Palacký University Olomouc

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Faculty of Science

Department of Zoology and Laboratory of Ornithology

Developmental modularity of cerebral tissues in the evolution of avian locomotion using high

resolution imaging and geometric morphometric

Ph.D. Thesis

Vincent Beyrand

Supervisors: Prof. Stanislav Bureš

Dr. Paul Tafforeau

Olomouc 2018

Promoter

Prof. Stanislav Bureš Palacký University in Olomouc Faculty of Science Department of Zoology and Laboratory and Laboratory of Ornithology 17. listopadu 50 Olomouc 771 46 Czech Republic

Dr. Paul Tafforeau European Synchrotron Radiation Facility Beamline ID19 38 avenue des Martyrs 38000 Grenoble

Opponents

Dr. Stig Walsh Department of Natural Sciences National Museums of Scotland Chambers Street Edinburgh EH1 1JF

Prof. Eric Buffetaut Centre National de la Recherche Scientifique UMR 8538 Ecole Normale Supérieure de Paris 24 rue Lhomond 75231 Paris CEDEX 5

« Life always find a way »

Michael Crichton

I declare that this thesis is my original work and has not been submitted for the purpose of obtaining the same or any other academic degree earlier or at another institution. My contribution to each to each of the chapters comprising this work is expressed through the autorship order of the included chapters and author’s contribution statements complementing the chapters.

Chapter 4 and 6 are/is reproduced with kind permission from the publishers

Olomouc, 31st January 2018

……………………………….

Vincent Beyrand

Bibliographic identification

Name and surname of the author: Vincent Beyrand Title: Developmental modularity of cerebral tissues in the evolution of avian locomotion using high resolution imaging and geometric morphometric Type of thesis: PhD thesis Department: Department of Zoology and Laboratory of Ornithology, Palacký University Supervisors: Prof. Stanislav Bureš Dr. Paul Tafforeau Study program: P1527 Biology Study field: Zoology Year: 2017

Abstract

Archosaurs is one of the vertebrate group with the longest history and the oldest origin. Through their long evolutionary history, they developed a large variability of size, morphological features and locomotion behaviours. Flight is a particular behaviour that has been developed twice independently by archosaurs during their evolution. As a complex locomotory behaviour, flight requires advanced cognitive capabilities in order to deal with all the information necessary for a proper locomotion. As the center of processing of information and selection of appropriate response, brain is an important structure to study in order to understand how cerebral capacities in archosaurs evolved in parallel of flight evolution. Because of its position at the root of birds, Archaeopteryx from the Jurassic of Germany, is a very important taxon as it is considered as the oldest form having developed active flight capabilities in the avian lineage. The study of the features showed the different Archaeopteryx specimens add information on how flight capabilities evolved in birds. Another important point of this evolutionary process is the mechanism leading to the appearance cerebral of features related to flight. In this respect,

Haslzkaraptor escuillei, a small dromaeosaur from the Cretaceous of Mongolia, is a key specimen, showing brain characters very similar to Archaeopteryx, despite the fact that it was clearly not a flying animal and probably not having flying ancestors.

This thesis focuses on the study on the general shape of the endocast and the evolution of its coiling along the development of flight within archosaurs. A new Mongolian dromaeosaur, with particular features revealing a new ecomorphology and particular cerebral characteristics have also been studied during this thesis, with a particular focus on the neurovascular sytem into the snout, dentition organisation and brain anatomy. Because of the rareness and delicacy of fossil specimens bringing information about the origin of flight, their studies does not allow the use of destructive methods. As those fossils cannot be fully extracted from their rock slab, we need special methods in order to access as much as possible information on their anatomical characters for understanding their living behaviour.

For that, we used X-ray imaging methods available at the European Synchrotron Radiation Facility, which are considered nowadays as the golden standard for non-destructive 3D investigation of fossils.

Along archosaurs evolution toward flying forms, endocasts show an increase of coiling as well as of infilling level by the brain itself. Basal archosaurs such as crocodiles show an elongated and low- filled endocast, reflecting the primitive condition observed in lepidosaurian. Non-maniraptoriform dinosaurs and then Maniraptoriforms show two successive events of coiling increase, but only small maniraptoriforms suggest an increase of infilling. In crocodiles and non-maniraptoriforms dinosaurs, coiling and low infilling are independent from body size, contrary to maniraptoriforms for which small specimens do present a higher filling level than large sized specimen, for similar coiling values. Finally, birds show a total decoupling of those two characters and size. This general pattern is observed during crocodilian embryonic development, for which coiling and infilling decrease along ontogeny. This suggest a serie of progenetic events, associated with a general size reduction, along archosaurs lineages toward flying forms which was leading to cerebral shape unlocking the cerebral capabilities for flight.

Further studies would require more research on shape modification of the different brain structure, by defining which character of brain anatomy influence flight specialisation, fossil reconstruction of crushed fossil in order to have a more accurate view of the process originating flight.

Keywords : archosaur, endocast, coiling, infilling, developmental heterochrony, paedomorphosis, flight origin

Number of pages : 235

Language : English

Content

Abstract (in English)…………………………………………………………………………………….1

Chapter I General introduction……………………………………………………………………….7 I-Evolution of archosaurs……………………………………………………………………….9 I-A-Evolutionary history of archosaurs and origin of birds……………………….……9 I-B-Development of flight within Archosauria……………………………………….13 I-C-Influence of developmental heterochrony within Dinosauria…………………….14 II-Paleoneuroanatomy…………………………………………………………………………16 II-A-Brain organisation……………………………………………………………….16 II-B-History of paleoneuroanatomy…………………………………………………..24 II-C-Review of brain anatomy in bird-line through the evolution of flight……………27

Chapter II Bi-energy imaging for neuroanatomical features………………………………………31 I-Generalities and history of imaging methods………………………………………………...33 II-Use of contrast agent and bi-energy scans…………………………………………………..34 III-Propagation phase contrast………………………………………………………………...39 IV-Combined use of K-edge/bi-energy and propagation phase contrast imaging techniques….39 V-Application to neuroanatomy……………………………………………………………….42

