Current Biology 24, 2386–2392, October 20, 2014 ª2014 Elsevier Ltd All rights reserved

http://dx.doi.org/10.1016/j.cub.2014.08.034

ReportGradual Assembly of Avian Body Plan
Culminated in Rapid Rates of Evolution
across the Dinosaur-Bird Transition
Stephen L. Brusatte,1,* Graeme T. Lloyd,2 Steve C. Wang,3and Mark A. Norell4
1School of GeoSciences, University of Edinburgh, Edinburgh
EH9 3JW, UK
2Department of Earth Sciences, University of Oxford, Oxford
OX1 3AN, UK
3Department of Mathematics and Statistics, Swarthmore
College, Swarthmore, PA 19081, USA
4Division of Paleontology, American Museum of Natural
History, New York, NY 10024, USA

Summary
The evolution of birds from theropod dinosaurs was one of
the great evolutionary transitions in the history of life [1–22]. The macroevolutionary tempo and mode of this transition is poorly studied, which is surprising because it may
offer key insight into major questions in evolutionary biology,
particularly whether the origins of evolutionary novelties or
new ecological opportunities are associated with unusually
elevated ‘‘bursts’’ of evolution [23, 24]. We present a comprehensive phylogeny placing birds within the context oftheropod evolution and quantify rates of morphologicalevolution and changes in overall morphological disparity
across the dinosaur-bird transition. Birds evolved significantly faster than other theropods, but they are indistinguishable from their closest relatives in morphospace. Our results
demonstrate that the rise of birds was a complex process:birds are a continuum of millions of years of theropod evolution, and there was no great jump between nonbirds and birds
in morphospace, but once the avian body plan was graduallyassembled, birds experienced an early burst of rapid anatomical evolution. This suggests that high rates of morphologicalevolution after the development of a novel body plan may be acommon feature of macroevolution, as first hypothesized by
G.G. Simpson more than 60 years ago [25].
Results
The fossil record provides unique insight into major evolutionary transitions: the origins of entirely new body plans andbehaviors. In one of the great transitions in the history of life,
bipedal carnivorous theropod dinosaurs evolved feathers
and wings [1, 2], dramatically reduced their body size [3–6],
and gave rise to birds. The dinosaur-bird transition is captured
by a rich fossil record that has expanded tremendously inrecent years—including thousands of feathered dinosaur
specimens from northeastern China found over the past two
decades [2]—providing an unparalleled opportunity to dissecta major morphological, behavioral, and paleobiological transformation in deep time. In particular, the dinosaur-bird transition can provide key insight into major questions in contemporary evolutionary biology, particularly whether the origins ofevolutionary novelties or new ecological opportunities are*Correspondence: stephen.brusatte@ed.ac.uk

associated with unusually elevated ‘‘bursts’’ of evolution [23,24]. This hypothesis was first articulated by George Gaylord
Simpson in the 1940s [25] and has been the subject of intense
debate ever since.
Phylogenetic Analysis
Birds are members of the theropod dinosaur subgroup Coelurosauria, a diverse clade that includes tyrannosauroids and dromaeosaurids, among others [7–14]. Our comprehensive, newphylogenetic analysis is a species-level analysis that includes
nearly all Mesozoic coelurosaurs that are known from well-preserved and diagnostic fossils available for study. It is the latest
iteration of the Theropod Working Group (TWiG) project, a20-year program centered at the American Museum of Natural
History that has been building progressively larger and more
inclusive data sets of coelurosaurian phylogeny based on
personal study of specimens. Previous TWiG analyses havefocused extensively on the most derived paravian coelurosaurs: birds (technically known as avialans) and their very
closest relatives, such as dromaeosaurids and troodontids[8, 9]. Here, for the first time, we incorporate a broad range ofmore basal (nonparavian) coelurosaurs into a TWiG analysis.
Our data set includes 150 coelurosaurs scored for 853 characters, approximately twice the size of previous TWiG data sets
(Supplemental Experimental Procedures available online).
Our phylogenetic analysis places birds within the broader
framework of theropod evolution (Figure 1; see also Figures
S1 and S2). Tyrannosauroids are the most basal major coelurosaurian subgroup; therizinosauroids and alvarezsauroids forma clade with oviraptorosaurs and paravians exclusive of morebasal coelurosaurs; therizinosauroids and oviraptorosaurs are
not sister taxa; and, for the first time, a TWiG analysis recovers
a polytomy between avialans, dromaeosaurids, and troodontids, meaning that the immediate relative of birds cannot beclearly identified. The recently described Aurornis, Xiaotingia,
and Anchiornis comprise a clade of basal troodontids, not avialans, as recently proposed [14]. The iconic Archaeopteryx is
positioned as the basal-most avialan taxon, a ‘‘traditional’’
placement that is in agreement with most previous studies[8–10], not as a closer relative of dromaeosaurids, as wasfound in a recent series of analyses [11, 12].
Morphological Rates
The anatomical characters compiled for the phylogenetic
analysis provide a ready source of data for examining trends
in anatomical evolution across the dinosaur-bird transition.
Because our data set includes features from throughout theskeleton, it can encapsulate changes in overall anatomy anddocument the evolution of the entire avian body plan. It complements recent analyses focused on more specific features,such as body size [3–6, 22] and limb measurements [19–21].
Maximum-likelihood analyses of rates of character evolution
on the phylogeny, which test whether individual branches orentire clades have significantly different rates than theremainder of the tree [26, 27], identify high rates in birds (avialans) and the internal branches leading toward birds (Figure 2;
see also Figure S3). High rates in birds are consistently foundunder a variety of conditions: in different most-parsimonious

