2.
Norberg, U. Vertebrate Flight: Mechanics, Physiology, Morphology, Ecology and Evolution (Springer, Berlin, 1990).
3.
Xu, X. et al. An integrative approach to understanding bird origins. Science 346, 1253293 (2014).
4.
Gatesy, S. M. & Middleton, K. M. Bipedalism, flight, and the evolution of theropod locomotor diversity. J. Vertebr. Paleontol. 17, 308–329 (1997).
5.
Chatterjee, S. & Templin, R. J. Biplane wing planform and flight performance of the feathered dinosaur Microraptor gui. Proc. Natl Acad. Sci. USA 104, 1576–1580 (2007).
6.
Xu, X. et al. A bizarre Jurassic maniraptoran theropod with preserved evidence of membranous wings. Nature 521, 70–73 (2015).
7.
Padian, K. Dinosaur up in the air. Nature 521, 40–41 (2015).
8.
Liu,
Y., Liu, Y., Ji, S. A. & Yang, Z. U–Pb zircon age for the Daohugou
Biota at Ningcheng of Inner Mongolia and comments on related issues. Chin. Sci. Bull. 51, 2634–2644 (2006).
9.
Huang, D. Yanliao biota and Yanshan movement (in Chinese). Acta Palaeontologica Sin. 54, 501–546 (2015).
10.
Campione,
N. E., Evans, D. C., Brown, C. M. & Carrano, M. T. Body mass
estimation in non-avian bipeds using a theoretical conversion to
quadruped stylopodial proportions. Methods Ecol. Evol. 5, 913–923 (2014).
11.
Persons, W. S., Currie, P. J. & Norell, M. A. Oviraptorosaur tail forms and functions. Acta Palaeontol. Pol. 59, 553–567 (2013).
12.
O’Connor, J. K. & Sullivan, C. Reinterpretation of the Early Cretaceous maniraptoran (Dinosauria: Theropoda) Zhongornis haoae as a scansoriopterygid-like non-avian, and morphological resemblances between scansoriopterygids and basal oviraptorosaurs. Vertebr. Palasiat. 52, 3–30 (2014).
13.
Gatesy, S. M. & Thomason, J. in Functional Morphology in Vertebrate Paleontology (ed. Thomason, J. J.) 219–234 (Cambridge Univ. Press, Cambridge, 1995).
14.
Zhang,
F., Zhou, Z., Xu, X., Wang, X. & Sullivan, C. A bizarre Jurassic
maniraptoran from China with elongate ribbon-like feathers. Nature 455, 1105–1108 (2008).
15.
Zhang, F., Zhou, Z., Xu, X. & Wang, X. A juvenile coelurosaurian theropod from China indicates arboreal habits. Naturwissenschaften 89, 394–398 (2002).
16.
Turner, A. H., Makovicky, P. J. & Norell, M. A. A review of dromaeosaurid systematics and paravian phylogeny. Bull. Am. Mus. Nat. Hist. 371, 1–206 (2012).
17.
Xu, X. et al. A new feathered maniraptoran dinosaur fossil that fills a morphological gap in avian origin. Chin. Sci. Bull. 54, 430–435 (2009).
18.
Balanoff, A. M. & Norell, M. A. Osteology of Khaan mckennai (Oviraptorosauria: Theropoda). Bull. Am. Mus. Nat. Hist. 372, 1–77 (2012).
19.
Hutchinson, J. R. The evolution of pelvic osteology and soft tissues on the line to extant birds (Neornithes). Zool. J. Linn. Soc. 131, 123–168 (2001).
20.
Zhang, F. et al. Fossilized melanosomes and the colour of Cretaceous dinosaurs and birds. Nature 463, 1075–1078 (2010).
21.
Thorington, J. R. W., Darrow, K. & Anderson, C. G. Wing tip anatomy and aerodynamics in flying squirrels. J. Mamm. 79, 245–250 (1998).
22.
Oshida,
T., Hiraga, H., Nojima, T. & Yoshida, M. C. Anatomical and
histological notes on the origin of the long accessory styliform
cartilage of the Russian flying squirrel, Pteromys volans orii. Mammal Study 25, 41–48 (2000).