Chapter III Fossils…………………………………………………………………………………….49 I-Compsognathus longipes…………………………………………………………………….51 II-Halszkaraptor escuillei……………………………………………………………………..56 III-Archaeopteryx……………………………………………………………………………...64

Chapter IV Synchrotron scanning reveals amphibious ecomorphology in a new clade of bird-like dinosaurs…………………………………………….....73

Chapter V Geometric morphometrics analysis and cerebral information reflecting evolutionary history of archosaurs and the development of flight………………………91 I-Geometric morphometrics and application in paleontology………………………...93 II-Three-dimensional geometric morphometric analysis……………………………..93 III-Qualitative accuracy of endocranial representativity of brain anatomy…………113

Chapter VI Developmental evolution of the brain enabled archosaurian flight………………………………………………………………….119

Chapter VII Progenetic scenario within Archosauria……………………………………………..195

Co-author affiliation…………………………………………………………………………………..201

Bibliography………………………………………………………………………………………….203

Acknowledgments……………………………………………………………………………………236

Abbreviations: ESRF: European radiation Synchrotron Facility; ESRF collection: Specimen

preserved at the European Synchrotron Radiation Facility; LFAC: La Ferme aux Crocodiles,

Pierrelattes, France; TL: Thierry Loeb, Echirolles, France; ENS: Ecole Normale Supérieure,

Lyon, France; MHN Grenoble: Museum d’Histoire Naturelle, Grenoble, France; MNHN:

Museum National d’Histoire Naturelle, Paris, France; CCEC: Centre de Conservation et d’Etude

des Collections, Lyon, France; Peaugres: Safari de Peaugres, Peaugres, France.

Chapter I General introduction

I-Evolution of archosaurs

I-A-Evolutionary history of archosaurs and origin of birds

Archosaurs find their origin during the early Triassic, after the split with Lepidosauria, their sister taxa within Diapsida (Romer 1966, Reig 1970, Benton and Clark 1988). Along their evolutionary history, they developed particular posture from sprawling to erect and semi-erect (Edwards 1977, Parish

1987, Reilly and Elias 1998). This variation of limb position influenced the large amount of locomotory behaviour that have been developed within this lineage (quadrupedal/bipedal, terrestrial/aquatic/flying,…) leading to a large range of body shape (Hutchinson and Gatesy 2000,

Hutchinson 2006, Bates and Schachner 2012, Allen et al. 2013). Archosaurs are only represented by living crocodilians and birds nowadays, but they were also represented by dinosaurs, pterosaurs and fossil forms of crocodylomorphs (Figure I-1).

Crocodilians are the most primitive archosaurian group (Figure I-1). They are, with birds, the only extant groups of archosaurs (Walker 1972, Gauthier 1986). This group appeared in the Late Triassic

(225 million years ago), represented by the genera Protosuchus (Brown 1933, Brown 1934). If this group did not developed different posture and locomotion mode, as the majority of crocodiles are semiaquatic species with semi-erected posture, they did show various body size in extant forms from the 1.5 meters for Paleosuchus palpebrosus to almost 7 meters for Crocodylus porosus, and up to 12 meters for the extinct Cretaceous Sarcosuchus imperator (Broin and Taquet 1966). If young individuals of extant taxa eat fish and insects, adults are mainly carnivorous, with some species showing extreme morphological adaptation for piscivory, as the gavialidae Gavialis gangeticus or the Crocodylidae

Crocodylus cataphractus, which present a more slender snout and tiny teeth compared to the enlarged snout of carnivorous species such as Crocodylus niloticus (Cuff and Rayfield 2013). One of the important structures of this group, related to amphibious predatory behaviour is the development of a complex neurovascular system on the snout, with hollow structures related to a neurovascular mesh used as a sensory system to feel underwater vibrations from potential preys (Witmer et al. 2008), also find in aquatic lepidosaurian (Foffa et al. 2014) as well as in Theropoda (Barker et al. 2017, Cuesta et al. 2018),

9 and more particularly in Spinosauridae (Dal Sasso et al. 2005, Ibrahim et al. 2014, Vullo et al. 2016,

Hone and Holtz 2017). For the purpose of the following studies, because they mostly preserved their morphological organisation along their evolutionary history, this group is considered as presenting on many aspects the primitive state of archosaurian morphology, as this bauplan, mainly limb position and locomotion modes, is close to what is observed in their close relatives, like lepidosaurs.

Disapeared at the end of the Cretaceous, pterosaurs were the main archosaurian flying group during the Mesozoic, before the rise of flying birds. The oldest specimens of pterosaurs are

Eudimorphodon ranzii (Zambelli 1973) and Faxinalipterus minima (Bonaparte et al. 2010), and even if their phylogeny is quite well understood, their archosaurian origin remain unclear. If some studies place

Scleromochlus taylori at their early origin (Padian 1984, Bennett 2000, Peters 2000) those results are still highly debated (Hone and Benton 2007). This taxon seems finally to be closer to dinosaurs than to pterosaurs (Nesbitt et al. 2017). Another specimen with a well-developed uropatagia, Shaviropteryx, have also been considered as a potential ancestor of pterosaurs (Peters 2000). If the origin from terrestrial archosaurmorph to flying pterosaurs originated during the Triassic, it seems that morphological transformation went very quickly and there is still no fossil specimen known presenting an intermediate morphology. It makes difficult to understand the transition leading from terrestrial ancestor to primitive flying pterosaurs (Bennet 1997). All the known pterosaurs were flying species, from the small body sized species to the gigantic Azdarchidae (Witton and Habib 2010, Vermeij 2016).

As well as the groups previously mentioned, dinosaurs raised during the Triassic with the dinosauriform Nyasasaurus parringtoni (Nesbitt et al. 2013). Dinosauria are represented by two major groups, Saurischia on one side and Ornithischia on the other one, even if this bimodal phylogeny have been recently challenged (Baron et al. 2017). Dinosauria developed extreme body morphology such as horns, long necks or shields. Gigantism is usually the main feature that comes to mind about dinosaurs but size increase is not the only process of size modifications observed in this group. Size decrease have been observed in Dinosauria, but in Maniraptora, the group at the origin of birds (Turner et al. 2007,

Bhullar et al 2012), this might have had an influence on the rise of flight capabilities in Tetanurae.