Rapid Evolution across Dinosaur-Bird Transition
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Figure 1. Phylogenetic Relationships of Coelurosaurian Theropods Based on a Data Set of 152
Taxa Scored for 853 Characters
Strict consensus tree of 99,999 most-parsimonious trees (3,360 steps, consistency index =0.322, retention index = 0.777). Silhouettes arefrom http://phylopic.org/. See also Figures S1and S2 for the full strict reduced consensus tree.

Experimental Procedures and http://dx.doi.org/10.5061/dryad.84t75). This
provides robust evidence that birds(and their stem lineage) evolved fasterthan other theropods and that their
origin was associated with an ‘‘earlyburst’’ of rapid morphological evolution.
Previous studies have found significant
changes in body size and limb morphology either progressively prior tothe origin of birds or within morederived birds [3, 5, 6, 19, 20, 22], but
our analysis of the overall phenotype
puts the major rate shift at the origin of
Avialae itself.
High rates are also common amongtyrannosauroids, the only major coelurosaurian subgroup to evolve colossal
size (5 tons or more in mass). If genuine,
this may suggest that dinosaurs developed gigantism by accelerating rates
of morphological evolution, perhaps
incongruous with a recent finding thatlarge theropods had slower rates of
proportional body size evolution thansmaller lineages [6]. However, the hightyrannosauroid rates appear to be artifactual, probably caused by an overinflation of taxa and characters in thedata set relevant to these iconic andwell-studied theropods. First, high tyrannosauroid rates are not seen in all
iterations (based on different branch
durations) of the primary analysis, andin some iterations, significantly low
rates are recovered. Second, the hightyrannosauroid rates disappear inmany of our sensitivity analyses (Supplemental Experimental Proceduresandhttp://dx.doi.org/10.5061/dryad.
84t75). This is not the case with thehigh rates in birds, as these are seen in
all branch dating iterations and persist
in all sensitivity analyses.

trees (MPTs), using different branch dating techniques,
when terminal and internal branches are tested separately,
and when the phylogeny is subsampled down to a common
number of species in each major subgroup (Supplemental

Disparity and Morphospace
Occupation
When the character data set is used to
calculate disparity, by ordinating all
taxa in a morphospace depicting the
spread of morphological variability among coelurosaurs [28],there is no firm evidence that birds group separately from otherspecies or have greater disparity than other coelurosaurgroups (Figure 3; Tables S1–S3). Although there is separation

Current Biology Vol 24 No 20
2388

Allosaurus
Bicentenaria
Zuolong
Tanycolagreus
Coelurus
Kileskus
Guanlong
Proceratosaurus
Sinotyrannus
DilongJuratyrant

Tyrannosauroidea

Eotyrannus
Xiongguanlong
Dryptosaurus
Appalachiosaurus
Bistahieversor

Tyrannosauridae

Tugulusaurus
Ornitholestes
Juravenator
Sinocalliopteryx
Huaxiagnathus

Compsognathidae

Mirischia
Compsognathus
Sinosauropteryx
Nqwebasaurus
Pelecanimimus
Shenzhousaurus
Beishanlong
Harpymimus

Garudimimus

Ornithomimosauria

Sinornithomimus
Archaeornithomimus
Gallimimus
Anserimimus
Struthiomimus
Qiupalong
Ornithomimus

Alvarezsauroidea

Therizinosauroidea
Epidexipteryx
Pedopenna

Oviraptorosauria(inc. Epidexipteryx + Pedopenna)

