeous feathers are well preserved along the whole length of the tail)
and does not reflect a basal phylogenetic position for Eosinopteryx
among paravians, because long rectrices are now known to
occur in at least one basal member of each of the five major
known lineages in this region of the theropod tree, including
Byronosaurus
digit I in Anchiornis, which is medial to metatarsal II1. The
phalanges of pedal toes II, III and IV decrease gradually in length
proximodistally, as in Archaeopteryx and terrestrial cursorial
birds15. The pedal unguals of Eosinopteryx are much shorter than
those of Archaeopteryx6, Anchiornis1,2, troodontids5 and
dromaeosaurids9, even shorter than the corresponding
penultimate phalanges.
As in Anchiornis2, the longest remiges of Eosinopteryx are at
least 150% the length of the humerus (Fig. 2) and are symmetrical
on the forelimbs. Long, densely packed and symmetrical
pennaceous feathers are present along the posterior part of the
thigh and crus, consistent in distribution with the tetrapterygian
condition of several other basal paravian taxa2,16. However,
careful preparation shows that feathers were absent from the
metatarsus and pes of YFGP-T5197. Feathers covering other
regions of the body (head, neck, thorax, back and tail) are
plumulaceous and ‘rachis-like’ structures described on the
plumulaceous feathers at the base of the tail and on the neck in
Mei7 are absent in Eosinopteryx. The feathers on the tail are short,
o20 mm long; all are plumulaceous, composed of a bundle of
filaments that are joined together proximally and remain nearly
parallel as they pass distally (Fig. 2). Pennaceous rectrices are
absent.
75
Campanian
80
Late
85
90
Turonian
95
125
Barremian
130
135
Valanginian
140
Berriasian
145
Tithonian
150
160
165
170
175
Kimmeridgian
Middle
Callovian
Bathonian
Bajocian
Aalenian
Jurassic
155
Late
Epidendrosaurus
Epidexipteryx
Hauterivian
Sinornithoides
Jinfengopteryx
Sinovenator
Mei
Early
Anchiornis
Eosinopteryx
Aptian
120
Xiaotingia
115
Wellnhoferia
Archaeopteryx
Albian
Jeholornis
110
Sapeornis
Confuciusornis
Protopteryx
Yanornis
105
Cenomanian
Cretaceous
100
Santonian
Coniacian
Oxfordian
Avialae
Troodontidae
Deinonychosauria
Figure 3 | Phylogeny of Paraves. Time-calibrated strict consensus tree of the 10 most-parsimonious trees. Tree length ¼ 1,386; consistency index (CI)
excluding uninformative characters ¼ 0.3; retention index (RI) ¼ 0.7. We added four feather-related characters to the original matrix3 but these do not
influence the topology of the strict consensus tree. Character 375: remiges on the forelimb absent (0) or present (1); character 376: pennaceous feathers
on the tibia absent (0) or present (1); character 377: feathers on metatarsus and pes absent (0) or present (1); character 378: rectrices absent (0) or
present (1).
4
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ARTICLE
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basal avialans, the basal deinonychosaurians Archaeopteryx and
Wellnhoferia6, the basal troodontid Anchiornis18, the
scansoriopterygid Epidexipteryx19 and the basal dromaeosaurid
Microraptor20. The secondary loss of rectrices is regarded here as
an unambiguous autapomorphy for E. brevipenna (Fig. 4).
Pennaceous rectrices attached to the tibia were also a relatively
ubiquotous adaptation among maniraptorans, present in
Eosinopteryx, Anchiornis2, Xiaotingia3, Microraptor15, Pedopenna21,
Archaeopteryx and Wellnhoferia6; this character is regarded here as
an unambiguous synapomorphy for Deinonychosauria (Fig. 4).
