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,

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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

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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

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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

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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

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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

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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