Oviraptorosauria

Archaeopteryx
Sapeornis
Jeholornis
Jixiangornis

Avialae

Confuciusornis
Other avialans

Anchiornis clade

Troodontidae
Other Troodontidae

Dromaeosauridae

Figure 2. Summary of Results of Two Rate Tests on the First of Ten Randomly Sampled Most-Parsimonious Trees
Clades are collapsed as in Figure 1, with the full tree and all per-branch and clade rate results shown at http://dx.doi.org/10.5061/dryad.84t75. Pie charts
along individual branches indicate the proportion of significantly high (red), significantly low (blue), and nonsignificant (white) per-branch rates based on 100
replicates to take into account dating uncertainty. Results for the clade test are shown for the nine major subclades, with the larger pie charts indicating the
proportion of high, low, and nonsignificant rates across 100 replicates of dating uncertainty, using the same color scheme. Silhouettes are from http://phylopic.org/. See also Figure S3 for the full clade rate results on our primary tree.

Rapid Evolution across Dinosaur-Bird Transition
2389

PC axis 2
0
50 100 150

Figure 3. Discrete Character Morphospace of
Coelurosaurian Theropods, Depicting the Overall
Anatomical Variability of Species-100 -50

Bivariate plots of principal coordinate axes 2
versus 1 and 3 versus 2 are shown (axes 1–3 account for 4.25% of total variance). Birds arelargely distinct from other coelurosaurs on principal coordinate axis 1, but not on axis 2 or 3 (orall subsequent axes). Permutation tests indicatethat there is no clear, significant separation between birds and their closest relatives among
theropods (Tables S1–S3; Supplemental Experimental Procedures).

-500
PC axis 1

50

-100

-50

PC axis 3
0
50

100

-100

demonstrates, for example, that birds
and dromaeosaurids are less distinct
from each other than are therizinosauroids and oviraptorosaurs, one of thesignificant comparisons. In other words,
birds are not a notable outlier whenplaced in the context of the entire coelurosaur morphospace. Although birds
are clearly distinct compared to all otherliving vertebrates, the avian bauplan
isn’t especially distinct relative to othercoelurosaurs, particularly their closest
relatives.
These results are consistent withmany recent phylogenetic studies,
ours included (see ‘‘Phylogenetic Analysis’’ in the Results), which find few
characters separating Avialae fromnonavialan theropods. These results
may also help explain why so many alternative phylogenetic analyses havedifficulty in placing certain taxa (suchas Anchiornis and Archaeopteryx)
consistently in either Avialae or among
the clades of nonavialan theropods
most closely related to birds [7–14].

-100

-50

0
50
PC axis 2

100

150

Discussion

The rate and disparity results presented
here paint a complex picture of thedinosaur-bird transition and the early
evolution of birds. In general anatomical
Ornithomimosauria
Compsognathidae
Tyrannosauroidea
Therizinosauroidea
terms, birds are a continuum of millionsof years of theropod evolution. There isno great jump between nonbirds andbirds in morphospace. Instead, those
Dromaeosauridae
features that today combine to set birds
Oviraptorosauria
Troodontidae
Avialae
Alvarezsauroidea
apart from other vertebrates—feathers,
wishbones, air sacs, and hundredsof birds and other coelurosaurs on the first principal coordi- more—evolved piecemeal in Mesozoic theropods [18]. Therenate axis (which explains only a small portion of overall vari- fore, we surmise that a Mesozoic naturalist would make no imance), there is wide overlap on all other axes. Permutation mediate distinction between a Velociraptor-type animal andtests, which assess whether the morphospace means of two an Archaeopteryx-type animal. That said, there is an increased
groups significantly differ from each other over all axes, find rate of morphological evolution associated with the origin ofbirds to be indistinct from their closest paravian relatives birds, beginning in the stem lineage leading toward birds and(Tables S1 and S2; Supplemental Experimental Procedures). continuing throughout most of the avialan portion of Mesozoic
Pairwise comparisons between other coelurosaur subgroups coelurosaur phylogeny. This rate does not correspond to a
are also generally insignificant, but a few are significant. This major shift in morphospace occupation, so it does not reflectCurrent Biology Vol 24 No 20
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the sudden and simultaneous acquisition of a distinct avian
body plan. Instead, it suggests that birds evolved their distinctive features gradually and that once the classic bird-like skeleton was assembled, something was unlocked that allowed
birds to evolve rapidly within their fairly indistinct area ofmorphospace.
There is growing evidence that changes in discrete character evolution, body size, and limb anatomy occurred quickly
in the vicinity of the origin of birds, either at the node Avialae, inclose avialan outgroups, or beginning with slightly morederived birds [3–6, 19–22]. It is likely that different types ofdata will pinpoint changes at slightly different positions on
phylogeny, but in general, recent studies converge in identifying the dinosaur-bird transition as an abnormally rapid
period of morphological evolution. We hypothesize that highrates of morphological change after the development of anovel body plan, whether that development is sudden or
gradual, may be a common feature of macroevolution. Thisis generally consistent with Simpson’s theory of adaptive radiations and quantum evolution [25] and a recent study that
identified high morphological rates in Cambrian arthropods,
after their characteristic bauplans were assembled [29]. It isalso consistent with recent studies that found high rates ofmorphological evolution during the early history of lungfish[27], tetrapods [30], and archosaurs (the larger group containing dinosaurs and crocodiles) [31]. Although such ‘‘earlybursts’’ are rarely found in analysis of neontological data[23], improved methods [6, 24, 27] and the deep-time perspective of a good fossil record may show that they are a major
driver of evolution and biodiversity.