Several specimens of small feathered dinosaurs, such as Microraptor (Xu et al. 2003), Sinornithosaurus

(Xu et al. 1999) or Changyuraptor (Han et al. 2014) have been discovered over the past years, showing morphological adaptations and supporting a possible existence of various flight modalities within dinosaurs, independently of birds. Another important character from dinosaurs, which will be developed later in this thesis is the large variation of teeth shape, in relation to dietary modification and ecology

(Holtz et al. 1998, Abler 1992, Holtz 2003).

Since its discovery in 1856, Archaeopteryx is considered as the most basal bird (Figure I-1), even if this theory have been challenged (Chatterjee S. 1991, Xu et al. 2011). Bird-line is rooted in

Maniraptora (Gauthier 1986, Zhou 2004, Xu et al. 2011). Because of its morphological characteristics,

Archaeopteryx is considered as a transitional form between terrestrial non-avian dinosaurs and modern birds (Ostrom 1975, 1978, Burgers and Chiappe 1991). It as a possible candidate for the origin of avian flight even if its flying capabilities are still debated (Harrison 1976, Olson and Feduccia 1979, Speakman

1993, Voeten et al. 2018).

Figure I-1. Simplified phylogeny of reptilian dataset used in the following studies. Shapes not to scale. As pivotal taxa in the following studies, Archaeopteryx and Halszkaraptor are separated from the group they rely on. (figure on the next page).

Mesozoic, and more particularly Cretaceous have seen the radiation of two major avian clades, namely Enantiornithine and Ornithurae, at the origin of modern taxa. The avian fossil record is particularly well documented in China all along the Cretaceous (Elzanowski 1977, Sereno 1992,

Zhonghe 1995, Sanz et al. 1997, Hou 1999, Kurochkin 1999, Zhang 2001, Zhou 2001, Zhou 2002, Hou et al. 2004, Zhang 2004, Zhou 2005, Zheng et al. 2007, Zhou et al. 2008, O’Connor 2009,Wang 2010,

O’Connor 2011, 2013). Avian ancestors are also known in Europe but only until the mid-Cretaceous

(Nessov and Borkin 1983, Nessov 1992, Kurochkin 1996, Panteleyev 1998, Walker et al. 2007,

Zelenkov and Averianov 2011) and in America during the Early Cretaceous (Brodkorb 1976, Chiappe

1993, Chiappe 1994, Walker et al. 2007, Walker and Dyke 2009). Most of the species of both

Enantiornithine and Ornithurae were considered as potentially good flyers with already various flight modes (Chiappe 1991, 1995, Hou et al. 1996, Zhou et al. 2008, Wang et al. 2011). In addition to these flight modes, those fossils birds were present in different environment, like lacustrine deposits reflecting subtropical environments (Sanz and Buscalioni 1992, Sereno and Rao 1992, Hou 1994, Zhonghe 1995,

Sanz et al. 1996, Zhang et al. 2001), marine deposits ( Molnar 1986, Chiappe et al. 2002), fluvial sediments (Chiappe 1993, Chiappe and Calvo 1994, Brett-Surman and Paul 1995) or deposits representing arid to semi-arid environments (Elzanowski 1977) and presented different diet as shrimps

(Sanz et al. 1996) or amber (Dalla Vecchia and Chiappe 2002) were found in their gastric contents.

Originating from dinosaurian ancestors, birds are, with crocodiles, the other living archosaurian group still existing nowadays. They represent one of the largest group of tetrapods in term of species diversity with almost 10,000 species nowadays (Dyke and van Tuinen 2004), presenting large range of variation for body size, locomotion mode, diet, ecology and behaviour. One of the major aspects of birds evolution is the apparition of flight capabilities. They developed morphological adaptations, mainly on the forelimb, passing from the dromaeosaurian hand to the wing shape allowing flight (Ostrom 1975), feathers (Brown 1963), tail reduction (Gauthier and Padian 1989), and cognitive skills (Alonso et al.

2004) like vision.

I-B-Development of flight within Archosauria

The evolution of flying capabilities is one of the most noticeable innovation that occurred during the evolutionary history of archosaurs. This locomotory behaviour requires particular morphological and cognitive adaptations. One of the structure observed to understand the development of such behaviour is the wing, which is an extreme evolution of the tetrapod hand allowing to form a sail for thrust and bearing going against gravity and air resistance. It is interesting to notice that flight appeared at least twice within archosaurs (birds and pterosaurs) even if it seems to be the consequence of different processes as the organisation of the wing differs greatly between both groups. If in pterosaurs legs and wings are connected together with a patagium, birds have both members decoupled. The shape and organisation of the bones forming the wing also differ greatly as bones play a major role on the elongation of the mechanical structure of the wing in pterosaurs, contrary to birds, in which, feathers also play this role. The main common feature shared by both groups are the influence of the sternum and coracoid in the attachment of the wing muscles.

Assessing the origin of flight within pterosaurs is difficult because of the lack of transitional forms in the fossil records considered as ancestors of pterosaurs. In this case, assessing size variation of pterosaurs and their ancestors around the time when powered flight was developed is difficult, but considering birds, it is suggested that body size reduction from their dinosaurian ancestors (Padian et al.

2001) was one of the process permitting the development of morphologies exapted for flight (Turner et al. 2007).

I-C-Influence of developmental heterochrony within Dinosauria

The transition from terrestrial to flying forms within archosaurian involved a lot of morphological changes within these taxa, but one of the important questions we are facing is how these modification occurred and which mechanisms were involved in such particular morphologies.

This topic, as well as most of the evolutionary questions, have usually been studied through the classical neodarwinian point of view, considering natural selection and genetics, involving mutations and their transmission to their offsprings. And example of such mechanisms recently developed is the influence of growth rate modifications of body parts during ontogeny being considered as influencing on the modifications of the body bauplan (Gould 1977, McKinney and McNamara 1991).

