1
The ecology, tempo and mode of the
dinosaur to bird transition: examining
multiple aspects of a major evolutionary
event
Thomas Alexander Dececchi
Doctor of Philosophy
Department of Biology
McGill University
Montreal, Quebec
2011-12-15
A Thesis submitted to McGill University in partial fulfillment of the requirements
of the degree of Doctor of Philosophy.
Copyright Thomas Alexander Dececchi 2011
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DEDICATION
To my family, especially my fiance Jordana Laporte and my parents for
inspiration and support. Also to the menagerie of pets I have had over the years,
whenever I wonder why I study biology I just look at them and then remember
how wonderful nature is.
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ACKNOWEDGEMENTS
I would like to thank all members of the Larsson lab, both past and present for
discussions throughout this project. I would also thank my friends for listening
and tolerating me, with special thanks to Aleksandra Mloszewska for advice and
help with all French translations over the years. I would like to extend my thanks
to M. Carrano, P. Makovicky, C. Sullivan, K. Padian, D. Evans, J. Mller, M.
Vavrek, X. Xu and N. Campione, and many others for thoughtful discussions on
the topics contained herein. I would like to thank all the institutions that permitted
me to view specimens as well as the many individuals that provided me with
measurements. I extend great thanks to my supervisor Dr. Hans Larsson for his
guidance and knowledge but also for his patience with me and my writing. Finally
I would like to thank Jordana Laporte, my fiance and the most important person
in guiding me through this journey. Thank you for putting up with me.
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CONTRIBUTION OF AUTHORS
For all work presented herein I was the principal investigator and either
performed or help perform all analyses and interpretations. For all but one chapter
the sole investigators were my supervisor, Dr. Hans Larsson, and myself. In
Chapter III Dr. Larsson and I were joined by Dr. David Hone, then at the IVPP in
Beijing. For that project I was the lead investigator in all phases of the research,
though Dr. Hone and Larsson aided with the phylogenetic and dietary analysis.
While I am indebted to both Dr. Larsson and Dr. Hone for their help, the findings
and analysis presented in that chapter, as in all other chapters, is primarily my
own.
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ABSTRACT
The origin of birds is one of the major evolutionary events in vertebrate history.
The transition from non-avian to avian theropod dinosaurs encompass the origin
of powered flight, a suite of musculoskeletal adaptations for powered flight, and
early radiation of one of the most taxonomically and ecologically diverse groups
of vertebrates today. The evolution of flight has occurred only three times in
vertebrates: birds, bats and the extinct pterosaurs. Unlike either of the other two
clades where flight has evolved, bats and pterosaurs, birds have an extensive
fossil record documenting the evolution of flight related characters. This
exceptional record allows for a detailed examination of the origin of flight in ways
that are not possible in any other clade. In this thesis I will examine four separate
but interrelated aspects of the non-avian to avian theropod transition and comment
on how my findings shape our view of the origin of birds and powered flight in
vertebrates and the tempo and mode of a macroevolutionary transition.
The first chapter of my thesis is a detailed examination of character change in the
forelimb and pectoral girdle of Theropoda including the non-avian to avian
transition. This work focuses on both the placement and magnitude of character
change along the phylogenetic backbone from early theropods through to birds. I
created and scored 123 different theropod taxa and two outgroup taxa for 179
discrete skeletal characters taken from the theropod and basal bird literature and
traced these characters across all current phylogenetic hypotheses. Across these
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phylogenetic permutations, three nodes repeatedly showed significant increased
levels of evolutionary change: Tetanurae, Paraves, and Ornithothoraces. Notably
Aves itself did not have above average evolutionary change and in most
permutations had little to no character change in the forelimb at this node. This
punctuated signal and the lack of forelimb skeletal evolution at Aves supports the
hypothesis that the basic composition of the avian wing was in place before the
origin of birds, and that other factors had a significant role in the transition from
non-volant to volant locomotion.
Chapter two is a re-description and re-analysis of a small feathered maniraptoran
for the Jehol Biota Yixianosaurus longimanus. This taxon, which is known from
only a single specimen, is represented by an articulated and largely complete
forelimb and pectoral girdle. Under the supervision of Dr. Larsson and in
collaboration with Dr. David Hone then of the IVPP (Institute of Vertebrate
Paleontology and Paleoanthropology), I re-examined and scored the type material,
and estimated its phylogenetic relationships for the first time. The phylogenetic
analysis suggests that Yixianosaurus shares a basal position within Maniraptora,
near Coelurus and Therizinosauria. This re-description was incorporated into a
larger study of the proposed ecological niches selection of Jehol theropods based
on the linear bone measurements and morphology of the forelimb skeleton. I
tested whether proposed trends of manual proportions seen in this and other Jehol
theropods are both distinct from other theropods and demonstrate a highly derived
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grasping function that suggests climbing abilities. I found that the elongate manus
of supposed climbing theropods is not consistently present among these
theropods. Furthermore similar if not greater values for metrics proposed to show
high grasping potential than in arboreal theropods are also present in obligate
terrestrial herbivorous taxa such as Ornithomimosauria which are suspected to
have poor grasping abilities. This work adds to our understanding of the evolution
of Maniraptora by further refining the evolutionary characters and trends at its
origins and suggests more accurate functional characters and paleoecolgical
reconstructions for some advanced maniraptorans.
The third section of my thesis is a test of the arboreal origin of birds theory and an
examination of the paleoecological setting for the origin of the avian flight stroke.
This work presents the traditional trees down versus ground up debate on the
origin of flight in a testable framework. This was done using an extensive dataset
of 114 modern arboreal, scansorial, and terrestrial mammals, lizards, and birds
and a detailed examination of morphological signals previously linked to climbing
ability. This work demonstrates that all non-avian theropods and Archaeopteryx
group closer to terrestrial cursors than any climbing lineage. It also highlights the
differences between post-Archaeopteryx basal birds, which are generally accepted
to have had the ability to actively fly, and non-avian theropods in regards to
arboreal adaptations. Basal birds cluster closer to modern perching birds whereas
all non-avian theropods and Archaeopteryx cluster with strictly terrestrial avians,
8
such as ratites. This work strongly suggests that theropods were not arboreal until
after the origin of both birds and flight, and places the origin of the avian flight
stroke in a terrestrial context.
The final chapter examines the effects of allometry on the theropod appendicular
skeleton. Across Theropoda, there is a minimal 4 fold difference in adult body
size, with a trend of decreasing body size approaching and crossing the non-avian
to avian transition. Through the use of snout to vent length as a size proxy, a
common approach in extant vertebrates, both the absolute and relative scaling of
limb elements are studied. Using nodal reconstructions on trees encompassing 6
distinct phylogenetic hypotheses, the purported trend of maniraptoran theropods
elongating their forelimb beyond those expected by commensurate size reduction
are tested. The results suggest that non-paravian theropods have no signal of
forelimb enlargement beyond that expected through allometry. Furthermore this
study suggests that avians have shorter than expected hindlimb lengths, which
conflates the signal of forelimb enlargement seen in this clade. This work shows
the need to establish a baseline for interspecific limb analysis studies and
challenges some of the current models and evolutionary narratives surrounding
the origin of the avian forelimb.
