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A Feathered Dinosaur Tail with Primitive Plumage Trapped in Mid-Cretaceous Amber

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In the two decades since the discovery of feathered dinosaurs [1-3], the range of plumage known from non-avialan theropods has expanded significantly, confirming several features predicted by developmentally informed models of feather evolution [4-10]. However, three-dimensional feather morphology and evolutionary patterns remain difficult to interpret, due to compression in sedimentary rocks [9, 11]. Recent discoveries in Cretaceous amber from Canada, France, Japan, Lebanon, Myanmar, and the United States [12-18] reveal much finer levels of structural detail, but taxonomic placement is uncertain because plumage is rarely associated with identifiable skeletal material [14]. Here we describe the feathered tail of a non-avialan theropod preserved in mid-Cretaceous (∼99 Ma) amber from Kachin State, Myanmar [17], with plumage structure that directly informs the evolutionary developmental pathway of feathers. This specimen provides an opportunity to document pristine feathers in direct association with a putative juvenile coelurosaur, preserving fine morphological details, including the spatial arrangement of follicles and feathers on the body, and micrometer-scale features of the plumage. Many feathers exhibit a short, slender rachis with alternating barbs and a uniform series of contiguous barbules, supporting the developmental hypothesis that barbs already possessed barbules when they fused to form the rachis [19]. Beneath the feathers, carbonized soft tissues offer a glimpse of preservational potential and history for the inclusion; abundant Fe(2+) suggests that vestiges of primary hemoglobin and ferritin remain trapped within the tail. The new finding highlights the unique preservation potential of amber for understanding the morphology and evolution of coelurosaurian integumentary structures.
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Report
A Feathered Dinosaur Tail with Primitive Plumage
Trapped in Mid-Cretaceous Amber
Highlights
dThe first non-avialan theropod fragments preserved in amber
are described
dVertebral outlines, curvature, and plumage suggest a source
within Coelurosauria
dBranching structure in the feathers supports a barbule-first
evolutionary pattern
dIron within carbonized soft tissue suggests traces of original
material are present
Authors
Lida Xing, Ryan C. McKellar,
Xing Xu, ..., Kuowei Tseng, Hao Ran,
Philip J. Currie
Correspondence
xinglida@gmail.com (L.X.),
ryan.mckellar@gov.sk.ca (R.C.M.)
In Brief
Xing et al. describe the tail of a non-
avialan theropod (coelurosaur) preserved
in Burmese amber, combining bone
outlines with microscopic details of
plumage and integument. This specimen
sheds new light on the appearance and
evolution of plumage of dinosaurs,
providing a direct association between
amber-entombed plumage and body
fossil material.
Xing et al., 2016, Current Biology 26, 3352–3360
December 19, 2016 ª2016 Elsevier Ltd.
http://dx.doi.org/10.1016/j.cub.2016.10.008
Current Biology
Report
A Feathered Dinosaur Tail with Primitive Plumage
Trapped in Mid-Cretaceous Amber
Lida Xing,
1,2,13,
*Ryan C. McKellar,
3,4,13,14,
*Xing Xu,
5,13
Gang Li,
6,13
Ming Bai,
7,13
W. Scott Persons IV,
8
Tetsuto Miyashita,
8
Michael J. Benton,
9
Jianping Zhang,
2
Alexander P. Wolfe,
8
Qiru Yi,
6
Kuowei Tseng,
10,11
Hao Ran,
12
and Philip J. Currie
8
1
State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing 100083, China
2
School of the Earth Sciences and Resources, China University of Geosciences, Beijing 100083, China
3
Royal Saskatchewan Museum, Regina, Saskatchewan S4P 4W7, Canada
4
Biology Department, University of Regina, Regina, Saskatchewan S4S 0A2, Canada
5
Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy
of Sciences, Beijing 100044, China
6
Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese Academy of Science, Beijing 100049, China
7
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
8
Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada
9
School of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK
10
Department of Exercise and Health Science, University of Taipei, Taipei 11153, China
11
Department of Geology, Chinese Culture University, Taipei 11114, China
12
Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection, Ministry of Education, Guilin 541004, China
13
Co-first author
14
Lead Contact
*Correspondence: xinglida@gmail.com (L.X.), ryan.mckellar@gov.sk.ca (R.C.M.)
http://dx.doi.org/10.1016/j.cub.2016.10.008
SUMMARY
In the two decades since the discovery of feathered
dinosaurs [1–3], the range of plumage known
from non-avialan theropods has expanded signifi-
cantly, confirming several features predicted by
developmentally informed models of feather evolu-
tion [4–10]. However, three-dimensional feather
morphology and evolutionary patterns remain diffi-
cult to interpret, due to compression in sedimen-
tary rocks [9, 11]. Recent discoveries in Cretaceous
amber from Canada, France, Japan, Lebanon,
Myanmar, and the United States [12–18] reveal
much finer levels of structural detail, but taxonomic
placement is uncertain because plumage is rarely
associated with identifiable skeletal material [14].