of these asks whether an individual branch has a significantly higher orlower rate of evolution than the rest of the tree, and the second asks whether
a particular clade has a significantly higher or lower rate than the remainderof the tree. Only Mesozoic coelurosaurs were included in these analyses,
which utilized the 853-character discrete data set from the phylogenetic
analysis. For each analysis, the tree was time scaled before characters
were optimized, using the ‘‘equal’’ branch scaling measure based on theabsolute ages of the terminal taxa [31, 39]. After time scaling, ancestral character states were estimated using the likelihood-based rerooting functionin the R package phytools [40], which in turn allows the total number ofchanges along each branch to be recorded. Per-branch rates were calculated based on the total number of changes along the branch, with a correction for missing data, divided by the time duration of the branch [27]. Multiple replicates were used to take into account uncertainty in branch
durations, based on uncertainty in the ages of the terminal taxa. Likelihood
was then used to assess which branches and clades had higher or lower
rates than the rest of the tree, following the protocols of [27].
For our primary analysis, we randomly selected a single MPT and applied
the per-branch and per-clade tests using 100 replicates. We followed thiswith a number of sensitivity tests to gauge how robust the recovered patterns were. The first of these involved randomly selecting nine other MPTs
to assess how differences in tree topology affect the rate results. The
second examined the effects of different time-scaling algorithms by using
a different option, the minimum-branch-length method [39]. The third tested
for rate heterogeneity on a tree where branches were scaled to a unit length,
to gauge how much of the rate results could be explained solely by
the amount of character change (not branch duration). The fourth
examined the effect of the number of sampled taxa in each major clade
by randomly removing taxa from Alvarezsauroidea, Avialae, Compsognathidae, Dromaeosauridae, Ornithomimosauria, Oviraptorosauria, Therizinosauria, Troodontidae, and Tyrannosauroidea until each one was the same
sample size (set at six species, based on the smallest clade, the compsognathids). Finally, the fifth tested for potential bias in rate between terminal
and internal branches (such as that due to the lack of sampled autapomoprhies) by separating the two branch types and repeating the per-branch
and per-clade tests.

Experimental Procedures
Phylogenetic Analysis
The phylogenetic analysis includes 152 taxa scored for 853 discrete characters. The analysis is the latest and most inclusive version of the American
Museum of Natural History’s TWiG data set. This data set has grown iteratively over the past 15 years with the addition of new taxa and characters [8,9]. The focus of previous TWiG analyses has been paravian theropods (avialans, dromaeosaurids, and troodontids), reflecting long-standing interestin the origin of birds and the relationships of birds and their closest dinosaurian relatives. We added a wealth of new data relevant to nonparavian coelurosaurs, particularly nonmaniraptoran ‘‘basal’’ coelurosaurs (tyrannosauroids, ornithomimosaurs, compsognathids, and singleton taxa). Comparedto the most recent TWiG data set [9], this analysis includes 41 new taxa and379 new characters. As a result, the analysis presented here includes anearly complete sample of Mesozoic coelurosaurs that have been available
to us for personal study. The new taxa include a nearly complete sample of‘‘basal’’ coelurosaurs and the recently described paravians Eosinopteryx[32] and Aurornis [14], which are particularly close relatives of birds. The
new characters include a number of novel characters pertinent to ‘‘basal’’coelurosaurs, characters relevant to the ingroup relationships of tyrannosauroids that were previously published by our research group [33], andcharacters from recent phylogenetic analyses of nonparavian coelurosaur
subgroups [34–37]. The character list and data set are provided at http://dx.doi.org/10.5061/dryad.84t75.
The phylogenetic data set was analyzed with equally weighted parsimony in
TNT v 1.1 [38]. Allosaurus was used as the outgroup to root the tree. The data
set was first analyzed under the ‘‘New Technology’’ search options, using
sectorial search, ratchet, tree drift, and tree fuse options with default parameters. The minimum length tree was found in ten replicates, a procedure thataims to initially sample as many tree islands as possible. The generated MPTs
were then analyzed under traditional tree bisection and reconnection branchswapping, a procedure that aims to more fully explore each tree island. Cladesupport was assessed via decay indices and jackknife resampling analysis.
Morphological Rates
Rates of discrete character morphological evolution in a phylogenetic
context were assessed using likelihood tests conducted in R [27]. The first