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ABRG
L'origine des oiseaux est l'un des vnements majeurs dans l'histoire volutive des
vertbrs. La transition des dinosaures theropod en oiseaux comprends le vol
d'origine aliment, une suite d'adaptations musculo-squelettiques pour le vol
motoris, et le rayonnement au dbut d'un des groupes les plus taxonomiquement
et cologiquement diversifi de vertbrs aujourd'hui. Le vol a evolue
independament chez seuelement les oiseaux, les chauves-souris, et les pterosaurs, et
est le plus competement documentee chez les oiseaux, grace a une vaste record
fossilliere. Ce record exceptionnel permet un examen dtaill de l'origine du vol
de manire qui nest pas possibles dans les autres clades. Ici, on examine quatre
aspects distincts, mais interdpendants de la transition des theropodes non-aviaire
en thropodes aviaire, et on commente sur la faon dont mes conclusions
faonner notre point de vue de l'origine des oiseaux et vol propuls chez les
vertbrs et le tempo et le mode d'une transition macrovolutifs.
Le premier chapitre de ma thse est un examen dtaill des changement de la
ceinture pectorale de membres antrieurs dans les theropod y compris les
membres transitoires non-aviaire - aviaire. Ce travail se concentre sur le
placement et l'ampleur du changement de caractre le long du squelette
phylogntique partir des thropodes En utilisant un ensemble de donnes
construit sur mesure, j'ai marqu 123 taxons diffrents thropodes et les deux
taxons groupe externe pour 179 caractres discrets squelettiques issues de la
littrature d'oiseaux et de thropodes basale et jai trac ces changements travers
10
une srie d'hypothses phylogntiques actuelles. Au travers de ces permutations
phylogntique, trois nuds plusieurs reprises montr des niveaux
significativement accru de changements volutifs: Tetanurae, Paraves et
Ornithothoraces. Notamment Aves lui-mme n'a pas suprieure la moyenne des
changements volutifs et dans la plupart des permutations avait peu ou pas de
changer de personnage dans le membre antrieur ce nud. Ce signal ponctu et
le manque d'volution du squelette du membre antrieur au Aves soutient
l'hypothse que la composition de base de l'aile aviaire a t mis en place avant
l'origine des oiseaux, et que d'autres facteurs ont un rle important dans la
transition de la non-volant au volant de locomotion.
Le chapitre suivant est une re-description et r-analyse d'une petite maniraptoran
plumes pour le Jehol Biota Yixianosaurus longimanus. Ce taxon, qui est connu par
un seul spcimen, est reprsent par une ceinture articule et complte largement
antrieurs et pectoraux. Ici, sous la supervision du Dr Larsson et en collaboration
avec le Dr David Hone, ainsi quavec l'IVPP, jai r-examin et marqu le
matriel type, ainsi que estim ses relations phylogntiques pour la premire
fois. L'analyse phylogntique suggre que Yixianosaurus part une position basale
dans le groupe thropodes Maniraptora, prs Coelurus et Therizinosauria. Cette
re-description a t incorpor dans une tude plus vaste de la slection propose
niches cologiques des thropodes Jehol bas sur les mesures linaires et la
morphologie des os du squelette du membre antrieur. J'ai evalue si les tendances
des proportions proposes dans Yixianosaurus et d'autres thropodes Jehol sont
11
la fois distincte des autres thropodes et sils dmontrent une fonction hautement
drives saisissant qui suggre que les capacits d'escalade. J'ai trouv que le
manus allonge de supposs "thropodes escalade" n'est pas toujours prsents
chez ces thropodes. Par ailleurs les valeurs sont similaires, sinon les memes, pour
les paramtres proposs pour montrer fort potentiel saisissant que dans
arboricoles thropodes sont aussi prsents dans n'oblige taxons herbivores
terrestres tels que Ornithomimosauria qui sont suspects d'avoir de faibles
habilets de prhension. Ce travail ajoute notre comprhension de l'volution de
la Maniraptora en affinant encore les caractres volutifs et les tendances sa
base et suggre que plus prcise des caractres fonctionnels et des reconstructions
paleoecolgical pour certains maniraptorans avancs.
La troisime section de ma thse est un test de l'origine arboricole de la thorie
des oiseaux et un examen de la mise en palocologie de l'origine de la course de
vol aviaire. Ce travail prsente le debat traditionnel arbre bas versus zro \sur
l'origine de la fuite dans un cadre testables. Cela a t fait en utilisant un ensemble
de donnes tendue de 114 mammifres arboricoles modernes, scansorial, et
terrestres, les lzards et les oiseaux et un examen dtaill des signaux
morphologiques prcdemment lis la capacit d'escalade. Ce travail dmontre
que tous les thropodes non aviaires et de Archaeopteryx du groupe proche de
curseurs terrestre que toute la ligne d'escalade. Il souligne galement les
diffrences entre le post-Archaeopteryx oiseaux basale, qui sont gnralement
acceptes d'avoir eu la possibilit de voler activement, et non aviaires thropodes
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en ce qui concerne les adaptations arboricoles. Les oiseaux basales ple
rapprochent les oiseaux modernes perchs alors que tous les thropodes non
aviaires et des grappes d'Archaeopteryx aviaires strictement terrestre, tels que les
ratites. Ce travail suggre fortement que les thropodes ne sont pas arboricoles
qu'aprs l'origine de deux oiseaux et le vol, et place l'origine de la course de vol
aviaire dans un contexte terrestre.
Le dernier chapitre examine les effets de l'allomtrie du squelette appendiculaire
thropodes. Partout Theropoda, il ya un minimum de quatre fois plus de
diffrence de taille du corps adulte, avec une tendance la baisse la taille du corps
approche et franchissement de la non-aviaire la transition aviaire. Grce
l'utilisation de longueur museau-cloaque comme un proxy taille, une approche
commune chez les vertbrs existantes, la fois l'chelle absolue et relative des
lments du membre sont tudies. En utilisant des reconstructions nodale sur les
arbres qui englobe une srie d'hypothses phylogntiques actuelles, la tendance
suppose de maniraptoran thropode du allongeant leur patte avant-del de celles
attendues par la rduction de la taille proportionnelle sont tests. Les rsultats
suggrent que non paravian thropodes ont aucun signal de l'largissement au-
del des membres antrieurs prvu par allomtrie. En outre, cette tude suggre
que aviaires sont plus courts que prvu longueurs membres postrieurs, qui
assimile le signal de l'largissement des membres antrieurs vus dans ce clade. Ce
travail montre la ncessit d'tablir une base pour les tudes d'analyse
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interspcifiques des membres et des dfis certains des modles actuels et volutifs
des rcits sur l'origine de la patte avant aviaire.