Here we describe the feathered tail of a non-avialan
theropod preserved in mid-Cretaceous (99 Ma)
amber from Kachin State, Myanmar [17], with
plumage structure that directly informs the evolu-
tionary developmental pathway of feathers. This
specimen provides an opportunity to document pris-
tine feathers in direct association with a putative
juvenile coelurosaur, preserving fine morphological
details, including the spatial arrangement of follicles
and feathers on the body, and micrometer-scale fea-
tures of the plumage. Many feathers exhibit a short,
slender rachis with alternating barbs and a uniform
series of contiguous barbules, supporting the devel-
opmental hypothesis that barbs already possessed
barbules when they fused to form the rachis [19].
Beneath the feathers, carbonized soft tissues offer
a glimpse of preservational potential and history for
the inclusion; abundant Fe
2+
suggests that vestiges
of primary hemoglobin and ferritin remain trapped
within the tail. The new finding highlights the unique
preservation potential of amber for understanding
the morphology and evolution of coelurosaurian
integumentary structures.
RESULTS AND DISCUSSION
Preservation
The tail within DIP-V-15103 is visible to the naked eye as an elon-
gate and gently curved structure (length = 36.73 mm). A dense
covering of feathers protrudes from the tail, obscuring underlying
details, so Synchrotron Radiation (SR) X-ray phase-contrast
mCT scanning was employed to examine concealed osteological
and soft tissue features (Figure 1). Soft tissues—presumably
muscles, ligaments, and skin—are visible sporadically through
the plumage, clinging to the bones in a manner suggestive
of the desiccation common to other vertebrate remains in
amber [20]. These tissues have largely been reduced to a carbon
film, retaining only traces of their original chemical composition.
Based on analyses further described in the Supplemental Infor-
mation,SRm-XFI shows that iron is present in the carbonized
soft tissues and as a series of fine linear features corresponding
to exposed plumage (Figure 2). Copper is slightly more abundant
in amber containing plumage, but this signal is cryptic and not a
clear indicator for preserved pigments. Elements such as Ca, Sc,
Zn, Ti, Ge, and Mn appear to be associated with clay minerals
filling voids in the amber. We derived the valence state of iron
in the sample qualitatively by comparison to the standard XAS
of Fe foil, Fe
2
O
3
,Fe
3
O
4
, and FeO. Our calculations indicate
that more than 80% of iron in the sample is ferrous (Fe
2+
). Similar
measurements have been made on vessels preserved within
3352 Current Biology 26, 3352–3360, December 19, 2016 ª2016 Elsevier Ltd.
Figure 1. Photomicrographs and SR X-Ray mCT Reconstructions of DIP-V-15103
(A) Dorsolateral overview.
(B) Ventrolateral overview with decay products (bubbles in foreground, staining to lower right).
(C) Caudal exposure of tail showing darker dorsal plumage (top), milky amber, and exposed carbon film around vertebrae (center).
(D–H) Reconstructions focusing on dorsolateral, detailed dorsal, ventrolateral, detailed ventral, and detailed lateral aspects of tail, respectively.
(legend continued on next page)
Current Biology 26, 3352–3360, December 19, 2016 3353
Tyrannosaurus and Brachylophosaurus bones and have been in-
terpreted as indicating the presence of goethite and biogenic
iron oxides produced from hemoglobin decomposition [21].
The presence of large quantities of Fe
2+
in DIP-V-15103 sug-
gests that some primary iron from hemoglobin or ferritin remains
trapped within the inclusion. SEM analyses show that pyrite
(FeS
2
) is also present, but not as a significant contributor to the
distribution of iron within the specimen (Figure S3).
The close contact between the skin and surrounding amber,
paired with the mummified external appearance of the skin
where it has shriveled across the surface of the vertebrae, sug-
gest one of two scenarios. Either the tail bearer was dead and
partially desiccated before encapsulation, or else it rapidly dried
due to resin interactions. Early-stage drying is further supported
by the limited amount of cloudy amber surrounding the tail (Fig-
ures 1C and S2), which is a preservational feature related to
decay products or moisture interacting with resin [22]. However,
drying and resin impregnation were not sufficient to preserve
cellular detail in the soft tissues. Based on the clays observed
where bone breaches the amber surface, skeletal material was
likely exposed on the surface after resin polymerization. The
bone has been partially dissolved and infilled with clay from
the surrounding matrix [17], much like insect body cavities in
this deposit (Figure S2A). Presence of Fe
2+
within the carbonized
remains suggests that organic components were trapped early
and remained undisturbed by subsequent events. Further taph-
onomic constraints are difficult to infer. It is unclear whether the
lack of melanosomes within the keratin sheets of the surrounding
feathers (Figures 2B and S3) might provide additional tapho-
nomic information or whether their absence results from weakly
pigmented feathers or the small sample area available for
SEM analyses. Artificial maturation experiments [23] have
shown the breakdown of modern melanosomes at a range of
temperatures, but this work was conducted at temperatures
that would also degrade amber. The taphonomic pathway that
led to the preservation of DIP-V-15103 is not entirely clear, but
it suggests promise for more detailed examinations of organics
or pigmentation in vertebrate inclusions.