In this phylogeny, the presence of long feathers on the
metatarsus and pes, observed in Anchiornis2, Xiaotingia3 and
Microraptor16, is regarded as an unambiguous synapomorphy for
the clade Troodontidae þ Dromaeosauridae, and their secondary
loss an unambiguous autapomorphy for Eosinopteryx (Fig. 4). It
cannot be totally excluded that the absence of pennaceous
feathers on the metatarsus and pes of Eosinopteryx is a
preservational artefact, because other integumental features (for
example, scales or scutes) are not preserved at the same location.
However, scutes and scales on the lower leg have never been
identified in any feathered dinosaur or Mesozoic bird described to
date. Despite its small size, the holotype of Eosinopteryx had
reached a late ontogenetic stage (subadult or adult): neurocentral
sutures are closed on all exposed vertebrae (Supplementary
Fig. S4) and the suture between the astragalus–calcaneum
Feathers on metatarsus and pes (377)
Rectrices (378)
Sinosauropteryx
0
0
0
0
Caudipteryx
1
0
0
1
Similicaudipteryx
1
0
0
1
Epidendrosaurus
?
?
?
?
Epidexipteryx
0
0
0
1
Jeholornis
1
0
0
1
Sapeornis
1
0
0
1
Confuciusornis
1
0
0
1
Remiges on forelimb (375)
Pennaceous feathers on tibia (376)
complex and the tibia cannot be discerned (Supplementary Fig.
S5). Ontogenetic stage, therefore, also cannot account for reduced
plumage, although temporary disappearance of rectrices and
pennaceous feathers on the metatarsus and pes might be
explained by a seasonal moult.
It is parsimonious that the plumage differences of Eosinopteryx
can be explained by its mode-of-life. With a shorter humerus and
manus and a reduced plumage, Eosinopteryx had a much shorter
wing span than other feathered paravians including Archaeopteryx, Wellnhoferia and Anchiornis. The straight and closely
aligned ulna-radius of Eosinopteryx also means that pronation/
supination of the manus with respect to the upper arm would
have been limited; combined with the absence of a bony sternum
and weakly developed proximal humerus, these attributes suggest
that Eosinopteryx had little or no ability to oscillate the arms to
produce a wing beat. The phalanges of the third toe of
Eosinopteryx decrease proximodistally and its ungual phalanges
are not very recurved and particularly short, suggesting a ground
dwelling, ‘cursorial’ mode-of-life as in many living birds15.
Reduced plumage on the tail and lower legs would have facilitated
this ecology and allowed Eosinopteryx to run easily. This new
specimen also shows that the plumage of paravian theropods was
already diversified by the Late Jurassic and already had different
functions: insulation, flight and visual display19,20. Although
Anchiornis and Eosinopteryx are clearly similar from osteological
375 378
1
1
375 (FO)
375 (SO)
0
0
377
376
0
378
0
1
377
1
Protopteryx
1
0
0
1
Yanornis
?
?
?
?
Archaeopteryx
1
1
0
1
Wellnhoferia
1
?
?
?
Xiaotingia
1
1
1
?
Anchiornis
1
1
1
1
Eosinopteryx
1
1
0
0
Jinfengopteryx
1
?
?
1
Sinovenator
?
?
?
?
Mei
?
?
?
?
?
Byronosaurus
?
?
?
Sinornithoides
?
?
?
?
Troodon
?
?
?
?
Saurornithoides
?
?
?
?
Zanabazar
?
?
?
?
Microraptor
1
1
1
1
Figure 4 |
Mapping of feather characters onto a simplified strict consensus tree. FO, fast optimization. SO, slow optimization. If not denoted, mapping
is unambiguous.
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ARTICLE
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms2389
and phylogenetic points-of-view, their plumage shows that they
were adapted to different ecological niches and implies a much
more complex picture in terms of the origin of flight than often
supposed. Indeed, it is likely that the diversification of
integumental structures facilitated the sympatry of numerous
closely related paravian theropods in the Late Jurassic Tiaojishan
Formation and later in the Early Cretaceous Jehol Group.