23.
Dial, K. P. Wing-assisted incline running and the evolution of flight. Science 299, 402–404 (2003).
24.
Lovette, I. J. & Fitzpatrick, J. W. Handbook of Bird Biology 3rd edn (John Wiley & Sons, Hoboken, 2016).
25.
Sullivan, C. et al. The vertebrates of the Jurassic Daohugou biota of northeastern China. J. Vertebr. Paleontol. 34, 243–280 (2014).
26.
Liu,
Y., Liu, Y. & Zhang, H. LA-ICPMS zircon U-Pb dating in the Jurassic
Daohugou beds and correlative strata in Ningcheng of Inner Mongolia. Acta Geol. Sin. 80, 733–742 (2006).
27.
Liu, Y.-Q. et al. Timing of the earliest known feathered dinosaurs and transitional pterosaurs older than the Jehol biota. Palaeogeogr. Palaeoclimatol. Palaeoecol. 323–325, 1–12 (2012).
28.
Chu,
Z. et al. High-precision U-Pb geochronology of the Jurassic Yanliao
biota from Jianchang (western Liaoning Province, China): age constraints
on the rise of feathered dinosaurs and eutherian mammals. Geochem. Geophys. Geosyst. 17, 3983–3992 (2016).
29.
Xu,
X., Zhou, Z., Sullivan, C., Wang, Y. & Ren, D. An updated review of
the Middle–Late Jurassic Yanliao Biota: chronology, taphonomy,
paleontology and paleoecology. Acta Geol. Sin. 90, 2229–2243 (2016).
30.
Benson,
R. B. J. et al. Rates of dinosaur body mass evolution indicate 170
million years of sustained ecological innovation on the avian stem
lineage. PLoS Biol. 12, e1001853 (2014).
31.
Christiansen, P. & Fariña, R. A. Mass prediction in theropod dinosaurs. Hist. Biol. 16, 85–92 (2004).
32.
Serrano,
F. J., Palmqvist, P. & Sanz, J. L. Multivariate analysis of
neognath skeletal measurements: implications for body mass estimation in
Mesozoic birds. Zool. J. Linn. Soc. 173, 929–955 (2015).
33.
Campione,
N. E. & Evans, D. C. A universal scaling relationship between body
mass and proximal limb bone dimensions in quadrupedal terrestrial
tetrapods. BMC Biol. 10, 60 (2012).
34.
Goloboff, P. A. & Catalano, S. A. TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics 32, 221–238 (2016).
35.
Brusatte, S. L. in Computational Paleontology (ed. Elewa, A. M. T.) 53–74 (Springer, Heidelberg, 2011).
36.
Laurin, M. The evolution of body size, Cope’s rule and the origin of amniotes. Syst. Biol. 53, 594–622 (2004).
37.
Wang, M. & Lloyd, G. T. Rates of morphological evolution are heterogeneous in Early Cretaceous birds. Proc. R. Soc. Lond. B 283, 20160214 (2016).
38.
Bapst, D. W. paleotree: an R package for paleontological and phylogenetic analyses of evolution. Methods Ecol. Evol. 3, 803–807 (2012).
39.
Revell, L. J. Size-correction and principal components for interspecific comparative studies. Evolution 63, 3258–3268 (2009).
40.
Benson,
R. B. J. & Choiniere, J. N. Rates of dinosaur limb evolution
provide evidence for exceptional radiation in Mesozoic birds. Proc. R. Soc. Lond. B 280, 20131780 (2013).
41.
Hu,
D. et al. A bony-crested Jurassic dinosaur with evidence of iridescent
plumage highlights complexity in early paravian evolution. Nat. Commun. 9, 217 (2018).
42.
Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics. 20, 289–290 (2004).
43.
Felsenstein, J. Phylogenies and the comparative method. Am. Nat. 125, 1–15 (1985).
44.
Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
Acknowledgements
We
thank S.-X. Jiang, D.-Y. Huang, Y.-H. Pan and Z.-Q. Yu for discussion,
Q.-R. Meng for help in the field, T. Zhao for taking scanning electron
microscopy photographs, D.-H. Li for specimen preparation and W. Gao for
photographing. This research was supported by the National Natural
Science Foundation of China (41688103; 41722202), Youth Innovation
Promotion Association CAS (2016073) and the State Key Laboratory of
Lithospheric Evolution (Z201604).
Reviewer information
Nature thanks Thomas Richard Holtz, Peter Makovicky and Kevin Padian for their contribution to the peer review of this work.
Affiliations
Key
Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy
of Sciences, Institute of Vertebrate Paleontology and
Paleoanthropology, Chinese Academy of Sciences, Beijing, China
- Min Wang
- , Jingmai K. O’Connor
- , Xing Xu
- & Zhonghe Zhou
Center for Excellence in Life and Paleoenvironment, Chinese Academy of Science, Beijing, China
- Min Wang
- , Jingmai K. O’Connor
- , Xing Xu
- & Zhonghe Zhou
Contributions
Z.Z.
and M.W. designed the research project; Z.Z. and M.W. conducted the
fieldwork; M.W. performed the phylogenetic, histological and
phylogenetic principal component analyses; and M.W., J.K.O., X.X. and
Z.Z. wrote the manuscript.
Competing interests
The authors declare no competing interests.
Corresponding author
Correspondence to
Min Wang.
Extended data figures and tables
-
a, Counter slab.
b, Skeletal reconstruction based on preserved bones.
c, Skull.
d, Gastroliths and the unidentified bony stomach content. Abbreviations as in Fig.
1,
except for: fe, feather associated with the neck; lil, left ilium;;
lti, left tibia; pd, pedal digits; and ub, unidentified bony element.
The white box indicates the position from which the sample was taken for
histological analysis. Scale bars, 10 mm (
a,
c,
d), 20 mm (
b).
-
a–d, Thin cross-section of the left humerus (a, b) and the unidentified bony stomach content (c, d). The arrowheads indicate the osteocyte lacunae. Scale bars, 100 μm (a–c), 200 μm (d).
-
a–
d, Interpretative drawings of the neck and pectoral girdle (
a), caudal vertebrae and pygostyle (
b), left forelimb (
c) and pelvis and left hindlimb (
d). Abbreviations as in Figs.
1,
2,
except for: ca, caudal vertebrae; cm, calcaneum; de, deltopectoral
crest of humerus; do, dorsal vertebrae; I–III, metacarpals I–III; ip,
iliac peduncle of ilium; mtII–IV, metatarsals II–IV; p1–4, pedal digits I
to IV; and st, styliform element. Scale bars, 10 mm (
a–
d).
-
a, Left forelimb of
Ambopteryx (IVPP V24192).
b–
d, Left forelimb (
b), right humerus (
c) and the right styliform element (
d) of
Yi
(STM 31-2). The proximal margins of the humeri are marked in white
dashed lines to show the differences between these two taxa.
Abbreviations as in Figs.
1,
2, except for: st, styliform element. Scale bars, 10 mm (
a), 20 mm (
b–
d).
-
a–c, Line drawings of the hands of Ambopteryx (a), Epidendrosaurus (b) and Yi (c). Scale bars, 10 mm (a, b), 20 mm (c).
-
a–d, Feather samples associated with the neck. e–f,
Samples of membranous tissues taken from the area between the left
femur and left manual digits. Arrows denote the positions of the
samples. Scale bars, 2 μm.
-
Bremer and bootstrap values are labelled near the corresponding node in bold italic and upright non-bold font, respectively.
-
Complete tree for the coelurosaurians used in generating the PPCA morphospaces shown in Fig.
3b, c.
Supplementary information
-
This
file contains Supplementary Text Sections 1–5; which include additional
anatomical description, stomach contents and diet of Ambopteryx longibrachium, Supplementary Tables 1, 2, 4 and 5, and the data used in the phylogenetic analysis.
-
-
This
file contains appendicular limb bone measurements of Mesozoic
coelurosaurians used in the phylogenetic principal components analysis.
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