Osteology
SR X-ray mCT scanning of DIP-V-15103 (Figure 1) revealed that
soft tissues have a density insufficiently different from the
partially replaced skeletal elements to permit X-ray imaging
and virtual dissection of osteology alone. Consequently, many
diagnostic and comparative osteological details remain
obscured. However, two vertebrae are clearly delineated
ventrally (Figures 1F–1H). Extrapolating lengths of these verte-
brae, the preserved tail section contains at least eight full verte-
brae and part of a ninth. The vertebrae are elongate, with antero-
posterior lengths double the maximum diameter of the tail (Table
S1). Vertebral proportions and tail flexion preclude membership
within the Pygostylia [as in 24]. Even with the skin adpressed to
the bony surface, no features other than the grooved ventral sulci
of two centra are clearly visible. This lack of topography suggests
that the vertebrae lack prominent neural arches, transverse pro-
cesses, or hemal arches. Therefore, the preserved segment is
only a small mid to distal portion of what was likely a relatively
long tail, with the total caudal vertebral count not reasonably
less than 15, and likely greater than 25. Based on specimen
size, it also seems likely that the tail belonged to a juvenile.
DIP-V-15103 is interpreted as a non-avialan coelurosaur tail:
its vertebral profiles and estimated length rule out avebrevicau-
dan birds, oviraptorosaurs, and scansoriopterygians—lineages
generally characterized by a short caudal series with subequal
centra [25–27], with the exception of Epidendrosaurus. The
branched feathers have a weak pennaceous arrangement of
barbs consistent with non-avialan coelurosaurs, particularly
paravians. Although the feathers are somewhat pennaceous,
none of the observed osteological features preclude a compsog-
nathid [28] affinity. The presence of pennaceous feathers in pairs
down the length of the tail may point toward a source within Pen-
naraptora [9], placing a lower limit on the specimen’s phyloge-
netic position. However, the distribution and shape of the
feathers only strongly supports placement crownward of basal
coelurosaurs, such as tyrannosaurids and compsognathids. In
terms of an upper limit, the specimen can be confidently
excluded from Pygostylia; in addition, it can likely be excluded
from the long-tailed birds, based on pronounced ventral grooves
on the vertebral centra. Additional taxonomic assessment de-
tails are provided in the Supplemental Information.
Plumage
Both SR X-ray mCT reconstruction and standard light micro-
scopy confirm feather attachments throughout the preserved
tail length (Figure 1). A bilaterally paired series of posterodorsally
oriented feathers extends from the dorsal midline (Figures 1D
and 1E). Another row of feathers is present at mid-height on
each side of the tail, with feathers extending posterolaterally at
roughly 45to its long axis (Figures 1D–1G). These follicle pairs
appear evenly spaced along the length of the tail. Where the out-
lines of two vertebral centra are visible, follicles are located at the
mid-lengths of centra and at intervertebral joints. Ventral
plumage is sparse, consisting of fine feathers that follow the
long axis of the tail closely (Figures 1B, 1G, and 1H). Overall,
the plumage forms laterally directed keels on either side of the
vertebral column, providing a unique opportunity to observe
feather counts and orientations within the contour-like caudal
plumage of a coelurosaur. DIP-V-15103 does not show the
splaying of large pennaceous rectrices observed alongside the
posteriormost caudals of long-tailed birds [29]. Either splaying
was absent in this individual or it was only present caudally,
beyond the preserved region. Nevertheless, the arrangement
of feathers into lateral keels in DIP-V-15103 is similar to the para-
vian tail fan or frond [9]. Such arrangements, composed of
different feather types, can occur not just at the distal tip but
also along the entire length of the tail. Amber preservation
Arrowheads in (A) and (D) mark rachis of feather featured in Figure 4A. Asterisks in (A) and (C) indicate carbonized film (soft tissue) exposure. Arrows in (B) and
(E)–(G) indicate shared landmark, plus bubbles exaggerating rachis dimensions; brackets in (G) and (H) delineate two vertebrae with clear transverse expansion
and curvature of tail at articulation. Abbreviations for feather rachises: d, dorsal; dl, dorsalmost lateral; vl, ventralmost lateral; v, ventral. Scale bars, 5 mm in (A),
(B), (D), and (F) and 2 mm in (C), (E), (G), and (H). See also Figure S2.