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Table of Contents
Dedication ...............................................................................................................2
Acknowledgements ................................................................................................,3
Contribution of Authors..........................................................................................,4
Abstract....................................................................................................................5
Abrg.....................................................................................................................,9
1 Introduction to the problem of the origin of birds and its place as a
macroevolutionary transition..............................................................................22
1.1 Paleontology pre- and post synthesis...............................................................23
1.2 Theropod to bird transition..............................................................................25
1.3 History of the debate........................................................................................27
1.4 The origin and evolution of flight....................................................................29
1.5 Thesis focus.....................................................................................................,31
2- Patristic evolutionary rates suggest a punctuated pattern in forelimb
evolution before and after the origin of birds....................................................39
Bridging text..........................................................................................................40
2.1 Abstract............................................................................................................41
2.2 Introduction......................................................................................................42
2.3 Methods............................................................................................................43
2.4 Results..............................................................................................................48
2.5 Discussion........................................................................................................52
2.6 Figures
2-1.........................................................................................................................,56
2-2..........................................................................................................................58
2.7 Tables
15
2-1..........................................................................................................................60
2-2.........................................................................................................................65
2-3..........................................................................................................................68
2-4..........................................................................................................................70
2-5..........................................................................................................................72
2.8 Supplementary material
Taxon list...............................................................................................................74
Character list..........................................................................................................80
Matrix...................................................................................................................101
Supplementary Tables
S-1........................................................................................................................124
S-2........................................................................................................................132
S-3........................................................................................................................137
S-4........................................................................................................................139
S-5........................................................................................................................144
S-6 .......................................................................................................................149
S-7 .......................................................................................................................154
S-8 .......................................................................................................................159
S-9 .......................................................................................................................164
S-10 .....................................................................................................................169
S-11 .....................................................................................................................174
S-12 .....................................................................................................................179
S-13 .....................................................................................................................184
S-14 .....................................................................................................................189
S-15 .....................................................................................................................194
S-16 .....................................................................................................................199
S-17 .....................................................................................................................204
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S-18 .....................................................................................................................209
S-19 .....................................................................................................................214
S-20 .....................................................................................................................219
S-21 .....................................................................................................................224
S-22 .....................................................................................................................225
S-23 .....................................................................................................................228
S-24 .....................................................................................................................230
S-25 .....................................................................................................................232
S-26 .....................................................................................................................235
S-27 .....................................................................................................................238
S-28 .....................................................................................................................241
S-29 .....................................................................................................................242
Supplementary Figures
S-1 .......................................................................................................................243
3 Yixianosaurus longimanus (Theropoda: Dinosauria) and its bearing on the
evolution of Maniraptora and ecology of the Yixian fauna...........................245
Bridging Text.......................................................................................................246
3.1 Abstract .........................................................................................................247
3.2 Introduction ...................................................................................................248
3.3 Description ....................................................................................................249
3.4 Phylogenetic analysis ....................................................................................258
3.5 Comparisons to Coelurosauria ......................................................................261
3.6 Discussion .....................................................................................................274
3.7 Conclusions ...................................................................................................287
3.8 Figures ...........................................................................................................288
3-1 .......................................................................................................................289
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3-2 .......................................................................................................................290
3-3 .......................................................................................................................292
3-4 .......................................................................................................................294
3-5 .......................................................................................................................296
3-6 .......................................................................................................................298
3-7....................................................................................................................... 300
3.9 Tables
3-1 .......................................................................................................................302
3-2 .......................................................................................................................304
3-3 .......................................................................................................................306
3-4 .......................................................................................................................307
3-5 .......................................................................................................................311
3-6 .......................................................................................................................315
4 Assessing arboreal adaptations of bird antecedents: testing the ecological
setting of the origin of the avian flight stroke .................................................318
Bridging text .......................................................................................................319
4.1 Abstract .........................................................................................................320
4.2 Introduction ...................................................................................................321
4.3 Materials and Methods ..................................................................................324
4.4 Results and Discussion ..................................................................................330
4.5 Discussion .....................................................................................................339
4.6 Conclusions ...................................................................................................344
4.7 Figures
4-1 .......................................................................................................................347
4-2 .......................................................................................................................349
4-3 .......................................................................................................................351
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4.8 Supporting Information
Supporting Figures
S-1 .......................................................................................................................353
S-2 .......................................................................................................................356
S-3 .......................................................................................................................359
S-4 .......................................................................................................................362
S-5 .......................................................................................................................365
S-6 .......................................................................................................................368
S-7 .......................................................................................................................371
S-8 .......................................................................................................................374
S-9 .......................................................................................................................377
S-10 .....................................................................................................................380
S-11 .....................................................................................................................383
S-12 .....................................................................................................................385
S-13 .....................................................................................................................387
4.9 Supplementary Tables
S-1 .......................................................................................................................389
S-2 .......................................................................................................................399
S-3 .......................................................................................................................402
S-4 .......................................................................................................................409
S-5 .......................................................................................................................416
S-6 .......................................................................................................................422
S-7 .......................................................................................................................428
S-8 .......................................................................................................................431
S-9 .......................................................................................................................436
S-10 .....................................................................................................................442
S-11 .....................................................................................................................445
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S-12 .....................................................................................................................451
S-13 .....................................................................................................................457
S-14 .....................................................................................................................461
5 Allometric scaling and the origin of birds: how fore and hindlimb bone
length scales across Theropoda with emphasis on the non-avian to avian
transition.............................................................................................................463
Bridging text .......................................................................................................464
5.1 Abstract 465
5.2 Introduction ...................................................................................................466
5.3 Method ..........................................................................................................471
5.4 Results ...........................................................................................................480
5.5 Discussion .....................................................................................................487
5.6 Conclusions ...................................................................................................509
5.7 Figures ...........................................................................................................512
5-1 .......................................................................................................................513
5-2 .......................................................................................................................528
5-3 .......................................................................................................................530
5-4 .......................................................................................................................532
5-5 .......................................................................................................................534
5-6 .......................................................................................................................536
5-7 .......................................................................................................................543
5-8 .......................................................................................................................550
5-9 .......................................................................................................................557
5-10 .....................................................................................................................564
5-11 .....................................................................................................................571
5-12 .....................................................................................................................575
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5-13 .....................................................................................................................585
5-14 .....................................................................................................................592
5-15 .....................................................................................................................595
5-16 .....................................................................................................................597
5.8 Tables
5-1 .......................................................................................................................600
5-2 .......................................................................................................................603
5-3 .......................................................................................................................607
5-4 .......................................................................................................................611
5-5 .......................................................................................................................618
5-6 .......................................................................................................................623
5-7 .......................................................................................................................630
5-8 .......................................................................................................................636
5-9 .......................................................................................................................639
5-10 .....................................................................................................................642
5-11......................................................................................................................645
5-12 .....................................................................................................................649
5-13 .....................................................................................................................653
5-14 .....................................................................................................................655
5-15 .....................................................................................................................657
5-16 .....................................................................................................................667
5-17 .....................................................................................................................683
5-18 .....................................................................................................................687
5-19 .....................................................................................................................691
5-20 .....................................................................................................................694
5-21 .....................................................................................................................695
5-22 .....................................................................................................................697
21
5-23 .....................................................................................................................699
5-24 .....................................................................................................................702
5-25 .....................................................................................................................708
5-26 .....................................................................................................................712
5-27 .....................................................................................................................714
6 Summary of our understanding of the theropod to bird transition and
conclusions .716
6.1 Introduction ...717
6.2 Objective of this thesis ..720
References ......724
22
CHAPTER I
Introduction to the problem of the origin of Aves and its place as a
macroevolutionary transition
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1.1 PALEONTOLOGY PRE- AND POST SYTHESIS
Paleontology has long held a difficult place in the realm of Evolutionary
Biology (Hunt 2010). While it deals with one of the great sources of information
and the only primary source to understand the patterns and process of how clades
evolved, traditionally paleontology has had a rocky relationship with neontology
(see Gould 1980 for a summary). Ever since Darwin wrote about how The noble
science of Geology loses glory from the extreme imperfection of the record
(1859, p. 472) evolutionary biologists have spoke of the fossil record with an
almost apologetic tone. It did not help that many of the leading pre-synthesis
palaeontologist, such as Sir Richard Owen and H.F. Osborn rejected Darwinian
natural selection as the primary explanatory factor that shaped the history of life,
though neither doubted evolution itself (Osborn; 1922, 1933; Gould 1980;
Camadri 2001).