These changes in the development period, speed and duration of a taxa are known as heterochrony, and can play significant role in modifications of size and/or shape of an organ, depending on the increase or decrease of the normal development time. It can be seen as two main ways: peramophosis

(predisplacement, hypermorphosis and acceleration extend development) and paedomorphosis

(postdisplacement, hypomorphosis and deceleration shorten development). The concept that will be developed more extensively in the following chapters and articles of this thesis is paedomorphosis, based on previous research that considered paedomorphosis as a driver of the transition between dinosaurs and birds (Bhullar et al. 2012, Lee et al. 2014). Paedomorphosis is devided into two different modalities: neoteny or progenesis. Neoteny refers to the retention of ancestral juvenile traits in adult forms of same size by delaying the development. On the contrary progenesis is a reduction of developmental timing leading to adult looking like their ancestral juvenile states at a lower size.

It is commonly considered that these developmental process explain variation along the evolutionary history of taxa. One of the well-known example is the influence of paedomorphosis and peramorphosis in the human lineage, leading change in body shape from chimpanzee ancestors to modern human bauplan (Gould 1977). Another well known example is the development of the axolotl

Ambystoma mexicanum (Tompkins 1978). Those changes influenced modification of skull shape (Shea

1989, Penin et al. 2002) and brain encephalisation (Montagu 1955, Gould 1977, Langer 2006).

Heterochrony seems to have also been an evolutionary force driving the evolution of skull shape of

Diapsids, and as such have influenced the early stages of Archosauriforms evolution (Ezcurra and Butler

2015). Recent study have considered that the evolution of dinosaurian skull was the consequence of a succession of both peramorphic and paedomorphic events (Foth et al. 2015, McNamara and Long 2012), leading to snout elongation and braincase rearrangement. These paedomorphic events, in addition with

15 the size miniaturisation observed at the origin of avialan lineage (Lee et al. 2014), influenced the evolution of avian skull characteristics and its evolution within Theropoda (Bhullar et al. 2012, 2016).

II-Paleoneuroanatomy

II-A-Brain organisation

In vertebrates, brain is a structure surrounded by the braincase and having a role of reception of inputs from the environments, treatment of this information and elaboration of the appropriate response.

This structure is organised in different areas which have their own role in perception of the environment and the answer to give. At this point, it is necessary to precise that all the structures that will be presented in the following part of this chapter are found in all vertebrates and almost all chordates. Shape and size variation of brain anatomy can reflect behaviour, cognitive capabilities and evolutionary history of a group (Sol et al. 2005, Sol et al. 2007, Sol et al. 2010, Kawabe et al. 2013, Fuchs et al. 2014).

Neurocranium and brain anatomy are described as deeply linked together as the first one is surrounding and protecting the second, changes in the organisation of one influence changes in the other (Fabbri et al. 2017). Brain volume seems to be related to rates of anatomical evolution (Wyles et al. 1983). Brain drives behaviour, but it seems that some particular behaviours and the environment influence brain shape and size. These changes, like those related to temporary social interactions, like migration or courtship display tend to be reversible (Fernald 2003, Barnea 2009), which is not the case for age dependant mass variation (Graber and Graber 1965). Sexual dimorphism does not seem to influence changes on brain volume or shape (Guay and Iwaniuk 2008). If phylogeny can have a little impact on cerebrotypes variations, it seems that ecology have the main effect (Garamszegi et al. 2002, Iwaniuk and Hurd 2005) as species from the same clade shows large variability of endocranial shapes (Smith and Clarke 2012).

Development and the complexity of brain regions are mainly depending on the behaviours controlled by these cerebral areas (Madden 2001), divided into sensorial and motor regions (Ferrier 1874). The independent study of the different cerebral structures does not tend to be an efficient proxy for

16 understanding evolution of cognition within vertebrates as areas controlling primitive behaviour have nothing to do with cognitive abilities (van Horik et al. 2012). As such, brain shape tend to reflect cognitive capabilities and evolutionary history of the clade (Kawabe et al. 2013). The shape of the adult brain also tend to depend from the embryologic development and reproduction mode of the taxa (Martin

1981), which tend to suggest that differences in ontogeny timing influence brain organisation.

Vertebrates developed limited amount of different brain structure along their evolution. Most of the structure observed in archosaurian were already existing in early vertebrates such as hagfish and lampreys (Nishikawa 1997). Some structure, considered as homologuous at first sight, have appeared independently several times. During brain evolution, it seems that there were few major changes but a succession of small innovations with preservation of basic characteristics. These changes can be linked with metabolic changes within taxa as the increase of brain size is a process that requires important energetic resources for both size increase and functioning of the developed structures (Safi et al. 2005).

The most anterior part of the brain is the prosencephalon, forming the forebrain in association with the diencephalon, and divided in two hemispheres (Figure I-2), acting in data acquisition related with threat involving vision, influencing threat evaluation and appropriate motor and physiological response (Turner 1892). The forebrain is formed by the assemblage of the two brain hemispheres

(telencephalon), olfactory bulbs and tracts (nerve I or olfactory nerve), and hippocampus. Most of variations in brain shape seem to be related to modification for the forebrain (Fuchs et al. 2014), mainly related with changes in the telencephalon (Kawabe et al. 2013) as it is an important structure in the changes of cognitive capabilities (Iwaniuk et al. 2005). Relative size ratio of the telencephalon versus complete brain volume varies a lot between birds (more than 50%), Archaeopteryx (45%) and dinosaurs

(25%) (Burish et al. 2004). Shape variability of the telencephalon seem to be linked to diversity of functional specialisation and to the increase of brain complexification within groups (Nieuwenhuys et al. 1998).