3354 Current Biology 26, 3352–3360, December 19, 2016
suggests that the tail fans and fronds preserved in paravians are
not merely a taphonomic artifact of compression.
If DIP-V-15103 indeed represents a juvenile coelurosaur tail,
the feathers most likely characterize adult plumage; however,
there is some room for uncertainty. Basal taxa within Pennarap-
tora, such as Similicaudipteryx, are thought to have undergone
dramatic molts that affected the tail region [8], while some
basal members of Pygostylia have precocial juveniles with
adult-like plumage [14]. The pennaceous feathers and bar-
bules of DIP-V-15103 suggest an adult-like plumage, in which
Figure 2. SR m-XFI Maps and Scanning Electron Micrographs of DIP-V-15103
(A) Elemental maps and region of interest (ROI) image for exposed soft tissue preservation in DIP-V-15103; black carbon film surrounds clay minerals infilling void
between vertebrae or partially replacing them; milky amber related to decay surrounds vertebrae and plumage (ROI prior to clay flake removal is better visible in
Figure S3H).
(B) Patchy keratin preservation with traces of fibrous structure in DIP-V-15103 ventral feather.
(C) Fibrous keratin sheets and isolated melanosomes from barb of modern Indian peafowl (Pavo cristatus; Galliformes).
Scale bars, 2 mm in (A) and 1 mm in (B) and (C). See also Figure S3.
Current Biology 26, 3352–3360, December 19, 2016 3355
feathers would not have been replaced by different morpho-
types in subsequent molts. Alternatively, the feather bearer
may not have conformed to the molt patterns found in modern
birds.
The feathers of DIP-V-15103 are similar to each other in
morphology, regardless of position on the tail (Figures 3 and
S4). All preserved feathers have a weakly defined rachis that is
nearly indistinguishable from the barb rami apically and that is
Figure 3. Photomicrographs of DIP-V-15103 Plumage
(A) Pale ventral feather in transmitted light (arrow indicates rachis apex).
(B) Dark-field image of (A), highlighting structure and visible color.
(C) Dark dorsal feather in transmitted light, apex toward bottom of image.
(D) Base of ventral feather (arrow) with weakly developed rachis.
(E) Pigment distribution and microstructure of barbules in (C), with white lines pointing to pigmented regions of barbules.
(F–H) Barbule structure variation and pigmentation, among barbs, and ‘rachis’ with rachidial barbules (near arrows); images from apical, mid-feather, and basal
positions respectively.
Scale bars, 1 mm in (A), 0.5 mm in (B)–(E), and 0.25 mm in (F)–(H). See also Figure S4.
3356 Current Biology 26, 3352–3360, December 19, 2016
slightly thickened basally (Figure 3). Both rachises and barbs are
sub-cylindrical in cross-section. Although the rachis thickens
basally, the maximum diameter near the follicle is approximately
three times that of an adjacent barb ramus (Figures 3 and S4).
Feathers near the anterior end of the dorsal series have the
greatest basal expansion observed among the plumage, with
rachis widths approaching 60 mm(Figures 3,4A, and 4B).
Rachises among these feathers become as narrow as 18 mmin
Figure 4. DIP-V-15103 Structural Overview and Feather Evolutionary-Developmental Model Fit
(A and B) Overview of largest and most planar feather on tail (dorsal series, anterior end), with matching interpretive diagram of barbs and barbules. Barbules are
omitted on upper side and on one barb section (near black arrow) to show rachidial barbules and structure; white arrow indicates follicle.
(C) Evolutionary-developmental model and placement of new amber specimen. Brown denotes calamus, blue denotes barb ramus, red denotes barbule, and
purple denotes rachis [as in 5, 12].
Scale bars, 1 mm in (A) and (B).
Current Biology 26, 3352–3360, December 19, 2016 3357
apical positions, while barb rami have widths ranging from 15
to 23 mm. Within individual feathers, barbs are positioned alter-
nately along the rachis, approaching an opposite arrangement
basally, with wide spacing between and a weak planar arrange-
ment (Figure 4). Flexion within the amber indicates that barb rami
were flexible, and the rachis itself was somewhat flexible. The
open, flexible structure of these feathers is more analogous to
modern ornamental feathers than to flight feathers, showing
structural similarities to the distal components of contour
feathers in certain Anseriformes (Figures 3 and S5). The paired
feather arrangement is similar to rectrices in modern birds, sug-
gesting that tracts had become established in basal tail plumage
before pygostyle development, with tail plumage becoming
more specialized over time. If the entire tail bore plumage similar
to that trapped in DIP-V-15103, the feather bearer would likely
have been incapable of flight.