Disparity and Morphospace Occupation
In order the test the morphological ‘‘distinctiveness’’ of birds relative toother theropods, we plotted all coelurosaurs in our data set into a multivariate morphospace, which represents the spread of anatomical form in agroup [28]. This morphospace is nonphylogenetic (phenetic) in nature andonly denotes the total spread of morphological variation in coelurosaurs
without any indication of the speed at which this variation accumulates,making our morphospace-based tests distinct from our rate-based tests
above. The morphospace was constructed by deriving a Euclidean distancematrix from our 853-character discrete data set, which was then subjected
to principal coordinates analysis (PCO; equivalent to multidimensional
scaling), a multivariate ordination technique that summarizes informationfrom the distance matrix into a smaller and more manageable set of coordinate axes. The first axis represents those character distances contributing
most to the overall variability among coelurosaurs, and each additional
axis represents distances of progressively less significance. Each coelurosaur has a score on each axis, which together represent aspects of the overall anatomical form for each taxon.
The ‘‘distinctiveness’’ of avialans relative to other coelurosaurs wastested in three ways. First, we used permutation tests to perform pairwise
comparisons of group means in R and PAST [41]. These comparisons tested
the equality of multivariate means (based on the 125 recovered PCO axes,
which comprise 90% of total variance) of two designated groups (forexample, avialans versus deinonychosaurs). The Mahalanobis distance between the two group means was calculated and compared with a null distribution of between-group distances obtained by random permutation of thegroup labels. Second, we compared Euclidean distances between avialans
and their closest relatives (dromaeosaurids and troodontids) with Euclidean
distances between several control pairs of coelurosaurian groups that aresister taxa or particularly close relatives. This served to assess whether
birds are more distant from their closest relatives in morphospace thanare various other pairwise groups of close relatives. The means and distributions of distances for the avialans versus close relative comparisonsand the various other coelurosaur close relative comparisons were assessed for statistical significance with t tests and Mann-Whitney-Wilcoxon
tests. Third, we tested whether avialans occupied a larger volume of morphospace than other coelurosaurs by calculating four disparity metrics forRapid Evolution across Dinosaur-Bird Transition
2391

the various coelurosaur subgroups (sum and product of the ranges and variances on the PCO axes). These disparity metrics quantify how much morphospace avialans and the other groups occupy. Differences in the disparity
metrics between avialans and other coelurosaur groups were tested for significance with a permutation test.
Accession Numbers
Data for this paper are available on Dryad at http://dx.doi.org/10.5061/
dryad.84t75.
Supplemental Information
Supplemental Information includes Supplemental Experimental Procedures, three figures, and three tables and can be found with this article online at http://dx.doi.org/10.1016/j.cub.2014.08.034.
Author Contributions
S.L.B. led the project, compiled the anatomical data set, ran the phylogenetic analyses, ran some of the disparity analyses, and wrote the manuscript. G.T.L. led the morphological rates component of the project, wrote
code in R, ran all rates analyses in R, and contributed to the manuscript.
S.C.W. wrote code in R, ran disparity analyses in R, and contributed tothe manuscript. M.A.N. is the leader of the TWiG project, collected anatomical data for the TWiG project, oversaw S.L.B.’s PhD thesis (on which thismanuscript is based), and contributed to the manuscript.
Acknowledgments
This work is funded by NSF DEB 1110357, Marie Curie Career Integration
Grant EC 630652, an NSF GRF, Columbia University, and the American
Museum of Natural History (S.L.B.) and by the Swarthmore College
Research Fund and James Michener Faculty Fellowship (S.C.W.). We thankR. Benson, A. Dececchi, G. Dyke, H. Larsson, and M. Lee for discussion andthree anonymous reviewers for helpful comments. We thank those whohave contributed to the TWiG dataset: L. Chiappe, J. Choiniere, J. Clark,
J. Clarke, P. Makovicky, A. Turner, and L. Zanno.
Received: July 10, 2014
Revised: August 11, 2014
Accepted: August 14, 2014
Published: September 25, 2014
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