Methods
Origin and authenticity of the specimen. As it is the case for most of the paravian
specimens known from western Liaoning Province, the holotype and only known
specimen of E. brevipenna was acquired by the Yizhou Fossil & Geology Park from
a Chinese fossil dealer, according to whom the specimen was collected at the
Yaolugou locality (Jianchang county, western Liaoning, China), not far from
Daxishan village where A. huxlei specimen LPM (Liaoning Paleontological
Museum)-B00169 was discovered2. The Tiaojishan formation is widely exposed in
this area22, though it also has limited outcrops of the Early Cretaceous Yixian
Formation23. The E. brevipenna specimen is preserved in a shale slab, the
sedimentary structures of which closely resemble those of the specimens of
A. huxlei and Xiaotingia zhengi also described from the Tiaojishan Formation; it is
in fact extremely difficult to distinguish between Tiaojishan and Yixian shale slabs
on the basis of macro-sedimentary features. It is, therefore, necessary to study in
detail the micro-sedimentary structures and the pollen assemblages within the
shale slabs to certify the age of the specimen, as it is also the case for the A. huxlei
and Xioatingia zhengi specimens described so far3.
The specimen was only partially prepared when it was sold by the Chinese
dealer. Careful preparation by the Yizhou Fossil & Geology Park staff and by
authors of this paper (FE and PG) did not reveal any trace of forgery, and the
probability that the specimen is a composite is accordingly low.
Age of the Tiaojishan Formation. The Tiaojishan Formation crops out in the
West Liaoning Province and is equivalent to the Lanqi Formation of North Hebei
Province24. The reason for the abundance of excellently preserved fossils is the
presence of interbedded tuffs originating from recurrent volcanic events25. In
western Liaoning, the Tiaojishan Formation is 130–970 m thick25 and is composed
of different types of rocks, including basalts, andesites, rhyolites, tuffs, tuffaceous
sandstones and conglomerates24,25. Because of the complicated stratigraphic
pattern in the Tiaojishan Formation, accurate dating of the formation is
particularly difficult24. Ages between 165±1.2 Ma and 153±2 Ma were obtained
by SHRIMP U-Th-Pb analysis of samples from the Tiaojishan ( ¼ Lanqi)
Formation26. Zhang et al.24 concluded that the upper boundary of the Tiaojishan
( ¼ Lanqi) formation dates between 156 and 153 Ma. Chang et al.25 obtained Ar-Ar
ages of 160.7±0.4 Ma and 158.7±0.6 Ma for the basal Lanqi Formation in North
Hebei Province. These results indicate that the age of the Tiaojishan Formation is
between the Callovian (Middle Jurassic) and the Kimmeridgian (Late Jurassic)27.
Nomenclatural acts. This published work and the nomenclatural acts it contains
have been registered in ZooBank, the proposed online registration system for the
International Code of Zoological Nomenclature. The ZooBank LSIDs (Life Science
Identifiers) can be resolved and the associated information viewed through any
standard web browser by appending the LSID to the prefix ‘http://zoobank.org/’.
The LSIDs for this publication are: urn:lsid:zoobank.org:act:068F0446-C80D-4F90837C-921AB291880F; urn:lsid:zoobank.org:pub:11EEC3B6-1BF7-4DDE-872FC84DE2CBBA20.
Acknowledgements
We thank B. Pohl and D. Leloup for making fossils available for study, Sun Ge and
A. Cau for their help and comments on the manuscript, T. Hubin for the photographs
and four referees for their helpful comments. This study was supported by a grant (BL/
36/62) to P.G. from the SPP Politique Scientifique (Belgium). D.H. was supported by the
Key Laboratory of Evolutionary Systematics of Vertebrates (CAS2011LESV011) and by
the National Natural Science Foundation of China (41172026).
Author contributions
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Additional information
Supplementary Information accompanies this paper at http://www.nature.com/
naturecommunications
Competing financial interests: The authors declare no competing financial interests.
Reprints and permission information is available online at http://npg.nature.com/
reprintsandpermissions/
How to cite this article: Godefroit, P. et al. Reduced plumage and flight ability of a new
Jurassic paravian theropod from China. Nat. Commun. 4:1394 doi: 10.1038/ncomms2389
(2013).