The feathers of DIP-V-15103 display exquisitely preserved
barbules. Strikingly, the simple barbules branch not only within
individual barbs but also unmodified from the rachis (Figures 3,
4,S4G, and S4H). In this regard, the feathers are comparable
to the contours of many modern birds, which also possess
some barbules that originate from the rachis (rachidial barbules),
although usually from the proximal barb base and in reduced
form. In DIP-V-15103, barbules branch in an evenly spaced,
paired, and nearly symmetrical manner. This pattern remains
consistent in both proximal and distal barbules, from proximal
to distal barbs, and along the rachis. Barbules are consistently
blade shaped, with pigmentation outlining five basal cells fol-
lowed by a poorly differentiated pennulum lacking discernible
nodes or nodal protrusions (Figures 3E–3H). Close spacing be-
tween barbules, combined with the orientation of their flattened
surfaces (parallel to the feather’s long axis), yields open-vaned
feathers that are largely pennaceous.
The weakly developed rachis and contiguous barbule branch-
ing in DIP-V-15103 represents a novel combination among
theropods. Within the evolutionary developmental model of
feathers [5], DIP-V-15103 appears to be intermediate
between stages IIIa (rachis with naked barbs) and IIIb (barbs
with barbules, lacking a rachis), but it does not exactly fit stage
IIIa+b (rachis with barbs bearing barbules) (Figure 4C). In
DIP-V-15103, barbs exhibit an alternating arrangement along a
poorly defined rachis, with nearly dichotomous branching
apically, and barbules continue along the surface of the rachis
and barbs. The weakly developed rachis appears to have formed
through fusion of individual barbs that already possessed bar-
bules (stage IIIb) instead of fusion of naked barbs (stage IIIa)
[5]. The barb branching pattern continues largely uninterrupted
toward the follicle, as do the pervasive, undifferentiated bar-
bules. Unless the condition observed in DIP-V-15103 represents
a secondary reduction of the rachis, the evolutionary pathway for
feathers in this coelurosaur may have been through stage IIIb
(barbs with barbules), not stage IIIa (fusion of naked barbs).
Cytological observations of barbule development along the
barb vane ridge support the evolutionary coupling of barbs and
barbules [19, 30]. Feather morphology of DIP-V-15103 contrasts
with the reduced rachis and long, naked, filamentous barbs in
the branched caudal plumage of the dromaeosaurid Sinornitho-
saurus [6, 8] and the therizinosauroid Beipiaosaurus [31]. This
suggests either a greater diversity of tail plumage in coelurosau-
rians than previously suspected or a simplified form of more-
derived pennaceous feathers in DIP-V-15103.
The unusual barbule configuration in DIP-V-15103 suggests
that barbules were primitively distributed evenly throughout
the length of the feather and only later became restricted to
the barbs and proximal rachis and oriented so that their edges
face the feather surfaces, as in modern avians. In modern birds,
barbule cells originate in the subperiderm and merge into a
syncytium on either side of the barb vane ridge [32, 33]. The
symmetrical arrangement of barbules along the barbs in
DIP-V-15103 implies symmetry of barbule cells across the
barb vane ridge. The contiguous barbule branching along the
rachis probably occurs along the barb vane ridge leading to
the apicalmost barb. In the lineage leading to birds, the bar-
bules became spatially restricted to the barbs and the proximal
portion of the rachis, presumably to accommodate increasing
barb number and density related to rigid pennaceous feathers
(stage IIIa+b and/or stage IV) [5]. Alternatively, the barbule
pattern in DIP-V-15103 may represent a highly derived and
potentially experimental character state unrelated to the avian
lineage. Whichever the case, DIP-V-15103 suggests that
non-avialan theropods had a greater variety of feather forms
than predicted from developmental phenotypes in modern
feathers [4, 5, 10].
Traces of pigmentation exist within the entombed plumage.
Discrete bands corresponding to basal cells within each barbule
are visible due to loosely confined pigments (Figures 3C–3H).
Pigmentation is more pronounced within apical portions of
each barbule and in the barb rami and rachis of dorsal feathers
(Figures 1C and S4H). Coloration varies little within individual
feathers, but dorsal plumage is significantly darker than ventral
plumage. Preserved coloration suggests a chestnut brown
dorsal surface, contrasting against pale or almost white ventral
plumage (Figures 1A–1C and S4A–S4D); however, taphonomic
impacts on visible colors are unclear. A small section of the
pale ventral plumage was available for SEM observations. No
melanosomes were observed, suggesting that ventral plumage
was either unpigmented or pigmented through alternative
means, such as carotenoids [34]. Keratin sheets are visible within
the feather layer, displaying the distinctive, porous, laminar
structure also observed in modern avian barbules under SEM
(Figures S2A and S2B).