Championed most famously by Simpson, the incorporation of
paleontology into the modern synthesis brought the field in tune with the
mainstream biological thinking of the time (Gould 1980). With the publication of
his influential book Tempo and Mode in Evolution (1944) Simpson brought the
field from one of a collection and cataloguing to one that sought to explain and
hypothesis test like much of biological science. Simpson looked to the processes
and patterns seen in microevolution for explanations .This was unlike many of his
contemporaries who viewed changes documented in the fossil record as the result
24
of abiotic or at least non-adaptive factors (Gould 1980). In addition to
understanding the role of microevolution in shaping the history of life, Simpson
thought that the fossil record showed evidence for higher levels selection. To him
these macroevolutionary processes operated at longer time intervals and were not
simply extended periods of microevolution (Simpson 1944).
One of the major aspects of macroevolution in Simpsons mind, and
indeed the mind of many modern palaeontologists, is the divergence of higher
level clades (Simpson 1944; Erwin 2000; Jablonski 2000, 2008a, b). These
divergences were said to often correspond to the transition between Adaptive
Zones (1944) which are discontinuous peaks that populate the Adaptive
Landscape model. Simpsons Adaptive Landscape model presents us with method
to link both micro and macroevolution (Arnold et al. 2001) and explains the
discontinuous nature of the fossil record (Erwin 2000). At major transitions the
daughter groups diverge rapidly away from their ancestral fitness peak, quickly
crossing an area of low fitness to a new peak permitted by the acquisition of some
novel adaptation (Simpson 1944). These new adaptive zones often correspond to
new regions of evolutionary space that were previously unavailable to the clade
and may be driven by the colonization of new niches, morphological/ behavioural
evolution or the overcoming of a developmental constraint.
25
Once in a new zone there is often a release of previous constraints
(developmental, resources or competition) allowing for larger scale diversification
in the daughter adaptive zone compared to the ancestral zone or sister group
(Simpson 1953). It is the releasing from previous constraints at the crossing of
adaptive zones that links together two of the major concepts in macroevolution:
major evolutionary transitions and adaptive radiations (Futuyma 1986). One of the
classic examples of crossing adaptive zones in vertebrates is the origin of birds
(Guyer and Slowinski 1993) and powered flight (Carroll 1997).
1.2 THE THEROPOD TO BIRD TRANSITION
Modern Aves represents one of vertebrate evolutions greatest success
stories, both in shear diversity and in terms of their mastery of flight. Neornithes,
the clade that includes all living birds (Livezey and Zusi 2007), encompasses
between 9000-10000 species of extant birds (ICN, 2010; Lindow 2011 ) and
hundreds of fossil ones (Dyke and Gardiner 2011). Modern birds are the most
specious extant tetrapod clade (Kardong 2011) representing nearly a third of all
amniotes and almost 20% of known vertebrate diversity (ICN, 2010). Modern
avians are also ecologically and geographically diverse, being found on all
continents (Gill 1994). Due to their diversity and cosmopolitan nature birds have
a significant impact on the ecosystems providing critical ecological services
(Sekercioglu 2006).
26
Despite this extant species richness, the fossil record of modern birds
(Neornithes) is relativly depauperate compared to that of similar sized mammals
and reptiles (Fountaine et al. 2005; Lindow 2011). This lack of fossils has limited
our understanding of how modern avian groups evolved and the tempo, mode, and
timing of Neornithines origins and diversification is still debated (Feduccia 1995;
James 2005; Fountaine et al. 2005; Dyke and Gardiner 2011).
Counter intuitively, while our knowledge of modern bird evolution is still
poorly resolved our knowledge of the transition from non-avian to avian
theropods and the diversification of basal bird clades in the Early to Mid
Cretaceous is extensive (Padian and Chiappe 1998; Chiappe 2002; Chiappe and
Dyke 2006; Zhou and Zhang 2007; Clarke and Middleton 2008; Li et al. 2010;
Bell and Chiappe 2011; Xu et al. 2011). Much of this is due to the presence of
fossil Lagerstatten, deposits with exceptional preservation that allow for the
retention of extraordinary amounts of fossil information and often include soft
tissue structures (Selilacher et al. 1985). It is these types of beds that house a
large proportion of known Mesozoic avian diversity (Butler et al. 2009) and
allows for their study in great detail (Zhou and Zhang 2007). The most notable of
these Lagerstatten for the study of Mesozoic bird evolution are the Solnhofen
deposits of Germany, which yielded the first bird, Archaeopteryx (Wellenhofer
2008) and the Early Cretaceous aged Jehol beds of China (Zhou and Wang 2010).
27
The Jehol biota beds contain approximately a third of all known Mesozoic avian
taxonomic diversity and preserve representatives from all stages of basal avian
evolution (Li et al. 2010; Zhou and Wang 2010). This staggering diversity is only
increasing as new species are still being discovered regularly (Hu et al. 2011).
The plethora of well preserved specimens and their importance as a major
evolutionary event has lead to much interest in the theropod to bird transition
(Chiappe and Padian 1998; Chiappe 2003; Dial 2003; Xu et al. 2010, 2011).
Unfortunately, if this problem is approached without careful consideration that
interest is in danger of producing much heat, but little light.
1.3 HISTORY OF THE DEBATE
The history of the study of the origins of birds begins with the history of the first
bird, Archaeopteryx. The type specimen of Archaeopteryx is a single isolated
feather that was discovered in the lithographic limestone quarries of Solnhofen
Germany in 1860 and was described a year later (Griffith 1986; Wellnhofer
2008). Shortly after this the first skeletal material was discovered in the same
quarry (Wellenhofer 2008). This was a mostly complete and partially articulated
specimen that now resides in the British Museum of Natural History and is
referred to as the London specimen. Since than ten more specimens have been
described (Mayr et al. 2007), the most recent of which was announced in October
28
2011. This specimen has yet to be formally described. The individual
Archaeopteryx specimens are preserved in varying degrees of completeness
ranging from only limb elements to articulated individuals complete with attached
feathers (Ostrom 1985; Mayr et al. 2007; Wellnhofer, 2008). These specimens
also document a range of ontogentic stages from the young juvenile Eichsttt
specimen (JM 2257) to the sub-adult Solnhofen specimen (BMMS 500) (Erickson
et al. 2009).
Almost from the moment of its discovery, Archaeopteryx garnered much
attention in scientific circles. The early description presented it as a link between
reptiles and birds, a view that continues to this day (Ostrom 1985; Witmer 2002).
While the osteology of Archaeopteryx generally resembles that of a small
maniraptoran (Elzanowski 2002; Wellnhofer, 2008; Xu et al. 2011) it is the
presence of asymmetrical feathers preserved in articulation with the forelimbs that
has garnered the most interest. The size, shape and placement of these feathers
presented the possibility that Archaeopteryx could fly, though this has been a
source of much debate (Norberg 1985; Vazquez 1992; Elzanowski 2002; Senter
2006; Nudds and Dyke 2010).
Archaeopteryx has gained a large amount of public attention (Witmer 2002). and
is considered by many to be one of the most important fossils discovered (Hecht
29
1985).It is seen as a missing link between avian and non-avian reptiles
(Elzanowski 2002; Witmer 2002). As the classic missing link fossil
Archaeopteryx is often used as an education tool to teach evolution (Lawson
1999; Burton 2010). Although there has been recent controversy around its
phylogenetic placement (Xu et al. 2011) Archaeopteryx is generally considered to
be the first bird and is defined as such in many node based definitions of Aves
(Sereno 1999; Chiappe 2002; Chiappe and Dyke 2006). With the recent
discovery of feathered theropods and the numerous basal birds from China (Zhou
et al. 2010; Li et al. 2010) some even predating Archaeopteryx (Xu et al. 2010;
Xu et al. 2011) the debate over the pattern and process that drove the origin and
early diversification of birds has become more intense (Makovicky and Zanno,
2011).