NATURE COMMUNICATIONS | 4:1394 | DOI: 10.1038/ncomms2389 | www.nature.com/naturecommunications
& 2013 Macmillan Publishers Limited. All rights reserved.
Supplementary Information
Supplementary Figures
Supplementary Figure S1 Pectoral girdle of Eosinopteryx brevipenna YFGP-T5197. Abbreviations:
fu, furcula; ls, left scapula; rcor, right coracoid; rs, right scapula.
Supplementary Figure S2 Right manus of Eosinopteryx brevipenna YFGP-T5197. Abbreviations: mc,
metacarpal.
Supplementary Figure S3 Position of Eosinopteryx brevipinna within Paraves as a result of the
inclusion of Eosinopteryx in a recently published analysis of coelurosaurian phylogeny3. Strict
consensus tree of 10 MPT's. Tree Length = 1386; CI excluding uninformative characters = 0.3; RI = 0.7.
Nodal support (Bremer indices) is indicated above each branch. The number below each branch refers to
the different clades of the phylogeny.
Supplementary Figure S4 Proximal caudal vertebrae of Eosinopteryx brevipenna YFGP-T5197
Supplementary Figure S5 Distal part of right tibiotarsus of Eosinopteryx brevipenna YFGP-T5197
Supplementary Tables
Supplementary Table S1. Skeletal measurents of YFGP-T5197
skull
mandible
snout
cervical series
dorsal series
sacral series
caudal series
scapula
humerus
ulna
radius
manus
ilium
pubis
ischium
femur
tibiotarsus
metatarsus
pes phalanx III-1
pes phalanx III-2
pes phalanx III-3
pes phalanx III-4
forelimb
hindlimb
Length
(mm)
43.2
40.2
21.4
39.6
57.9
25.1
131.5
23.8
37.9
42
39.5
56.8
25
35
13.4
48.5
69.5
35.5
8.8
7.1
6.5
6
134.2
183.1
Width middle
(mm)
/
/
/
/
/
/
/
2.5
3.7
2
1.9
/
/
1.9
4.8
4.5
/
/
/
/
/
/
/
Supplementary Table S2. Measurements of YFGP-T5197 caudal vertebrae
N°
Length (mm)
Width middle
(mm)
Width caudal
end (mm)
1
/
/
/
2
/
/
/
3
/
/
/
4
5.7
3
/
5
5.6
2.8
3.7
6
5.8
2.8
3.7
7
6.4
2.8
4.4
8
6.4
2.8
4.4
9
6.4
2.8
4.4
10
7.6
2.8
3.8
11
9.6
2.5
3.5
12
9.6
1.7
3.3
13
8.8
1.7
3.3
14
8
1.5
2.2
15
7.6
1.5
2.2
16
8
1.5
2.2
17
8
1.5
2.2
18
7.4
1.2
1.8
19
6.3
1.2
1.8
20
9.2
1.2
/
Supplementary Table S3. Relative proportions of selected elements in basal
Deinonychosauria and Troodontidae
skull length/
femur length
neck length/
hindlimb length
trunk length/
hindlimb length
tail length/
femur length
scapula length/
femur length
humerus length/
femur length
radius length/
femur length
manus length/
femur length
tibiotarsus
length/
femur length
pes length/
femur length
forelimb length/
hindlimb length
Eosinopteryx
YFGP-T5197
0.89
Archaeopteryx
HMN/1880/81
0.99
Wellnhoferia
BMMS 500
0.97
Anchiornis
PMOL-B00169
0.96
Xiaotingia
STM 27-2
0.72
Mei
IVPP-V12733
0.65
0.22
0.33
-
0.24
-
0.23
0.32
0.42
-
0.31
-
0.32
2.71
3.27
-
-
-
3.17
0.49
+/- 0.7
-
0.68
0.65
0.56
0.79
1.21
1.24
1.04
0.85
0.52
0.81
1.03
1.03
0.81
0.75
0.48
1.17
1.48
1.48
1.55
-
0.83
1.43
1.3
1.37
1.61
-
1.31
1.34
1.18
1.2
1.56
-
1.3
0.73
1
0.99
0.8
-
0.5
Abbreviations: BMMS, Bürgermeister Müller Museum,Solnhofen, Germany; HMN, Museum für
Naturkunde, Humboldt University, Berlin, Germany; IVPP, Institute of Vertebrate Paleontolohy and
Paleoanthropology, Beijing, China; PMOL, Paleontological Museum of Liaoning, Shenyang, China;
STM, Shandong Tianyu Musem of Nature, Shandong, China; YFGP, Yizhou Fossil & Geology Park,
Yizhou, China.