As well as in human (, Davidson and Hugdahl 1996, Toga and Thompson 2003), there is an asymmetry in cerebral function between left and right hemispheres in birds (Wiltschko and Wiltschko

2007) reflecting different roles. The left hemisphere separates distracting from relevant stimulis while right hemisphere controls fear and reaction against a threat (Rogers 2008, Rogers 2012). The left hemisphere tend to be important in migratory groups as it possibly have magnetoreceptive properties, used for geolocalisation (Wiltschko and Wiltschko 2007). Telencephalon have experienced a mosaic evolution depending on cognitive requirements in different species. Enlargement of specific but similar brain areas in Psittaciformes, Passeriformes and Corvidae tend to express high cognitive levels (Corfield

2008, Corfield et al. 2012). The telencephalon is divided in several subregion, which have their own and independent functions like integration of general information (Nieuwenhuys et al. 1998), magnetic receptors related to orientation (Mouritsen et al. 2005), learning of motor (Moreno et al. 2009, Milner and Walsh 2009) and dietary behaviours (Corfield et al. 2012) and integration of information based on visual stimuli (Butler and Cotterill 2013, Fuchs et al. 2014).

One of the telencephalic structure showing the highest shape variability is the wulst, located on the top of the cerebral hemisphere. Its size, shape and position vary a lot within modern birds. This structures plays an important role in vision, mainly in nocturnal and migratory taxa (Mouritsen et al.

2005). It organises the somatosensorial answers and the excitability of visual units located in the optic tectum. As such wulst size does not only reflects visual information but also motors and somatosensorial abilities (Iwaniuk et al. 2008). It could also possibly moderate the inhibition of path between the different telencephalic layers and influence learning (Nieuwenhuys et al. 1998). The role of the wulst is also important in the way how the animal can perceive movements. It receives informations from the thalamus about large sized and/or fast speed objects, considering the animal own movements but also the movements coming from its environment (Baron et al. 2007). Species migrating over long distances tend to have a more developed wulst than those migrating on shorter distances (Fuchs et al. 2014).

Neurones present in the wulst are highly sensitive to variations of the binoculary field of view

(Harmening 2011), which is unique among the other forebrain structures. The size of the wulst is correlated with eyes orientation and the angular aperture of the binoculary field of view. Species with

18 large binocular field of view and eyes placed on the front of the head tend to have bigger wulst. Wulst is related to eye position but not to eye size (Nieuwenhuys et al. 1998). The wulst got enlarged during modern birds evolution (Jerison 2007). If it is clearly absent in Ornithurae (Walsh et al. 2015), its presence have been proposed in Archaeopteryx, but the results presented in this PhD demonstrate that wulst was absent in this species contrary to what some previous studies suggested (Balanoff et al. 2013).

The olfactory tracts and lobes are located on the most anterior part of the telencephalon. It is generally admitted that vision and the role of vestibular system replaced olfaction through archosaurian evolution, with similar olfactory ratio between non-avian dinosaur and Archaeopteryx, slightly higher than in modern birds (Zelenitsky et al. 2009). This transition between olfactory based to vision based behaviour is already visible in Mesozoic birds such as Hesperornis (Zelenitsky et al. 2011), which is already considered as a complex flyer.

The other part forming the forebrain is the diencephalon (Figure I-2), sending information to the cerebral cortex in relation with autonomous controls. It is very differentiated in birds, with sensorial centers occupying a large part of the diencephalon. The border with mesencephalon is unclear

(Nieuwenhuys et al. 1998). The pineal glande, on the top of the brain and posterior to the cerebral hemispheres, contains neurones involved in melatonine regulation depending on luminosity as well as visual information (Nieuwenhuys et al. 1998). It also control the circadian cycle and maybe act as a photoreceptor (Menaker and Zimmerman 1976, Milner and Walsh 2009,). The thalamus present elements related to magnetic reception aiming for orientation. It controls ascendant sensorial system, influencing visual, auditory and somatosensorial centers, helping for movement perception from the environment but also for colour vision (Nieuwenhuys et al. 1998). In this cerebral area, biological rhythm and growth rate, an important factor in the transition of bauplan in archosaurs, are controlled by the pituitary gland. In relation with sensorial informations, hypothalamus initiate defensive behaviour when stimulated (Akerman 1965). The nerve II (optic nerve) and the optic tract are also part of the diencephalon. Their role is to transmit visual stimuli and to innerve the eye. It is considered being the most developed nerve in birds (Turner 1892) which is congruent with the high visual abilities required by flight. It is well developed in falconiformes and less in nocturnal birds (Orosz et al. 2007).

The midbrain, or mesencephalon, is located postero-ventrally compared to the forebrain (Figure

I-2). Its role is to integrate motor behaviour in relation with auditive and visual information, general reflex system, and to make the relation between hindbrain and forebrain. This cerebral area is well developed in birds because of their higher visual requirements (Cobb 1963). The optic tectum is a very important structure for controlling movements in flight (Ferrier 1874) by creating an auditory and visual map based on those movements (DuLac and Knudsen 1991) but also including visual and auditory information from potential threats (Symonds et al. 2013). These maps contain information of movements orientation, size and eye direction. Both maps are aligned, visual map being necessary for calibrating the auditory map (Knudsen and Brainard 1991). This requires visual experience and the movements controlled by this structure change depending on species. The optic tectum contain a precise map of movements orientation, size and eye direction. This visual map is well aligned with the auditory map (Knudsen 1988, duLac and Knudsen 1991, Knudsen and Brainard 1991). As well as the visual map, the auditory map can be modified by learning and experience, but always in order to maintain sensorial modalities (Knudsen 1983). This relation relation between visual and auditory maps helps increasing objects location in the environment of the individual (Kaas and Hackett 2000). Visual experiences maintain or modify, if necessary, the perception of the signal and the associated movement depending on the initial stimuli (Dulac and Knudsen 1991). It is also linked the alarm calls of songbirds (Brown

1965, Brown 1971). Vision and perception plays a role in data acquisition related to threat. Species with well-developed visual system use to have a more developed optic tectum (Symonds et al. 2013). After acquiring environmental information, signals are sent to specific parts of the forebrain. Contrary to the wulst, the optic tectum detects low speed and small sized objects. It also reacts to localisation and identification stimuli. If information coming from the eyes are important in the performance of the tectum, its size does not seem to be related with the position of orbits or angle of the binoculary field of view (Iwaniuk et al. 2008). The optic tectum contains two kind of cells, isthmo-optic nucleus (ION) and ectopic isthmo-optic nucleus (EION). ION are much more developed in frugivorous birds than in birds of prey, suggesting that these cells are linked with the research of static food. The tecto-fugal system plays role in colour recognition and pupil dilatation (Orosz et al. 2007). The midbrain also present nerves

III (oculomotor nerve) and IV (trochlear nerve). The oculomotor nerve affect de vertical movement of

20 the eye. Can emerge from the brain from an oculomotor foramen or as a branch of nerves V or VI

(Turner 1892). The trochlear nerve controls the oblique dorsal muscle of the eye (Turner 1892, Orosz et al. 2007).