1.4 THE ORIGIN AND EVOLUTION OF FLIGHT
Modern birds are closely associated with flight, as only 1% of extant or
recently extinct avian taxa are flightless (Roff 1994; McCall et al. 1998). Birds
are by far the dominate clade of extant aerial vertebrates having greater than ten
times the species richness as bats and far greater ecological impact (Sekercigolu
2006). Birds were not the first volant vertebrate clade as pterosaurs developed
powered flight minimally 80 million years before the first bird (Bonaparte et al.
2010). The origin of birds occurred approximately 150 million years ago and the
subsequent avian radiation is suspected to have been rapid, By the Early
30
Cretaceous (approximately 130 million years ago) avians had diversified into a
major factor in the Mesozoic ecosystems (Chiappe and Dyke 2006; Zhou and
Wang 2010). There is little evidence of competition between early birds and
pterosaurs despite the rapid diversification of birds and temporal overlap of the
two clades (McGowan and Dyke 2007; Dyke et al. 2008; Butler et al. 2009).
Of the three cases of powered flight originating in vertebrates (bats, birds
and pterosaurs) birds best document the transition from non-volant to volant
forms. Both bats and pterosaurs have very poor fossil records in regards to their
origins. Powered flight is present already in the oldest known specimens of each
group (Bonaparte et al. 2010; Simmons et al. 2008). This is in contrast to the long
transitional series of fossils that exist recording the evolution and refinement of
multiple flight related traits across non-avian and avian theropods (Chiappe 1995,
2002; Clarke and Middleton 2008; Dececchi and Larsson 2009; Xu et al. 2010).
The debate surrounding the origin of flight seeks to uncover the selective
drivers for one of the major evolutionary transitions in vertebrate life (Carroll
1997). Of the three known independent acquisitions of powered flight in
vertebrates it is birds that present us with the best opportunity to examine the
origin and evolution of a major locomotory and life history trait. The extensive
fossil records both pre-and post-dating the theropod to bird transition allows us to
31
examine the tempo, sequence and ecological setting of flight related character
evolution (Xu et al. 2010).
Previous authors have taken individual characters and created evolutionary
narratives surrounding their use. However, examining the large body of evidence
surrounding the non-avian/ avian transition allows us to test the different
ecological scenarios proposed for the origin of birds. It is these inquiries that I
believe are of great interest and importance in taking the study of the evolution of
avians beyond the cataloguing or narrative building that has surrounded it. I will
address these in this thesis.
1.5 THESIS FOCUS
This thesis examines four separate but interrelated parts of the study of
how one group of non-volant theropods evolved into volant avians. These
sections are: the study of the rate of forelimb evolution and placement of character
change; the reanalysis of a Chinese feathered theropod with implications for
maniraptoran evolution; the discussion of the ecological setting of the transition
and the origin of avian flight stroke; and the discussion of the effects of allometry
on patterns of fore- and hind limb evolution. Each section is covered by a
different project. Each project takes a different approach to viewing one of the
myriad of aspects of the evolution and diversification within Maniraptora with the
special focus on how these trends affect the origin of Aves. Each semi-
independent section of the overall study of the subject will be discussed in a
separate chapter; yet they fit into a single fundamental narrative. Some sections
32
have been published as independent studies. But, when viewed as a whole the
combination of all chapters presents the pattern and process of evolution across
the theropod to bird transition in greater detail.
Rates in Morphology
The study of evolutionary rates began with Simpsons Tempo and Mode in
Evolution (Simpson 1944; Haldane 1949; Gould 1980). Simpson demonstrated
that palaeontology could provide more than just the evidence that evolution
occurred, but it could also determine what form it took and, more importantly the
speed at which it took place (Gould 1980).
Building on Simpson, researchers sought practical and non-subjective
measures of evolutionary rate. Most emphasis has been placed on continuous
variables usually linear dimensions. There is debate surrounding their success,
however they remain the basic metrics used by morphologist for the past 60 years.
Classic measures like the Darwin, the Haldane or the Simpson are often used in
modern studies but for studies of extinct lineages in deep time these metrics
become unfeasible and other metrics are needed (Larsson et al. In press). One of
these metrics, patristic distance, is less precise but easier to apply to fossil data
from small sample populations from which measures such as generation time are
unknown.
33
Patristic distance analysis
Derived from the numerical taxonomic approach championed by Sneath and
Sokal (1972) patristic distance analysis is the sum total of all character changes
including reversals that occur along each phylogenetic branch between any two
nodes on a tree. This is the same as cladistic distance sensu (Jackson and
Cheetham 1994). It is a pairwise methodology allowing for comparisons of
relative rates of evolution between branches (Smith 1994). Patristic
methodologies are intimately linked to an a priori phylogenetic hypothesis and
any modification of this hypothesis will alter the calculated rate scores (Wagner
1997). The reliance on a particular phylogenetic reconstruction limits the use of
this methodology to well resolved clades. Additionally, patristic methods rely on
the assumption that all character changes are equally probable and equally
weighted. This uniform approach assumes that any state change in character 1 and
character 100 or the changing from states 0-1 and 1-2 within character 100 are
equivalent, independent of time. Attempts have been made to answer questions of
the limits of character spaces within lineages (Wagner et al. 2006), but little
attention is paid to these problems.
In Chapter II, patristic distance analysis is used to examine patterns of forelimb
evolution within Theropoda. This dataset was not used to create a toplogy due to
possiblility of convergent evolution due to functional similarity. Due to this
limitation I mapped the data onto a supertree constructed from numerous smaller
34
scale phylogenies independent of the data. The amount of change at each node
within the tree was counted. Due to potential effects of missing data the
phylogenetic axis from basal Saurischia to birds was the primary focus. The data
was permutated to account for different phylogenetic hypotheses regarding the
relationship between various taxa and the node Aves. The dataset was subdivided
into four different forelimb modules due to the possibility of differential patterns
of evolution within different parts of the limb. These modules are the pectoral
girdle, the stylopodium, the zeugopodium and the autopodium.
Morphology of the Maniraptoran Forelimb
As the primary generator of thrust and power during flight (Tobalske 2007) the
avian forelimb and pectoral girdle is central to the understanding of how flight
originated. While the anatomy of this region has been well categorized by
previous authors (Ostrom 1969; Nicholls and Russell 1985; Zanno 2006;
Jasinoski 2003; Wellenhofer 2008) there is work to be done to understand broader
patterns within this region. Previous authors have reported trends surrounding
intralimb and interlimb proportions which they have linked to behavioural or
ecological signals (Ostrom 1969, Xu and Wang, 2003; Xu et al. 2011). The most
commonly used metrics such as ratios of the humerus to femur (H:F), ulna to
humerus (B.I.) and manus to forelimb. These metrics are frequently cited as
showing trends of progressive elongation within derived maniraptorans into basal
avians (Hu et al. 2008, Zhang and Zhou, 2002; Xu et al. 2003, 2010, 2011, Novas
35
et al. 2009). Yet these analyse have seldom involved more than direct
interspecific comparisons. These analyses have not placed the findings into a
broader context, with regards to theropods in general nor to the influence of
scaling on the values obtained. Over the course of the final three chapters of the
thesis I will examine these purported trends in detail to distil adaptive functional
signals from the data that can be used to evaluate the origin of birds.