Supplementary Methods
Phylogenetic nomenclature. We follow, in this paper, the following definition of higher-level theropod
taxa3, 19:
- Coelurosauria, the most inclusive clade containing Passer domesticus Linnaeus 1758 but not
Allosaurus fragilis Marsh 1877, Sinraptor dongi Currie and Zhao 1993, and
Carcharodontosaurus saharicus Depéret and Savornin 1927.
-
Paraves, the most inclusive clade containing Passer domesticus Linnaeus 1758 but not Oviraptor
philoceratops Osborn 1924.
-
Avialae, the most-inclusive clade containing Passer domesticus Linnaeus 1758 but not
Dromaeosaurus albertensis Matthew and Brown 1922 or Troodon formosus Leidy 1956.
-
Deinonychosauria, the most-inclusive clade containing Dromaeosaurus albertensis Matthew and
Brown 1922 but not Passer domesticus Linnaeus 1758.
-
Archaeopterygidae, the most inclusive clade including Archaeopteryx lithographica Meyer 1861
but not Dromaeosaurus albertensis Matthew and Brown 1922 or Passer domesticus Linnaeus
1758.
-
Scansoriopterygidae, the most inclusive clade including Epidendrosaurus Zhang et al., 2002 but
not Passer domesticus Linnaeus 1758 or Dromaeosaurus albertensis Matthew and Brown 1922.
Phylogenetic analysis. In order to assess its likely phylogenetic relationships, Eosinopteryx brevipenna
was included in the dataset from a recently published analysis of coelurosaurian phylogeny3. We also
added to this analysis Jinfengopteryx elegans, a paravian from the Early Cretaceous Qiaotou Formation of
Hebei Province (China) initially regarded as the sister-taxon for Archaeopteryx28. We also included four
additional characters in our analysis that are related to the development of the plumage:
-
Character 375. Remiges on the forelimb: absent (0), or present (1).
-
Character 376: Pennaceous feathers on the tibia: absent (0), or present (1).
-
Character 377: Feathers on metatarsus and pes: absent (0), or present (1).
-
Character 378. Rectrices: absent (0), or present (1).
The data matrix was re-analysed using the TNT software package29. The following heuristic
search settings were used to generate most-parsimonious trees (MPTs): hold 30,000 trees, 1,000 Wagner
builds, retain 10 trees per replication, with tree bisection and reconnection (TBR) as the search strategy.
Heuristic searches recovered 8 Most Parsimonious Trees (MPTs) of length 1395 steps, with a Consistency
index (CI) excluding uninformative characters = 0.3, and a Retention index (RI) = 0.7. Bremer indices
were calculated by re-running the analysis and saving all sub-optimal trees not more than 10 steps longer
than the MPTs. The strict consensus tree and relative nodal support are shown in Figure S6. For clarity,
only paravian taxa are depicted in Figure S6. The inclusion of the four feather-related features in the
analysis has no influence on either the topology or the robustness of the resulting strict consensus tree
(Figure S7).
The strict consensus tree (Figure S6) shows that Eosinopteryx brevipenna is the sister taxon of
Anchiornis huxleyi . Together with Xiatingia zhengi, also from the Tiaojichan Formation of western
Liaoning, these taxa are the most basal members of the clade Troodontidae described so far.