The last cerebral component is the rhombencephalon (hindbrain) (Figure I-2). This structure is divided into two parts. The most anterior part is the metencephalon. The major part forming the metencephalon is made from the cerebellum, which consist in a mass of white matter covert by cortical matter. Large animals tend to have a relatively larger cerebellum than smaller species. A small cerebellum is observed in owls, which can be explained by the fact that nocturnal birds use more their vestibulocochlear system than their vision for hunting compare to other groups of birds (Sultan and

Glickstein 2007). It is even smaller in secondarily flightless birds (Iwaniuk et al. 2004). This structure is related with visual, auditory, somatosensorial and vestibular systems, as it carries the flocculi, which are deeply related to the semicircular canals (Goodman 1964). It also plays a role in the positioning of movements and muscular response (Turner 1892). It is interesting to notice that even if modern birds and derived pterosaurs share a common brain shape, the flocculus is larger in pterosaurs than in birds, which could suggest an integration of sensorial informations from the wing (Witmer et al. 2004). The cerebellum plays a role in the data acquisition from threat from visual and auditory sources but also in the physiologic and motor response to those stimuli (Symonds et al. 2013). The enlargement of cerebellum would also be linked with beak control and an increase of visual control allowing the use of tools, as well as motor learning (Sultan and Glickstein 2007). The cerebellum is the only foliated structure in bird brain. The degree of foliation varies a lot between avian taxa. It seems that the degree of foliation is correlated with growth strategy as well as with body, brain and cerebellum size. Cerebellar size looks to be less influent in the degree of foliation than body size. Phylogenetic effect cannot be neglected as some groups seem to present more cerebellar foliation than others, closely related phylogenetic taxa tend to present similar levels of foliation. Behaviours and cognitive abilities tend to also play a role on the cerebellar foliation. Some behaviours related to high biomechanical constraints tend to have a lower level of foliation, as these constraints are limiting possibilities within the endocranial cavity. This increase of the cerebellar surface can help improving the previously mentioned

21 use of tools and other cognitive skills, as well as motor learning, coordination, sensory integration

(Iwaniuk et al. 2006). Considering the fact that the cerebellum is in relation with the semicircular canals as it is carrying the flocculus and based on its role in controlling and coordinating movements, foliation can be a proxy for estimating agility (Paulin 1993).

Placed on both side of the cerebellum, flocculi, integrate sensory information concerning head rotation and stabilisation of the vision. Their size are not linked with flight capabilities (Walsh et al.

2013). The rhombencephalon present a large variety of cranial nerves. The nerve V (trigeminal nerve) is used as a sensory path for tactiles organs of the beak and the head, dermis, eyelid, palate and nasal cavity (Orosz et al. 2007). Nerve VI (abducens nerve) controls external musculature of the eye (Turner

1892, Orosz et al. 2007). The nerve VII (facial nerve) essentially innervate glands and muscle of the middle ear, receiving sensory information from the nasal cavity, palate and tympanic membrane. Nerve

VIII (vestibulocochlear nerve) aim to transmit balance and auditory information. It is sending information about body position in the space from the semicircular canal input. Groups low auditory acuity compensate with head movements (Orosz et al. 2007).

The second part that form the hindbrain is the myelencephalon. The main part is the medulla oblongata, which is the physical link between the brain and the spinal chord. It plays a role in physiological and motor response when facing a threat. The medulla does not look to reflect any phylogenetic signal (Symonds et al. 2013). Nerve IX (glossopharyngeal nerve) is related to the tongue and control several glands, the pharynx, oesophagus and trachea. Nerve X (vague nerve) is linked with the digestive tract as well as nerve XII (hypoglossal nerve). Nerve XI (accessory nerve) irrigate the upper part of the body (Nieuwenhuys et al. 1998).

Figure I-2. Cerebral organisation and position of the different brain areas in the flycatcher

Ficedula albicollis. The brain is presented in anterior (A), posterior (B), lateral (C), dorsal (D) and ventral (E) views. The brain is subdivided in 3 major areas, the forebrain with the association between the telencephalon/cerebrum (orange) and the diencephalon (purple), the midbrain formed by the optic tectum (red) and the rhombencephalon, subdivided into the cerebellum (yellow) and the medulla oblongata (green). Arrows address the position of specific endocranial structures, wulst (W) and flocculus (Fl). Scale bar: 1.5mm.

II-B-History of paleoneuroanatomy

Considering its deep relation with behaviour, brain anatomy is an important topic to study for understanding the life style of extinct species. As it is nearly impossible to access and study all brain anatomy of all taxa of a group, considering the lack of sufficiently well preserved specimen for some of the taxa, the visualisation of the process leading from a brain shape to another can be difficult. This lack of information raise some important questions defined by Northcutt (2011). The first question is which changes in brain organisation and function have occurred along the evolution of the group. It refers to shape and size of structures happening during evolution and the consequences in term of behaviour. The second question rising is when these changes occurred. It can refers to precise dating of modifications within phylogeny but also mean relative dating comparing taxa. Another question are the processes and mechanisms behind these changes. Developmental heterochrony and other mechanisms can lead to changes in body shape and behaviours. The last question has been formulated as “Why did these changes occur?”. This formulation can be problematic, considering that this way to express could mean that the changes that occurred were made aiming their consequences. Considering possible exaptation, as an example, changes happened and were then had an influence in behavioural modifications.