The theropod tail reported here is an astonishing fossil, high-
lighting the unique preservation potential of amber. Importantly,
in the context of bird origins, feathers and flight are key ele-
ments contributing to the success of the clade. Recent finds
from Asia [1–4, 6, 8–11] have revealed unexpected diversity in
feather morphologies and flight modes among the proliferation
of small Jurassic-Cretaceous theropods near the origin of birds
with powered flight. DIP-V-15103 adds another morphotype to
this diversity. The integration of developmental studies [5, 7, 33]
and paleontology yields enriched models of morphological
character evolution that help explain major evolutionary transi-
tions in key clades such as theropods, including birds. With
preservation in amber, the finest details of feathers are visible
in three dimensions, providing concrete evidence for feather
morphologies and arrangement upon the tail, as well as sup-
porting an important role for barbs and barbules in feather
evolution.
3358 Current Biology 26, 3352–3360, December 19, 2016
EXPERIMENTAL PROCEDURES
DIP-V-15103 was imaged and observed using propagation phase-contrast
Synchrotron Radiation X-ray microtomography (PPC-SR X-ray mCT); standard
microscopy, micro- and macrophotography (including transmitted, incident,
dark-field, and UV lighting); and scanning electron microscopy (SEM). Chem-
ical composition was analyzed using Synchrotron Radiation micro-X-ray
fluorescence imaging (m-XFI) and X-ray absorption spectroscopy (XAS). Full
details of experimental procedures for imaging and chemical analyses are pro-
vided in the Supplemental Experimental Procedures. Feather morphological
terms follow [5] and [35], while pigmentation terminology follows [36]. Institu-
tional abbreviations include DIP (Dexu Institute of Palaeontology, Chaozhou,
China) and RSM (Royal Saskatchewan Museum, Regina, Canada). Specimen
measurements are based on ocular micrometer readings or 3D reconstruc-
tions (with commentary).
SUPPLEMENTAL INFORMATION
Supplemental Information includes Supplemental Experimental Procedures,
five figures, and one table and can be found with this article online at http://
dx.doi.org/10.1016/j.cub.2016.10.008.
AUTHOR CONTRIBUTIONS
L.X. and R.C.M.: project design, leadership, funding, visualization, and writing;
X.X., W.S.P., T.M., and P.J.C.: morphological analysis and editing; G.L., M.B.,
and Q.Y.: SR phase-contrast CT, 3D modeling, elemental analysis, and edit-
ing; K.T.: taphonomic analysis; M.J.B. and H.R.: data and CT model analysis
and editing; J.Z.: geological background; A.P.W.: SEM analysis and editing.
ACKNOWLEDGMENTS
We thank the Chinese Academy of Science (YZ201211, YZ201509, BASIC
Y5Z003), National Science Fund of China (31672345), State’s Key Project of
Research and Development Plan (2016YFA0401302), National Geographic
Society, USA (EC0768-15), and National Sciences Engineering Research
Council, Canada (2015-00681) for support; Beijing Synchrotron Radiation
Facility (BSRF) and Shanghai Synchrotron Radiation Facility (SSRF) for beam-
time; staffs of 4W1A and 4W1B of BSRF, and 13W of SSRF, for analytical
assistance; Zhao Haifei, Zhang Jie, An Pengfei, and Wang Yanping of BSRF
for research assistance; Ray Poulin (RSM) for discussions; and Nathan Gerein
(University of Alberta) for SEM assistance.
Received: July 10, 2016
Revised: September 7, 2016
Accepted: October 5, 2016
Published: December 8, 2016
REFERENCES
1. Ji, Q., and Ji, S.-A. (1996). On the discovery of the earliest fossil bird in
China (Sinosauropteryx gen. nov.) and the origin of birds. Chin. Geol.
233, 30–33.
2. Qiang, J., Currie, P.J., Norell, M.A., and Ji, S. (1998). Two feathered dino-
saurs from northeastern China. Nature 393, 753–761.
3. Chen, P.J., Dong, Z.M., and Zhen, S.N. (1998). An exceptionally well-pre-
served theropod dinosaur from the Yixian Formation of China. Nature 391,
147–152.
4. O’Connor, J.K., Chiappe, L.M., Chuong, C.M., Bottjer, D.J., and You, H.
(2012). Homology and potential cellular and molecular mechanisms for
the development of unique feather morphologies in early birds.
Geosciences (Basel) 2, 157–177.