Jinfengopteryx elegans, Sinovenator changii and Mei long, all from the Early Cretaceous Jehol Biota of
northeastern China, are successively later derived troodontids. Archaeopteryx and Wellnhoferia form an
unresolved polytomy at the base of the clade Deinonychosauria and Scansoriopterygidae are here
regarded as the most basal members of the clade Paraves. The results of our phylogenetic analysis
therefore support the hypothesis that Archaeopteryx, Wellnhoferia, Anchiornis, and Eosinopteryx are all
deinonychosaurs rather than primitive Avialae3. Bremer indices are generally higher than in the original
analysis, before including Eosinopteryx and Jinfengopteryx3.
We inferred polarity and optimized the four feather-related characters onto the consensus tree
using WINCLADA version 1.00.0830. This is shown in Figure S7. The presence of pennaceous feathers
on the tibia is regarded here as an unambiguous synapomorphy for Deinonychosauria. The presence of
feathers on the metatarsus and pes is an unambiguous synapomorphy for the clade Troodontidae +
Dromaeosauridae and confirms that the secondary loss of rectrices and feathers on the metatarsus and pes
are unambiguous (observed under both fast and slow optimizations) autapomorphies for Eosinopteryx
brevipenna.
Matrix. Our phylogenetic analysis is based on a matrix published in a recently published phylogeny of
Coelurosauria4 (doi:10.1038/nature10288). Several character state have been modified in Anchiornis
huxleyi, based on direct observations on the specimen LPM-B00169. Four feather-related characters (375378, see above) were added to the original matrix3.
Anchiornis huxleyi
001100?????????????11010??111?00?????0?1?000??1????1?1??????????+000??01??1?????00020?+01?
?0?101??+00?0??010?01???01101210??011+++011?31110000??1000000010?21?1001102200?2?11211
2???1?1?000??1?01?000121100010?1000?1??00?0???0????030010?1101000100100?01?0???0+0?01111
1101?00011020110101000101???0??1?11?102001011?1011000?20?1100001000?121000?00000110101
?0??0000000000100000110 1111
Eosinopteryx brevipenna
?011?????????????????0????????0????????1?????????????????????????00???01????????00020++?1??0?
?????????????????????01??1?30?0?1?????0??01??1?????????0000?000?1??0???022???2?1?2??0???????
???????????0???1???0?0???00????0??????0?????3001??11????0??????????0???0+0?0??????0?????1?02
0?0??0100????10100??11???02???01??1???0???????010?010?0?12100????00?1??1???????????00?????0
??01??1100
Jinfengopteryx elegans
?011???????????????1?01???11100??????001??0??1????????????????????000?1???????0?00020??011?1
???????????????0??????0210?210?0011?????01?31?11?00??10?0000?000??????????????????11??1????
1???0??????1?????0???0?1???00????000????000?0030010011000?0100100?01?0???0?0?01?1??101?10
?1?11010???100?0??010?000001020?????1??1?????????????1?01??????1??0???00?1??????????0????01
00?00?001?01??1
List of the unambiguous synapomorphies supporting the nodes shared by all MPTs. Character
numeration refers to the Character list a recently published phylogeny of Coelurosauria3
(doi:10.1038/nature10288). Nodes numeration refers to Figure S6.