Fresh brains of extant taxa can be relatively easily accessible, from museum collections or from dead corpses, it is more problematic when dealing with fossils. Except in extremely exceptional occasions, brains are not getting preserved during taphonomic processes (Pradel et al. 2009), which can also be generalised to soft tissues (Maldanis et al. 2016). In order to make possible the characterisation of cerebral anatomy of extinct taxa, the study of endocast appears as the only possible solution, as it accessible in both extant and extinct groups. The main issue is the representativity of endocast shape compared to the real brain one. If for birds endocast and brain are very similar (Iwaniuk et al. 2002,

Chapter II), the brain of crocodiles only fills about 50 % of their endocranial cavity (Hurlburt 1994,

Jirák and Janáček 2017), with significant distance between the brain surface and the surrounding braincase, which does make the endocranial cavity not accurate for studying brain shape. Concerning pterosaurs, the infilling ratio tend to be close to what is observed in birds (Witmer et al. 2003) contrary

24 to most dinosaurs which are closer to crocodiles for the neuroanatomical aspects (Hurlburt 1994).

Solutions are actually studied for reconstructing brain shape based on endocranial shape in dinosaurs

(Morhardt et al. 2012).

If the first endocranial description have been realised by Owen (1842) on the thalattosuchian

Steneosaurus, and in the addition of previous work of biologist, describing brain anatomy of extant species, the start of paleoneuroanatomy was leaded by Tilly Eidinger in the early 20th century, first on

Nothosaurus (Eidinger 1921) and then Archaeopteryx (Eidinger 1926), Pterodactylus (Eidinger 1941) and a large amount of mammalian groups, with a focus on Equidae (Eidinger 1948, 1950). These research on fossil endocast anatomy were complemented with studies of the brains of extant species, in order to understand how brain was working, to which function each cerebral structures were dedicated and for defining the physical and functional relationships between these areas (Ferrier 1874, Turner

1892, Cajal 1909, Papez 1937, Beach 1951, Rensch 1956).

First observations of endocast were realized using natural (when the endocast is naturally visible out of the braincase) or artificial endocast (the cerebral cavity is filled with a preparation that is extracted from the skull after a while) (Hopson 1979, Hurlburt 1994) or by serial sections (Figure I-3), which requires the destruction of the specimen. Physical serial sections are based on the serial slicing/ griding of the real specimen, for drawing the structure at each step and then reproducing every slice as a wax model, which lead to the destruction of the specimen and the impossibility to repeat any new studies of it. If this last methods is not a big issue for modern specimen for which new skulls can be easily accessible, it is much more problematic for fossils, as for most of them, there are only a few specimens available and so destructing the sample is not an option. This problem has been solved for most of the cases during the last decades with the use of computerised tomography (CT) (Conroy and Vannier 1984), in order to access internal anatomy of objects without any damages. These computing methods are basically using the same concepts as the serial sections except that the slices realised are virtual and the specimen is not destroyed, which allow repetition of observations for later investigation.

Endocranial cast of archosaurian are quite well known in general. The structure of the brain itself in crocodilians is less well known compare to research focusing on bird neuroanatomy. Despite

25 this, the role of the brain based on endocranial shape, like inferences in communication (Vergne et al.

2009), nerve organisation (George and Holliday 2013), ontogenetic studies (Dufeau and Witmer 2015) is quite well understood. Studies focusing on the brain organisation or the endocast/brain relationship are not very common (Janáček et al. 2017). The endocast of extinct crocodilians (Storrs et al. 1983,

Brusatte et al. 2016) or relatives (Gower and Sennikov 1996, Martinelli and Pais 2008, Holloway 2011,

Nesbitt 2015, Pierce et al. 2016, von Baczko and Desojo 2016) is also quite well known.

Dinosaurian endocranial anatomy is one of the most well studied within archosaurs. As for other extinct taxa, and even if some preliminary studies have been realised on preserved or extracted endocast

(Zheng 1996, Alifanov 2011),the rise of virtual imaging technics helped developing this field and increasing the amount of information available for understanding their endocranial anatomy and its consequencies. One of the main topic discussed in these studies is the relationship between endocranial organisation and the taxonomical information provided by such structure (Zheng 1996, Balanoff 2011,

Knoll et al. 2012). While understanding more the diversity of endocast within dinosaurs, some behavioural questions were starting to be adressed, like the head posture, influencing body position and dietary behaviour (Sereno et al. 2007). The influence of some structures over the others was adressed, like the large olfactory bulbs in tyrannosauroid (Brochu 2001) and the consequences on their hunting behaviour (Witmer and Ridgely 2009). The misinterpretation of the position of some cerebral structures led to erroneous conclusion, like for the optic tectum mingled with the lateral expansion of the telencephalon. Although real brain remains are not preserved, visualisation of cerebral tissues, in addition with visibility of the border between brain structures, can be observed in exceptional cases in the fossil record, helping to assess the representativity of the endocast compared to the real brain shape in dinosaurs, like evidence for vascularisation (Osmolska 2004, Evans 2005) and soft tissues surrounding the brain as meninge (Brasier et al. 2016).

Contrary to the endocranial anatomy and diversity of dinosaurs and other earlier archosaurs which are pretty well known, the cerebral anatomy of extinct birds, due to the fragility of their skeleton which causes a lack of 3D preserved specimen, is poorly known (Alonso 2004, Zelenitsky et al. 2011,

Walsh et al. 2015). It is necessary to extract the maximum information from the few specimen available.

As well as for birds, Pterosaurian neuroanatomy is still not very well known due to the very limited number of studies (Eidinger 1941, Witmer et al. 2003, Cordoniú et al. 2016) despite the important of specimen with skulls preserved in three dimensions.

II-C-Review of brain anatomy in bird-line through the evolution of flight

Another important topic in the study of brain evolution within Dinosauria is the transition from the ancestral crocodile-like brain observed in most of the dinosaurs, and the brain shape allowing cognitive flight skills, as in modern birds. Changes in skull shape and organisation (Fabbri et al. 2017) based on paedomorphic events through the archosaurian groups (Bhullar et al. 2012, Lee et al. 2014) might have influenced cerebral organisation, allowing for changes in cognitive abilities within given parts of the clade, like taxa that developed flying capabilities.