5. Prum, R.O. (1999). Development and evolutionary origin of feathers.
J. Exp. Zool. 285, 291–306.
6. Xu, X., Zhou, Z., and Prum, R.O. (2001). Branched integumental structures
in Sinornithosaurus and the origin of feathers. Nature 410, 200–204.
7. Prum, R.O., and Dyck, J. (2003). A hierarchical model of plumage:
morphology, development, and evolution. J. Exp. Zoolog. B Mol. Dev.
Evol. 298, 73–90.
8. Xu, X., Zheng, X., and You, H. (2010). Exceptional dinosaur fossils show
ontogenetic development of early feathers. Nature 464, 1338–1341.
9. Xu, X., Zhou, Z., Dudley, R., Mackem, S., Chuong, C.M., Erickson, G.M.,
and Varricchio, D.J. (2014). An integrative approach to understanding
bird origins. Science 346, 1253293.
10. Chen, C.-F., Foley, J., Tang, P.C., Li, A., Jiang, T.X., Wu, P., Widelitz, R.B.,
and Chuong, C.M. (2015). Development, regeneration, and evolution of
feathers. Annu. Rev. Anim. Biosci. 3, 169–195.
11. Norell, M.A., and Xu, X. (2005). Feathered dinosaurs. Annu. Rev. Earth
Planet. Sci. 33, 277–299.
12. McKellar, R.C., Chatterton, B.D.E., Wolfe, A.P., and Currie, P.J. (2011). A
diverse assemblage of Late Cretaceous dinosaur and bird feathers from
Canadian amber. Science 333, 1619–1622.
13. Nascimbene, P.C., Dove, C.J., Grimaldi, D.A., and Schmidt, A.R. (2014).
Exceptional preservation of feather microstructures in amber from diverse
faunas (Theropoda: Paraves) during the Lower and mid-Cretaceous.
9th European Palaeobotany-Palynology Conference, Pavoda, Italy Abstract
Book pp. 113–114.
14. Xing, L., McKellar, R.C., Wang, M., Bai, M., O’Connor, J.K., Benton, M.J.,
Zhang, J., Wang, Y., Tseng, K., Lockley, M.G., et al. (2016). Mummified
precocial bird wings in mid-Cretaceous Burmese amber. Nat. Commun.
7, 12089.
15. Schlee, D., and Glo
¨ckner, W. (1978). Bernstein: Bernsteine und Bernstein-
Fossilien. Stuttg. Beitr. Naturkd., C 8, 1–72.
16. Grimaldi, D.A., and Case, G.R. (1995). A feather in amber from the Upper
Cretaceous of New Jersey. Am. Mus. Novit. 3126, 1–6.
17. Grimaldi, D.A., Engel, M.S., and Nascimbene, P.C. (2002). Fossiliferous
Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diver-
sity, and paleontological significance. Am. Mus. Novit. 3361, 1–72.
18. Perrichot, V., Marion, L., N
eraudeau, D., Vullo, R., and Tafforeau, P. (2008).
The early evolution of feathers: fossil evidence from Cretaceous amber of
France. Proc. Biol. Sci. 275, 1197–1202.
19. Alibardi, L. (2006). Cells of embryonic and regenerating germinal layers
within barb ridges: implication for the development, evolution and diversi-
fication of feathers. J. Submicrosc. Cytol. Pathol. 38, 51–76.
20. De Queiroz, K., Chu, L.-R., and Losos, J.B. (1998). A second Anolis lizard in
Dominican amber and the systematics and ecological morphology of
Dominican amber anoles. Am. Mus. Novit. 3249, 1–23.
21. Schweitzer, M.H., Zheng, W., Cleland, T.P., Goodwin, M.B., Boatman, E.,
Theil, E., Marcus, M.A., and Fakra, S.C. (2013). A role for iron and oxygen
chemistry in preserving soft tissues, cells and molecules from deep time.
Proc. Biol. Sci. 281, 20132741.
22. Grimaldi, D.A., and Engel, M.S. (2005). Evolution of the Insects (Cambridge
University Press).
23. Colleary, C., Dolocan, A., Gardner, J., Singh, S., Wuttke, M., Rabenstein,
R., Habersetzer, J., Schaal, S., Feseha, M., Clemens, M., et al. (2015).
Chemical, experimental, and morphological evidence for diagenetically
altered melanin in exceptionally preserved fossils. Proc. Natl. Acad. Sci.
USA 112, 12592–12597.
24. O’Connor, J.K., Wang, X., Zheng, X., Hu, H., Zhang, X., and Zhou, Z.
(2016). An enantiornithine with a fan-shaped tail, and the evolution of the
rectricial complex in early birds. Curr. Biol. 26, 114–119.