Node 1 (Paraves): 122 (0 1), 137 (0 1), 139 (0 1), 155 (0 1), 184 (0 1), 197 (0 1), 202
(0 1), 232 (1 0), 267 (0 1), 274 (1 2), 277 (1 2or3), 317 (0 1), 318 (0 1), 320 (0 2),
336 (0 1), 362 (0 1)
Node 2: 171 (1 3), 175 (1 0), 176 (1 2), 217 (0 1), 348 (0 1), 360 (0 1), 361 (0 1)
Node 3: 66 (0 1), 91 (1 0), 136 (0 3), 138 (0 1), 165 (0 1), 166 (1 0), 235 (0 1), 262
(0 1), 270 (0 3), 277 (0 3), 280 (0 1), 294 (0 1), 304 (0 2), 319 (0 1)
Node 4 (Avaliae): 110 (0 1), 147 (0 1), 175 (0 2), 285 (0 1), 288 (1 0), 290 (0 1), 291
(0 1), 324 (0 1), 327 (0 1)
Node 5: 110 (0 2), 121 (0 2), 195 (0 1), 278 (0 1), 296 (0 1)
Node 6: 125 (0 1), 126 (0 1), 175 (2 3), 176 (1 2), 188 (0 1), 192 (0 1)
Node 7: 52 (0 1), 244 (0 1), 268 (0 1), 324 (1 0), 368 (1 0)
Node 8 (Deinonychosauria): 72 (0 1), 85 (2 0), 134 (0 1), 200 (0 1), 233 (0 1), 238 (1 0),
300 (0 1), 302 (0 2), 323 (0 1), 334 (0 1), 335 (1 2), 359 (1 0), 364 (1 0), 365 (1 0),
366 (0 1), 367 (1 0), 368 (1 0), 372 (0 1), 376 (0 1)
Node 9: 54 (0 1), 62 (1 0), 64 (1 0), 75 (0 1), 76 (0 1), 116 (0 1), 122 (1 0), 126 (0 1),
141 (0 1), 197 (1 0), 274 (0 1), 277 (0 2), 280 (1 0), 292 (1 0), 318 (1 0), 320 (1 0),
333 (0 1), 377 (0 1)
Node 10 (Troodontidae): 52 (0 1), 89 (0 1), 165 (1 0), 211 (1 0), 269 (0 1), 373 (0 1)
Node 11: 155 (1 0), 156 (1 0), 230 (0 3), 294 (1 0), 362 (1 0)
Node 12: 166 (1 0), 276 (1 0), 299 (0 1), 363 (1 0)
Node 13: 277 (0 1), 297 (1 0)
Node 14: 85 (0 1), 136 (0 1), 232 (0 1), 269 (1 0), 300 (1 0), 374 (0 1)
Node 15: 205 (0 1)
Node 16: 38 (0 2)
Node 17: 23 (1 0), 84 (0 1)
Node 18: 66 (0 1), 120 (1 0), 246 (1 0), 318 (0 1), 346 (1 0)
Node 19 (Dromaeosauridae): 21 (1 0), 43 (0 1), 88 (0 1), 103 (0 1), 123 (0 2), 198 (0 1),
202 (1 0) , 240 (0 1), 262 (1 0), 305 (0 1), 332 (0 1), 342 (0 1)
Node 20: 53 (1 0), 72 (1 0), 84 (2 1), 96 (1 0), 107 (1 0), 120 (2 1), 155 (1 0), 165
(1 0), 175 (1 2), 240 (0 3), 253 (0 1), 270 (1 0)
Node 21: 176 (1 2), 202 (0 1), 278 (0 1), 285 (0 1), 288 (1 0), 290 (0 1), 295 (0 1), 308
(0 1), 320 (0 2)
Node 22: 99 (1 2), 171 (2 1), 233 (1 0), 305 (1 0), 334 (1 0), 335 (2 1), 346 (1 0), 362
(1 0)
Node 23: 200 (1 0), 243 (1 0), 321 (0 1)
Node 24: 256 (0 1)
Node 25: 78 (0 1), 253 (1 0), 264 (1 0), 333 (1 0)
Node 26: 84 (1 0), 167 (2 1), 254 (0 1), 266 (1 0), 309 (1 0), 330 (2 0)
Node 27: 258 (1 0)
Supplementary References
28. Ji, Q., Ji, S., Lü, J., You, H., Chen, W., Liu, Y. and Liu, Y., 2005. First avialian bird from China
(Jinfengopteryx elegans gen. et sp. nov.). Geological Bulletin of China 24: 197-210.
29. Goloboff, P.A., Farris, J. and Nixon, K.C. TNT, a free program for phylogenetic analysis.
Cladistics 24, 774-786 (2008).
30. K. C. Nixon, WinClada ver. 1.00.08 (Published by the author, Ithaca, New York, 2004).