In Chapter III, in concert with my supervisor and Dr. D.W.E. Hone then at the
Institute of Vertebrate Paleontology and Paleoanthropology (IVPP) in Beijing, I
re-described a partial yet articulated small feathered theropod, Yixianosaurus
longimanus, from the Early Cretaceous Jehol Biota of China. The data in this
chapter elucidates the relationship between this relatively understudied taxon and
other coelurosaurs. The study also presents methods of comparing theropod
forelimb diversification that have broader implications for our understanding of
the ecological partitioning of the clade.
Chapter IV examines the question of the ecological setting for the origin of the
avian flight stoke by testing one of the arboreal theropod trees down hypothesis.
I focused on the flight stroke as opposed to flight itself as the flight stroke is a
necessary prerequisite for flight but is not restricted to it. In extant avians the
flight stroke has been modified into a variety of non-flight functions including:
36
Display (Merton et al. 1984; Zuk et al. 1995); maintaining a purchase on
struggling prey items (Fowler et al. In press); Wing Assisted Incline Running
(WAIR) (Dial 2003); or play (Bekoff and Byers 1998; Diamond and Bond, 2003).
Additionally the original function of the flight stroke may not have been linked to
flight as the thrust derived from the downward stroke could also have aided in
terrestrial locomotion by increasing running speed (Burgers and Chiappe 1999) or
to facilitate the traversing of barriers (Dial 2003).
The two prevailing hypotheses on the origin of flight are the terrestrial ground
up or the arboreal trees down views. The ground up postulates that the
ancestors of birds were small cursorial theropods that evolved feathers and the
flight stroke in a terrestrial context. There are a variety of proposed scenarios to
explain the origin of the flight stroke on the ground such as: to trap insect prey
(Ostrom 1979); to facilitate running (Burgers and Chiappe 1999); to aid in
jumping (Caple et al. 1983); or to aid in subduing captured prey (Fowler et al. In
press).
In contrast the trees down scenario involves an arboreal bird antecedent that
went through a gliding intermediate before evolving flight to move between the
trees (Dudley et al. 2007, Norberg 1985, Fedducia 1993, Chatterjee and Templin
2004, 2007, Zhou and Zhang 2002, Xu et al. 2000, 2003, 2010). Recently a new
scenario based on the behaviour of extant birds, WAIR (Wing Assisted Incline
Running), has been presented as a third possibility (Dial, 2003, Dial et al. 2008).
37
Some have questioned if these two hypotheses, ground up versus trees down,
represent a strict dichotomy (Padian, 2001; Witmer 2001, Dial et al. 2008).
Regardless whether or not this is true, and I would maintain it is not, the
ecological setting for the origin of the flight stroke is still of great importance as it
relates to the behaviour of the transitional forms. I tested if non-avian or basal
avian theropods possessed the necessary functional adaptations to overcome the
physical realities of life in the trees. I used a larger and more diverse dataset of
climbing amniotes than had been previously assembled and incorporated a range
of climbing styles and proficiencies. The results presented here are clear and
unequivocal, and should have an influence on the shape of future debates on this
topic.
In the final chapter (Chapter 5) I examine the potential linkage between allometry
and the perceived trends in forelimb length approaching the origin of birds. Along
the phylogenetic backbone towards Aves it has been noted that there is an
apparent increase in forelimb length (Xu et al. 2000; Chiappe 2004; Hu et al.
2008; Novas et al. 2009). Concurrently among coelurosaurian theropods there is a
trend of decreasing body size leading to Aves (Carrano 2006, Turner et al. 2007).
As body size is known to affect limb length (Alexander et al. 1979; Christiansen
1999) and I studied the relationship between limb length and body size across the
theropod to bird transition.
38
By creating both absolute and relative regression equations I determined both the
strength of each elements scaling relationship and also how proportional values
of the limb changed with scale. Taking a new approach this thesis examines how
the scaling affects major purported trends within derived theropod history leading
to and crossing the transition to avians. The study puts this transition into a proper
context by supplying a baseline against which taxon and clade specific deviations
can be measured. It also examines how early avians, in both the fore- and hind
limb, broke the non-avian theropod appendicular bauplan and suggests functional
and ecological reasons for these shifts.
39
CHAPTER II
Patristic evolutionary rates suggest a punctuated pattern in forelimb
evolution before and after the origin of birds
40
Bridging Text
The following section was published in the first issue of the 35th volume of the
journal Paleobiology in 2009. Here I examined the pattern of discrete character
change in the forelimb across Theropoda with special attention to the theropod to
bird transition. I constructed a comprehensive dataset scoring 123 theropods for
179 forelimb character taken from the literature. This data was then mapped on a
supertree constructed for a collection of smaller phylogenies. This topology was
also rearranged in multiple permutations to account for multiple different
phylogenetic hypotheses surrounding the placement of critical taxa. This work
showed that theropod forelimb evolution occurred in a punctuated manner and
that the node Aves is not a region of high character change. This work is
important for our understanding of the tempo and mode of a major evolutionary
transition.
41
2.1 ABSTRACT
The evolution of powered flight has traditionally been associated with the origin of birds,
the most successful clade of modern tetrapods, as exemplified by the nearly 10,000
species alive today. Flight requires a suite of morphological changes to skeletal anatomy
to create a light yet resistant framework for an airfoil and advanced nervous motor
control. Given the level of morphological integration necessary to create a suitable
aerofoil, the origin of flight may be intuitively assumed to be coupled with high
evolutionary rates of wing-related morphologies. Here we show that the origin of birds is
associated with little or no evolutionary change to the skeletal anatomy of the forelimb,
and thus Archaeopteryx is unlikely to be the Rosetta Stone for the origin of flight it was
once believed to be. Using comparative statistics and time-series analyses on a data set
constructed from all known forelimb skeletal anatomy of non-avian theropod dinosaurs
and a diverse assemblage of early birds, we demonstrate three focused peaks of rapid
forelimb evolution at Tetanurae, Eumaniraptora, and Ornithothoraces. The peaks are not
associated with missing data and remain stable under multiple perturbations to the
phylogenetic arrangements. Different regions of the forelimbs are demonstrated to have
undergone asynchronous periods of evolutionary peaks and stasis. Our results evince a
more complicated stepwise mode of forelimb evolution before and after the origin of
Aves than previously supposed.
42
2.2 INTRODUCTION
The origin of avian powered flight has been heralded as a key evolutionary novelty at the
origin of birds (Ostrom 1995). The evolution of avian flight required that theropod
dinosaurs dramatically modify their anatomy to accommodate the demands aerial
locomotion imposes: small body size (Padian et al. 2001), increased cerebellar and
cerebral brain volumes to coordinate flight (Alonzo et al. 2004), and an airfoil (Gauthier
and Padian 1985; Prum and Brush 2002). These evolutionary novelties in early birds
were so successful that soon after their first appearance in the Tithonian (ca. 150 Ma)
birds radiated into multiple diverse clades (Chiappe and Dyke 2006) and were the
dominant aerial vertebrate by the end of the Cretaceous. During this transition, bird
forelimbs underwent a profound remodeling as each element in the modern avian
forelimb was radically modified from its homologue in the earliest archosaurs. However,
previous analyses have shown that many avian skeletal (Sereno 1999), integumental (Ji et
al. 1998), and endocranial (Larsson 2001) characters are present in non-avian theropods,
suggesting these features were co-opted for flight by Aves from non-volant theropods.
