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Biol. Lett.
doi:10.1098/rsbl.2011.0884
Published online
Palaeontology
Likelihood reinstates
Archaeopteryx as
a primitive bird
Michael S. Y. Lee1,2,* and Trevor H. Worthy3
1
South Australian Museum, North Terrace, Adelaide, South Australia
5000, Australia
2
School of Earth and Environmental Sciences, University of Adelaide,
South Australia 5005, Australia
3
School of Biological, Earth and Environmental Sciences, University
of New South Wales, Sydney, New South Wales 2052, Australia
*Author for correspondence ([email protected]).
The widespread view that Archaeopteryx was a
primitive (basal) bird has been recently challenged
by a comprehensive phylogenetic analysis that
placed Archaeopteryx with deinonychosaurian
theropods. The new phylogeny suggested that
typical bird flight (powered by the front limbs
only) either evolved at least twice, or was lost/
modified in some deinonychosaurs. However,
this parsimony-based result was acknowledged
to be weakly supported. Maximum-likelihood and
related Bayesian methods applied to the same
dataset yield a different and more orthodox
result: Archaeopteryx is restored as a basal bird
with bootstrap frequency of 73 per cent and
posterior probability of 1. These results are
consistent with a single origin of typical (forelimbpowered) bird flight. The Archaeopteryx–deinonychosaur clade retrieved by parsimony is supported
by more characters (which are on average more
homoplasious), whereas the Archaeopteryx–bird
clade retrieved by likelihood-based methods is
supported by fewer characters (but on average less
homoplasious). Both positions for Archaeopteryx
remain plausible, highlighting the hazy boundary
between birds and advanced theropods. These
results also suggest that likelihood-based methods
(in addition to parsimony) can be useful in
morphological phylogenetics.
Keywords: bird origins; Theropoda; maximum
likelihood; Bayesian inference; Archaeopteryx;
phylogeny
1. INTRODUCTION
The status of Archaeopteryx as a primitive (stem, basal)
bird has been almost universally accepted since its discovery over 150 years ago, and this iconic creature has
occupied centre stage in debates about avian origins
and evolution in general [1,2]. A recent study [3] presented the most compelling evidence to date challenging this
long-held assumption: addition of an intriguing new
dinosaur fossil (Xiaotingia) to one of the most comprehensive phylogenetic analyses of theropods removes
Archaeopteryx from birds and places it with deinonychosaurs. Thus, Archaeopteryx becomes just one of a
plethora of advanced bird-like dinosaurs [2–6], no
more closely related to living birds than (for instance)
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2011.0884 or via http://rsbl.royalsocietypublishing.org.
Received 12 September 2011
Accepted 6 October 2011
Velociraptor. This phylogeny has important implications
for the evolution of many features in early birds, such
as the morphology of the skull and the flight apparatus
[3,6]. However, it was acknowledged that the new
phylogeny required further investigation, owing to weak
support (Bremer support of 2 and bootstrap less than
50%; [3]). Also, as with most morphological studies,
only parsimony (cladistic) methods were employed.
Here, we show that maximum-likelihood and related
Bayesian methods, which are widely used in molecular
biology but infrequently in palaeontology and morphology, robustly restore Archaeopteryx as a basal bird.
Such likelihood-based methods are widely [7], but not
universally [8], thought to be superior to parsimony if,
for instance, some taxa are on disproportionately long
branches, or particular characters have evolved much
more rapidly than others. Such complexities are inherent
in palaeontological data, with stratigraphically young
and/or rapidly evolving taxa at the end of long branches,
and certain characters evolving much more rapidly
than others [9]. In particular, where one topology is supported by many fast-evolving (homoplasious) characters
and another by fewer but more conservative characters,
equal-weighted parsimony might favour the first solution, whereas likelihood methods might favour the
second solution.
The divergent retrieved positions of Archaeopteryx
(with birds using likelihood, with deinonychosaurs
using parsimony) indicate that a dramatic reinterpretation of bird origins is not yet required, and demonstrate
the potential utility of likelihood-based phylogenetic
methods in morphology.
2. METHODS AND TERMINOLOGY
Avialae sensu [3] refers to the most-inclusive cladecontaining modern birds (exemplified by Passer
domesticus) but not deinonychosaurs (exemplified by
Dromaeosaurus albertensis). Aves is often applied to a
more restricted node-based clade, e.g. that containing
Archaeopteryx and modern birds (see [2,4,5]). In the current phylogenetic context (figure 1), the above meanings
of Avialae and Aves contain the same set of (known) taxa;
we use the vernacular term ‘birds’ to refer to these taxa.