25. Zhang, F., Zhou, Z., Xu, X., Wang, X., and Sullivan, C. (2008). A bizarre
Jurassic maniraptoran from China with elongate ribbon-like feathers.
Nature 455, 1105–1108.
26. O’Connor, J.K., and Zhou, Z. (2013). A redescription of Chaoyangia beish-
anensis (Aves) and a comprehensive phylogeny of Mesozoic birds. J. Syst.
Palaeontology 11, 889–906.
27. Persons, W.S., Currie, P.J., and Norell, M.A. (2014). Oviraptorosaur tail
forms and functions. Acta Palaeontol. Pol. 59, 553–567.
Current Biology 26, 3352–3360, December 19, 2016 3359
28. Currie, P.J., and Chen, P.J. (2001). Anatomy of Sinosauropteryx prima
from Liaoning, northeastern China. Can. J. Earth Sci. 38, 1705–1727.
29. O’Connor, J.K., Sun, C., Xu, X., Wang, X., and Zhou, Z. (2012). A new spe-
cies of Jeholornis with complete caudal integument. Hist. Biol. 24, 29–41.
30. Alibardi, L., and Sawyer, R.H. (2006). Cell structure of developing down-
feathers in the zebrafinch with emphasis on barb ridge morphogenesis.
J. Anat. 208, 621–642.
31. Xu, X., Tang, Z.L., and Wang, X.L. (1999). A therizinosauroid dinosaur with
integumentary structures from China. Nature 399, 350.
32. Alibardi, L. (2005). Cell structure of developing barbs and barbules in
downfeathers of the chick: Central role of barb ridge morphogenesis for
the evolution of feathers. J. Submicrosc. Cytol. Pathol. 37, 19–41.
33. Alibardi, L. (2007). Cell interactions in barb ridges of developing chick
downfeather and the origin of feather branching. Ital. J. Zool. (Modena)
74, 143–155.
34. Thomas, D.B., Nascimbene, P.C., Dove, C.J., Grimaldi, D.A., and James,
H.F. (2014). Seeking carotenoid pigments in amber-preserved fossil
feathers. Sci. Rep. 4, 5226.
35. Lucas, A.M., and Stettenheim, P.R. (1979). Avian Anatomy: Integument
(Washington, DC: US Government Printing Office).
36. Dove, C.J. (2000). A descriptive and phylogenetic analysis of plumula-
ceous feather characters in Charadriiformes. Ornithol. Monogr. 51, 1–163.
3360 Current Biology 26, 3352–3360, December 19, 2016
... Fossil discoveries of potential neonatal feathering are rare but have been reported in at least three instances (Xing et al., 2017(Xing et al., , 2020Xing, McKellar, Xu, et al., 2016). Most of these feathers were described as an unusual neoptile type with both a rachis and reduced pennaceous barbules organized into a simple vanule instead of the disorganized plumulaceous barbules common to adult down. ...
... We could not determine whether these organized barbules in C. coturnix were pennaceous or plumulaceous; a more detailed analysis utilizing SEM may be needed. All but one of the fossil feathers to possibly comprise neonatal down (Xing et al., 2017(Xing et al., , 2020Xing, McKellar, Xu, et al., 2016) show barbules F I G U R E 1 0 Implications of neoptile development based on feather morphology. Lines intersecting the feathers (a, Struthio camelus; b, Coturnix coturnix) represent isoclines that occur early (red) and late (blue) in the feathers' development. ...
... Our results are consistent with these previous studies. If these fossil feathers do exemplify natal down, that would imply that natal down in some or all extinct stem taxa lacks semi-naked barbs and is instead closer in morphology to the adult feathers of modern birds, as hypothesized in previous studies (O'Connor et al., 2020;Xing et al., 2017;Xing, McKellar, Wang, et al., 2016;Xing, McKellar, Xu, et al., 2016). Previous studies have also shown that some fossilized feathers lack barbules partially or entirely, though they never show the naked tips seen in extant bird natal down (Kundrát et al., 2020;Lefèvre et al., 2017;Perrichot et al., 2008;Sayão et al., 2011;Xing et al., 2017;Xing, Cockx, et al., 2018;Xing et al., 2020). ...
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... possess bulbous and protruding postclypeus (character 10:1) and support its inclusion in Psocodea. They have shorter antenna than head (character 25:0), which differentiates it from Liposcelididae and places it in Phthiraptera. Following characters further support its relationship within Amblycera: club-shaped antenna (character 26:0), compared with the filiform antenna of Liposcelididae 15 ; pedunculated first flagellar segment (character 27:1) but compressed terminal several ones (character 28:1), and antennae are never pedunculated in any of the other phthirapteran groups 16 ; two euplantula (character 49:0), in other families of the Amblycera, only the euplantula of the first tarsal segment is normally present. ...
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