We examined forelimb evolution within the non-avian to avian theropod
transition to assess the patterns of evolution of the skeleton most involved with avian
powered flight. Skeletal changes were ordered in a phylogenetic context to calculate
patristic evolutionary rates and allow for quantitative comparisons among selected
segments over bird evolutionary history. Preliminary steps using similar techniques to
examine evolutionary rates within early birds have been made (Chiappe 1995, 2002).
Here we have greatly expanded the focus and data set to examine the transitional period
and the origins of modern birds in both a qualitative and a statistical context. Unlike
Chiappe, we used multiple optimization routines to examine the distribution of character
43
change, testing a variety of phylogenetic hypotheses but not assuming that all elements
within the forelimb evolve in unison.
Because research on evolutionary rates about the origin of birds is still at an early
stage, we chose simply to assess rate variations along the phylogenetic axis from
Saurischia to Ornithothoraces (Supplementary Fig. 1). The first null hypothesis of
evolutionary rates we tested is that all rates are equal through the phylogenetic axis. This
most general null hypothesis is required where no other tests have been done before.
Given that rates are probably not equivalent throughout the tree, we also tested several
other hypotheses involving the origin of birds and avian powered flight. If the origin of
powered flight is accompanied by a suite of morphological adaptations for this mode of
locomotion, we would expect to see high rates of evolution about the transition (Carroll
1997). Thus, we can test whether or not significantly high rates of evolution of flight-
related morphologies coincide with the origin of Aves.
2.3 METHODS
Phylogenetic Framework
Phylogenetic relationships were based on a collection of nine current topologies obtained
from the literature (Supplementary Table 1). The phylogenies, which spanned the range
of non-avian theropod and early avian relationships, were concatenated to yield a tree
with 92 clades (Supplementary Fig. 1). The homoplastic nature of the forelimb characters
led to poor phylogenetic resolution when we used solely our data set (results not shown),
so we selected a pre-existing topology. This method also avoids circularity involved with
character evolution based on tree topologies derived from that same character data set.
44
Given the lack of a consensus phylogeny encapsulating theropods and including a diverse
assemblage of Mesozoic birds, we constructed an informal supertree (sensu Bininda-
Emonds 2004) using the phylogeny of Theropoda derived by Thomas Holtz from the
2004 edition of the Dinosauria (Holtz 2004) as our backbone. Because this concatenated
tree does address the relationships with Aves, we incorporated the phylogenetic topology
derived by Clarke and colleagues (2006) as the basis for the avian clades. The informal
method was chosen to reduce polytomies that result from the inadequate outgroup
sampling of some leaf phylogenies. Although informal supertrees are widely used, they
do have the inherent limitation of only allowing a single phylogenetic hypothesis to be
tested at a time (Bininda-Emonds 2004 and references therein). To compensate for this
we tested multiple different phylogenetic permutations (Table 1 and Supplementary
Tables 3-20) to represent the spectrum of recent proposed interrelationships among
derived maniraptoran taxa.
Lesothosaurus and Thecodontosaurus were used as non-theropod outgroups to
polarize character changes within Theropoda. We chose 123 different ingroup terminal
taxa representing 18 major nodes along the phylogenetic axis from Theropoda to
Ornithothoraces (Supplementary Tables 1). They include 1 herrerasaurid, 11
neotheropods (5 ceratosaurs and 6 coelophysids), 10 tetanurans, 7 allosauroids, 7 basal
coelurosaurs, 10 tyrannosauroids, 12 maniraptoriforms, 22 maniraptorans, 3
alvarezsaurids, 16 deinonychosaurians, 6 basal birds and 18 ornithothoracines. These taxa
represent the largest possible temporal, phylogenetic, ecological, and size-range diversity
known for Mesozoic theropods. These taxa represent a minimum of 22 clades,
encompassing a variety of life history strategies including: piscivory (spinosaurids),
insectivory (various small theropods and birds), omnivory (ornithomimids),
45
hypercarnivory (allosaurids, tyrannosaurids), and herbivory (therizinosaurs, Jeholornis,
Sapeornis). All taxa included a minimum of one forelimb skeletal element.
Character Database.
Discrete skeletal pectoral and forelimb characters were selected from nine independently
published theropod and early bird phylogenies and taxonomic descriptions for use in
scoring elements for this study (Supplementary Table 1). We selected character sets
from phylogenetic analyses that maximized the overlap across Aves and encompassed all
clades along the basal theropod to avian transition to minimize possible phylogenetic
edge effects and biased observations at particular nodes. Of these analyses, two included
both theropods and basal avians, five were for specific theropod clades, and two focused
on interrelationships of basal avian taxa, using theropods as the outgroup. All characters
from the phylogenetic analyses were concatenated, taking care to not have redundant
characters and character states. All taxa were scored for all possible characters by using
original scores from published sources and manually scoring the remaining characters.
Manual scoring entailed examination of relevant literature to determine character states
on the basis of descriptive, photographic, and/or illustrative evidence. All characters for
which no clear evidence was available were scored as a question mark. Scores for higher
classifications (e.g., at the family level) were not used, because these higher-level
amalgamations have the potential to mask species specific changes within lineages. In
cases where a taxon has been redescribed subsequent to the original phylogeny (e.g.,
Ornitholestes and Coelurus) or new material assigned to taxa (e.g., forelimb elements to
Tanycolagreus), these taxa were rescored manually. All specimens of Archaeopteryx
were considered as Archaeopteryx lithographica, although there is ongoing debate on the
status of species within the Archaeopterygidae (Mayr et al. 2007). All specimens of
46
Jeholornis prima and Shenzhouraptor sinensis were united under the senior synonym,
Jeholornis prima. The resulting data matrix (Supplementary Data Matrix) consists of
179 characters, divided into 402 total character states for the 125 non-avian and avian
taxa.
Character Evolution and Missing Data
Ancestral state reconstructions are limited to maximum parsimony methods because of
the multiple polytomies within this large phylogeny. Current maximum likelihood and
Bayesian methods require fully resolved tree topologies. We used three optimizations to
map charactersunambiguous, slow, and fast (Wincladas terminology)so that we
could capture the maximum range of character state changes (Nixon 2002). By
calculating the extreme possible values under accelerated and delayed models of
evolution, fast and slow optimizations allow use of data that cannot be unambiguously
optimized. This range of optimizations is expected to have encompassed the majority of
ancestral state reconstructions that maximum likelihood and Bayesian methods would
have yielded, when applied to a fixed tree topology with equal branch lengths and
discrete character data, had their use been possible.
Patristic rate methods have been used previously (Chiappe 1995, 2002; Sidor and
Hopson 1998) in attempts to determine relative rates of change among lineages where
absolute dating techniques are not available for all nodes. These methods assume uniform
branch lengths along the tree. We used patristic rate methods to examine if and when
nodes along the phylogenetic tree from Saurischia to Ornithothoraces show significantly
high levels of forelimb character change with respect to the average rate of forelimb
47
character change within the entire tree. Patristic methods do not impose a model for
evolutionary rate change a priori and allowed us to test whether the patterns seen in our
data were consistent with those seen in other data sets composed of skeletal characters
from the entire body and between modules of our own data set of forelimb data. Finally
this method allowed us to test whether our data showed signs of non-stochastic relative
rate changes and even to determine which nodes, if any, showed statistically significant
deviations from the mean expected values.