The data matrix of Xu et al. [3] was analysed using
parsimony, maximum likelihood (RaxML) and Bayesian
inference; formatted datasets with commands are
appended in electronic supplementary materials, S1–S3.
To confirm the published tree, the data were analysed
in PAUP [10], a different parsimony program to that
originally used. The following commands were used to
sample multiple tree islands but avoid memory overflow
on any large single island: hsearch addseq ¼ random
nreps ¼ 100 nchuck ¼ 1000 chuckscore ¼ 1. Strict and
majority-rule consensus trees were computed from the
most-parsimonious trees.
The data were also analysed with maximum likelihood
and Bayesian inference. Both analyses used the Lewis
[11] stochastic model with a gamma parameter to
account for rate variation across traits; Allosaurus was
set as the outgroup, and multi-state characters were
unordered (as per the original analysis [3]). Likelihood
analyses (figure 1) employed RAXML v. 7.2.8 [12],
with 1000 bootstraps followed by a maximum-likelihood
search: commands employed were -f a -m MULTIGAMMA -K MK -#1000. As RaxML cannot accept
This journal is q 2011 The Royal Society
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2
M. S. Y. Lee & T. H. Worthy
Allosaurus
Sinraptor
99
95
Archaeopteryx reinstated as a bird
Gorgosaurus
Tyrannosaurus
Eotyrannus
Dilong Tanycolagreus
Coelurus
82
Huaxiagnathus
77
Sinosauropteryx
88
Compsognathus
Haplocherius
Harpymimus
88
Deinocheirus
63
74
68 Shenzhousaurus
Pelecanimimus
88
68 Garudimimus
72 Archaeornithomimus
95 Gallimimus
Struthiomimus
Anserimimus
87 98 Ornithomimus
Ornitholestes
corrected divergence
Falcarius
76
Beipiaosaurus
79
0.2 ( = 20%)
64 Alxasaurus
Nanshiungosaurus
56
Nothronychus
72 Erliansaurus
55 Neimongosaurus
Segnosaurus
Therizinosaurus
Erlikosaurus
57
61
98
Alvarezsaurus
Patagonykus
93
100
Shuvuuia
Mononykus
Protarchaeopteryx
52
Incisivosaurus
52
Similicaudipteryx
Caudipteryx
Avimimus
Microvenator
Oviraptor
98 Ingenia
85
Heyuannia
Khaan
Conchoraptor
60
Rinchenia
IGM10042 unnamed oviraptorid
51
Citipati
Chirostenotes
58
Elmisaurus
Hagryphus
Archaeopteryx
Avialae/Aves (birds)
73
Wellnhoferia
W
ll h f i
Jeholornis
99
Epidendrosauruss
82
Epidexipteryx
Sapeornis
52
Confuciusornis
f
69
90
Protopteryx
80
Yanornis
Xiaotingia
Anchiornis
Deinonychosauria
91
Sinovenator
Mei
Byronosaurus
92
Sinornithoides
Si
ih i
73
IGM100 44 unnamed troodontid
96
z
Zanabazar
79
Troodon
100
78 Saurornithoides
56
Buitreraptor
68
Unenlagia
on i
Rahonavis
88
100 Sinornithosaurus
99
NGMC91 unnamed dromaeosaurid
68
Microraptor
Bambiraptor
bi
77
IGM1001015 unnamed dromaeosaurid
Adasaurus
89
Velociraptor
511 Saurornitholestes
S
ith
h l
90 Deinonychus
Atrociraptor
Achillobator
A
hhill b
83
Dromaeosaurus
76
Utahraptor
600
Figure 1. Archaeopteryx robustly reinstated as the most basal bird by maximum likelihood (RaxML tree, log L 27608.41). Birds
(including Archaeopteryx) is supported by likelihood bootstrap of 73%.
polymorphic cells for morphological data, these were
changed to ‘?’ for the RaxML runs. This affected only
eight out of 33 286 cells (0.024%) and was expected to
have almost no influence on the resultant topology; parsimony analyses were performed with the polymorphic
cells altered to ‘?’ to test this assumption.