The distribution of character changes with the entire tree was performed by using
Winclada under the three different optimization modes to bracket the maximum and
minimum possible number of changes at each node (Fig. 1 AE). A total of 1265
character state changes are present on the tree topology but only those changes along the
phylogenetic axis from Theropoda to Ornithothoraces are presented here (Table 1).
Missing data estimates for each node were calculated by using the union of all characters
represented for both sister nodes (Supplementary Table 22). Union of characters, in this
context, consists of examining the overlap in character scoring for all stems to determine
the number of unscored characters at each node. This method was used in conjunction
with the different optimization regimes to assess possible effects of missing data in any
one taxon. However, missing data is not a factor in our results; all skeletal elements were
well sampled at each node along the phylogenetic axis examined here. Most nodes on this
axis are completely represented and only three approach 5% missing data once
unionized. We excluded the data on the sternum and furcula from the main
phylogenetic axis studies because these elements are largely absent in many of the taxa
sampled (only 14 of the107 non-avian taxa were scored for five or more of the 11
characters of these two elements). This reduced the number of pectoral skeletal characters
from 51 to 40, but did not significantly change our results. One-sample t- and
48
Kolmogorov-Smirnov (K-S) tests were used to assess changes in evolutionary rates.
Because character acquisition is an additive process, the K-S tests for differences between
the observed cumulative frequencies (the amount added per unit of patristic distance) and
the expected values (Zar 1999). We selected t-tests because at small sample size (n = 19)
they perform better than z-tests (Crawley 2005); they were also more robust when
deviations from normality assumptions occurred in our data (Zar 1999). Skewness is not
expected to be a major factor in our results because skewed one-sample t-tests undergo
only moderate loss of resolution (Nanayakkara 1992); applying Johnsons modification
for t-tests had no effect on number or identity of significant nodes (results not shown). In
addition, we performed a bootstrapping analysis to attempt to calculate significance of
single values within a non-normally distributed data vector (Table 2). Bootstrapping was
done by resampling with replacement the range of scores across the phylogenetic axis
nodes 10,000 times and calculating each samples mean. The distribution of the means
approached a normal distribution by virtue of the central limit theorem. Values of each
distribution for the 0.001, 2.5, 97.5, and 99.999 percentiles were calculated from each
distribution to provide a nonparametric test for significance for proposed significantly
active and inactive nodes. Time-series cross-correlation tests were performed in PAST
(Hammer et al. 2001) to examine whether evolutionary rates across different forelimb
regions were synchronized, showing a significantly similar distribution in two modules
signal frequencies.
2.4 RESULTS
A single phylogenetic path originating at Saurischia and extending to
Ornithothoraces is described to assess evolutionary changes about the avian node. The
49
use of a nonparametric cumulative frequency test such as the Kolmogorov-Smirnov (K-S)
indicated that there were significant deviations from the assumption of a uniform
distribution of character change between nodes along the Saurischia to Ornithothoraces
path (Table 3). The use of a K-S test as opposed to other two-sampled tests allowed us to
determine whether the pattern of cumulative character changes seen was within the
bounds of random variation around a uniform random model. In addition, the use of this
test instead of a simple linear regression allows for comparison of each node
independently, thus preventing Type II errors in the cases where nodes with higher than
mean character counts follow those with below-mean counts (though we do see a similar
pattern in a linear regression with multiple nodes exceeding the 95% confidence bounds;
results not shown). By exceeding the bounds, the K-S test showed that our data have
periods of significantly deviant accumulations of character change, which cannot be
explained by stochastic variations around a mean accumulation rate. The data follow a
punctuated pattern of character evolution, with most change occurring at irregular
intervals and the majority of nodes contributing little to the overall pattern (Table 3, Fig.
1A). We take this as evidence of an active trend in our data, because most nodes with
high rates of change are not associated with long ghost lineages (Supplementary Material
Tables 28, 29). The only node with both high rates of change and a large ghost lineage is
Tetanurae, but this node is distant enough from Aves to be of much importance to the
present analysis. Although the dismissal of the null hypothesis of uniform rates of change
was not unexpected, the identification and location of the significantly active nodes was.
We also performed one sample t-tests to determine which, if any, nodes
significantly violated the expected distribution of change under each scenario. These tests
allowed us to construct 95% confidence intervals around the mean distributions of nodal
scores, which we took as the limits of stochastic variability in character count. As shown
50
in Table 1 and Supplementary Tables 4-20, our data indicate that few nodes consistently
violate the upper bounds of these confidence intervals, and of these only three
consistently violate them under all optimizations, across the spectrum of permutations.
These nodes indicate periods of significantly higher than expected amounts of character
change, and are taken to be periods of active evolution in the forelimb. These nodes have
t-values much greater than those seen at even p = 0.0001; thus any Type I error effects
experienced from the moderate level of skewness in our data will not affect our
interpretation of the results. Large amounts of change that represent significantly
accelerated rates of evolution of the forelimb skeleton under all three optimizations are
concentrated at three nodes: Tetanurae, Eumaniraptora, and Ornithoraces. (Table 1, Fig.
1A). Tetanurae show accelerated changes in the hand and wrist that created the
foundation for the avian manus. This node features the reduction of the hand to three
digits, close oppression of the base of digits I and II, and the origin of a semilunate
carpal. These changes indicate an evolution of a novel predatory motion of the forearm
involving tightly bounded anterior digits and unique wrist flexion along the transverse
plane, all critical in the avian flight stroke (Padian 2001).
Significantly greater than expected change never occurs at the node Aves, and
under two optimization settings (unambiguous and fast) no changes to the forelimb
occurred. Evolutionary stasis at the origin of birds is unexpected, given the presumed
association between the node Aves and the origin of flight. A suite of phylogenetic
perturbations to accommodate alternative phylogenetic hypotheses have insignificant
effects on the phylogenetic position and magnitude of evolutionary peaks at
Eumaniraptora and Ornithothoraces (Supplemental Tables 4-20). These results suggest
that the pattern of significant periods of character evolution observed at these nodes are
robust results and not artifacts of the phylogenetic hypothesis used.
51
Module analysis shows patterns similar to those seen in the generalized forelimb.
The forelimb was divided into four anatomical regions to examine what elements of the
forelimb contributed to each of the evolutionary peaks. All characters describing the
pectoral skeleton, stylopodium, zeugopodium, and autopodium were examined separately
(Fig. 1BE, Supplemental Table 3). All modules show high levels of skewness in the data
and a large number of zero counts, thus leading to the possibility of Type I errors when
using a standard t-test. To compensate for this potential bias, bootstrapping was
performed to construct firmer (99.999%) confidence intervals, and thus reduce the
number of false positive results. Each anatomical region indicates patterns of
evolutionary peaks and stasis, and time-series cross-correlation analyses indicate that
only the pectoral girdle and zeugopodium are significantly similar, with shared peaks at
Maniraptora and Eumaniraptora, whereas the other skeletal regions evolved separately
(Table 4, Supplemental Tables 22, 23). We calculated percentages of total possible
changes per forelimb region were calculated to standardize for differences in character
number between regions, but the significant peaks and cross-correlations seen in these
results are identical to those of the absolute values presented above (Supplementary
Tables 24-26).
Cross-correlation analysis was performed to determine whether patterns in
periodicity existed both between our forelimb and a preexisting whole-body (minus
forelimb) data set and between modules. Cross-correlation analysis allows the frequency
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