Bayesian analyses (figure 2) employed MRBAYES
v. 3.1 [13], with coding set to variable (to reflect lack
of invariant characters in matrix). Four independent
runs were used, each consisting of four (one cold
and three heated) chains of 10 million generations,
sampling every 2000 generations, with a majorityrule consensus. The first 40 per cent of each chain
was discarded as burn-in. Convergence across runs in
topology and parameters, respectively, was confirmed
by (i) split frequencies which had a low standard deviation of approximately 0.01 [13] and were highly
correlated [14] (figure 2b), and (ii) effectively identical
distributions of parameters which all had high effective
sample sizes exceeding 1000 [15].
To evaluate whether differential treatment of fastevolving (homoplasious) characters might be driving
the different topologies retrieved by parsimony,
Biol. Lett.
likelihood and Bayesian analyses, pairwise comparisons
of trees from these three methods were performed
using PAUP. The single best likelihood tree was used,
along with the resolved majority-rule consensus trees
from parsimony and Bayesian analyses (as characters
should not be optimized on unresolved strict consensus
trees). The characters which differentially supported
each tree and their average consistency and retention
indices [16] were ascertained. Analogous calculations
are not possible in current versions of RaxML and
MrBayes.
3. RESULTS AND DISCUSSION
Analysis using PAUP confirmed the heterodox position
of Archaeopteryx with deinonychosaurs retrieved by
parsimony [3], exactly replicating the strict consensus
tree, and optimal tree length of 1404, found in the
original study using a different program. While many
more most-parsimonious trees were found (99 000),
the original study [3] did not claim to exhaustively
sample MPTs, and the true number is likely to be
much higher than even the number found here.
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M. S. Y. Lee & T. H. Worthy
Archaeopteryx reinstated as a bird
(a)
3
Avialae/Aves (birds)
Archaeopteryx
Wellnhoferia
Jeholornis
1.0
1.0
0.61
1.0
Epidendrosaurus
Epidexipteryx
Sapeornis
0.72
0.73
corrected divergence
0.93
1.0
Confuciusornis
Protopteryx
Yanornis
0.2 (= 20%)
(b) 100
100
0
run 1 split frequencies
run 4 split frequencies
run 3 split frequencies
run 2 split frequencies
100
100
0
run 1 split frequencies
0
100
100
run 1 split frequencies
Figure 2. (a) Archaeopteryx united with other birds (posterior probability 1.0) in Bayesian analysis. Relevant part of MrBayes
majority-rule consensus shown; remainder of tree was also very similar to the likelihood tree in figure 1. Harmonic mean
log L of sampled trees 25689.40. (b) Frequencies of splits found in Bayesian run 1, plotted against frequencies found in
the other three runs, using AWTY [14]; all splits occurred at similar frequencies across all runs.
Table 1. The character evidence favouring the parsimony, maximum likelihood and Bayesian trees. Pairwise comparisons
using parsimony showing the number of characters (n) which differentially favour one tree over another, and the mean
consistency (ci) and retention (ri) indices for those suites of characters (averaged over both trees being compared).
favouring tree (1)
favouring tree (2)
comparison
n chars
average ci
average ri
n chars
average ci
average ri
(1) MP versus (2) ML
(1) MP versus (2) Bayesian
(1) ML versus (2) Bayesian
64
69
12
0.312
0.31
0.253
0.666
0.677
0.586
49
51
5
0.354
0.369
0.493
0.728
0.739
0.76
Changing the eight polymorphic cells to ‘?’ (question
mark) resulted in exactly the same consensus topology
and tree length of 1404 (i.e. all eight polymorphic cells
were analytically equivalent to ’?’). Thus, the necessary
recoding implemented in the RaxML analysis is
unlikely to have biased those results.
The maximum-likelihood and Bayesian analyses
produced a similar overall topology to parsimony, but
with one striking difference (figures 1 and 2a): Archaeopteryx and the very similar Wellnhoferia grouped with
birds, rather than with deinonychosaurs. Notably,
this more orthodox grouping of Archaeopteryx and
birds has at least moderate support (73% ML bootstrap, 1 Bayesian posterior probability). In contrast,
the heterodox grouping of Archaeopteryx with deinonychosaurs in the parsimony analysis was acknowledged to
be weakly supported [3]. The positions of Xiaotingia and
Anchiornis are poorly resolved; they group weakly with
troodontids among deinonychosaurs [17] (figure 1)
and if so, are no longer part of Archaeopterygidae sensu
Xu et al. [3].
Examination of the character support for the
parsimony, likelihood and Bayesian trees suggests a possible explanation for the divergent placement of
Biol. Lett.
Archaeopteryx. ‘Unweighted’ parsimony remains the
most common method of analysing morphological
data, and treats changes across all branches and across
all characters equally [18]. In contrast, the likelihood
and Bayesian models used here preferentially concentrate homoplasy on longer branches and/or faster
characters (characters are assigned to rate categories
following a discretized gamma distribution, using information intrinsic to the dataset). Examination of the
characters which differentially support one tree over
another is illuminating (table 1). More characters support the parsimony tree over the likelihood tree than
vice versa (64 versus 49). However, the characters supporting the parsimony tree are generally more labile
than those supporting the likelihood tree (ci 0.312
versus 0.354, ri 0.665 versus 0.728). The same pattern
is found when the parsimony and Bayesian trees are compared (69 versus 51; ci 0.310 versus 0.369, ri 0.677
versus 0.729). This is consistent with the difference in
tree topologies being at least partially driven by parsimony preferring trees supported by more (but on
average more homoplasious) characters, and likelihood
and Bayesian analyses preferring trees supported by
fewer (but on average more conservative) characters.
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4
M. S. Y. Lee & T. H. Worthy
Archaeopteryx reinstated as a bird
As expected, very few characters differentially support
the (very similar) likelihood and Bayesian trees
(12 versus 5), so not much weight should be put on the
differing average ci and ri of these small suites of
characters.
The likelihood and Bayesian topology is supported by
several derived characters which are unique and unreversed (but which are homoplasious on the parsimony
tree). These include traits unique to Archaeopteryx and
other birds, such as evenly spaced anterior maxillary
teeth (character #89) teeth and anterior chevrons with
flattened plate-like base (#122; but see [19]), as well as
traits unique to Xiaotingia, Anchiornis and troodontids,
such as anterior caudal vertebrae with distally tapering
transverse processes (#373). Conversely, some of the
similarities between Archaeopteryx and deinonychosaurs,
interpreted in the parsimony analysis as shared derived
characters [3], need to be reinterpreted as primitive characters of all birds and deinonychosaurs (paravians),
secondarily lost in birds above Archaeopteryx and Wellnhoferia. These include hyperextensibility of the second
(¼ first functional) toe (character #323), a posterior process on the ischium (#334) and a distally located
obturator process (#167).
The reinstatement of Archaeopteryx as a basal
bird in both likelihood-based analyses contradicts
macroevolutionary inferences that relied (at least
partly) on the shift of Archaeopteryx into deinonychosaurs. For instance, it does not support the proposal
that robust skulls and herbivory are primitive for
birds [3]. It also has important implications for the
evolution of flight. Powered, forewing-only flight typical
of modern birds has been generally inferred to be present
only in Archaeopteryx and other birds [2,5,20]. The flight
capabilities of some deinonychosaurs remain contentious: the most proficient, Microraptor gui, used both
the forelimbs and hindlimbs, and has been argued to
be a glider [21] and asymmetric pennaceous feathers
indicating aerodynamic ability are known only in dromaeosaurus outside of birds [22]. The likelihood-based
phylogenies are consistent with a single origin of typical
forewing-driven flight with no losses in basal birds (i.e.
the taxa here sampled); in contrast, the parsimony tree
implies either minimally two origins (in Archaeopteryx/
Wellnhoferia, and in ‘true’ birds), or an earlier origin
at the base of Paraves (with subsequent reduced flying
ability or modifications to four-winged locomotion
in various deinonychosaurs; [17,21]).
The results here do not demonstrate unequivocally
that Archaeopteryx belongs with birds rather than with
deinonychosaurs; bootstrap support is only approximately 73 per cent, while the posterior probability of 1
is tempered by arguments that Bayesian inference can
greatly overestimate support if the models implemented
are inadequate [8,23]. Resolution of the precise position
of Archaeopteryx will likely require more empirical data
such as new fossils or novel characters. The alternative
placements of Archaeopteryx highlight the closure of the
morphological gap between birds and theropod dinosaurs [2–6,17,22], and also suggest that dramatic
reinterpretations of early bird evolution are not yet
required. Furthermore, the more generally accepted
tree, found with likelihood-based methods (and the
strong contrast with parsimony), suggests that
Biol. Lett.
likelihood-based phylogenetic methods should be used
more often in palaeontology and morphology [24],
especially for large datasets [3] that have sufficiently
large numbers of characters to allow critical parameters
in likelihood models to be robustly estimated.
We thank the Australian Research Council linkage grant
scheme for funding, Xing Xu and two anonymous referees
for comments, and Sam Morrison and the Australian
Research Collaboration Service for use of cloud computing.
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Likelihood reinstates Archaeopteryx as a primitive bird