Even if the brain is not available in extinct taxa, which does not allow precise definition of the shape and inner borders between the cerebral structures, studies based on endocranial shape highlighted some behavioural signal in modern birds. The endocast of Charadriiformes tend to reflect their locomotory behaviour depending on the head position (Smith and Clarke 2012), relative brain size can be a signal for developmental strategy (Portmann 1946, Iwaniuk and Nelson 2003), variation of telencephalic volumes might be an indicator of social complexity (Burish 2004), evidence for

“intelligence” like for food storaging (Krebs et al. 1996), using of tools (Lefebvre 2002, Lefebvre 2013) or other learnings requirements (Rensch 1956, Reiner et al. 2008) or other intelligence evidence (Emery

2006). Brain size also reflect adaptations abilities to the environment itself (Moller and Eritzoe 2015) or to the other taxa living in the same environment (Moller and Eritzoe 2014) for resident species or migratory groups (Pravosudov et al. 2007). Like in parrots, it does seem that the phylogenetic signal of brain shape is relatively limited, which let think that endocranial studies are quite accurate for defining behavioural pattern in brain shape (Carrill et al. 2015). Considering vision as an important tool for

27 dealing with the environment of a flying animal, it sounds to be logical to consider that visual abilities, reflected by orbital size position and shape, can also influence brain organisation (Kawabe et al. 2013).

If the phylogenetic relationships between crocodiles and birds is generally accepted, there are a few evidences of the processes leading from the reptilian brain of crocodile to the complex and encephalised bird brain. A mosaic evolution tend to be at the origin of the modern brain shape (Iwaniuk et al. 2004) but the complete process and the different steps that happened between the crocodilian brain and the bird brain are poorly known. Recently, and on the addition of the studies realised on the skull anatomy (Bhullar et al. 2012), it has been suggested that ontogeny was playing an important tribute to the modifications occurring in the cerebral organisation in birds (Kawabe et al. 2015), and that differences in developmental strategies were reflecting some differences in cerebral structures (Nealen and Ricklefs 2001). This evolution and changes in brain anatomy through Craniates evolution seem to have unlock difference possibilities for more advanced behaviour at several steps of the changes

(Nishikawa 1997), which can reflect the same kind of event within archosaurs.

Due to the lack of well-preserved endocast for extinct birds and relatives, it is quite difficult to make observation on the endocranial shape and to assess the behaviour of extinct taxa. Although several

Archaeopteryx specimen were found, only the London specimen so far (because it present the most complete and the less distorted endocast) has been used for studying the endocranial morphology of the taxa considered as the most primitive ancestor of birds. It is crucial to have the opportunity to study these specimens of early birds as some authors considered that it was the earliest steps of the avian evolution were most of the brain shape and size modifications occurred (Sol et al. 2007). The endocast of the London archaeopteryx have been described as looking like really closely to what is observed in modern birds, based on the visibility of brain structures, the antero-posterior rotation of the optic tectum, the relative brain volume over body size, which make Archaeopteryx having one of the bigger brain in archosaurs, makes it closer to bird than to more primitive reptiles. These observations suggested that the brain of Archaeopteryx was already adapted for flight (Jerison 1968, Alonso et al. 2003, Witmer 2004,

Balanoff et al. 2013), and in addition with its morphological features, like arm transformed in wings

(Burgers and Chiappe 1991) and the presence of feathers (Norberg 1995, Christiansen and Bonde 2004,

Dyke 2010, Nudds and Dyke 2010, Foth et al. 2014) in some specimens, made the interpretation of evolved flight congruent for this taxa (Heptonstall 1970, Cox 1974, Harrison 1976, Ebel 1996, Long et al. 2003, Meseguer et al. 2012, Voeten et al. 2018).

Due to the lack of brain fossilised or the few specimen presenting a well preserved 3D shape of the skull, observations on extinct Mesozoic birds is difficult. Luckily, as for modern birds, their endocast represent accurately the morphology of their brain (Iwaniuk and Nelson 2002) which make any well- preserved specimen very valuable and informative for the understanding of brain evolution in this group.

Some Cretaceous birds are exquisitely preserved for allowing such observation on their brain morphology, like Enaliornis barretti (Elzanowski and Galton 1991) and Cerebavis cenomanica (Walsh et al. 2015). The endocranial anatomy of Hesperornis regalis and Ichtyornis dispar are not directly accessible but have been inferred from their skull shape (Eidinger 1951, Marsh 1880). All those specimens share cerebral shape closer to modern birds than to Archaeopteryx, but are apparently lacking the wulst.

In modern birds, endocranial anatomy, shape and organisation tend to be an important proxy for explaining directly behaviours (Smith and Clarke 2012, Carrill et al. 2015) or in coevolution with other structures also related to environmental stimuli like orbit size (Kawabe et al. 2013). Other studies concerning endocranial organization have been conducted over archosaurs with brain volume over evolution of body size (Alonso et al. 2004, Balanoff et al. 2013) suggesting that flight was not the only driving force of cerebral modifications but that the process leading to modern avian brain was much more complex than previously expected (Balanoff et al. 2016).

Figure I-3. Evolution of methodologies for reconstructing and visualising 3D shape of fossils. A)

Grinding machine used as the first paleontological tomographic studies, B) Wax model of the reconstruction of the early vertebrate Palaeospondylus (A-B modified from Sollas 1904, Cunningham et al. 2014), C) Graphic representation of grinding slices of Cephalaspis, D) Reconstruction of Cephalaspis in dorsal view, E) Reconstruction of Cephalaspis in lateral view (modified from Stensiö 1927), F-G)

Endocranial reconstruction of Tyrannosaurus rex ( © Robert Jones, Australian Museum and Matt

Martyniuk), H) Virtual reconstruction of Tyrannosaurus rex (modified from Witmer and Ridgely 2009), I)

Outer surface of the endocast of the London specimen of Archaeopteryx, J) Virtual reconstruction of the

3D shape of the London Archaeopteryx visualised by CT scan (I-J Alonso et al. 2004), K) Virtual reconstruction of the 3D shape of the London Archaeopteryx visualised by propagation phase contrast X- ray synchrotron microtomography.

Chapter II Bi-energy imaging of Neuroanatomical features

I-Generalities and history of imaging methods

Accessing internal anatomy of biological specimens have always been an important problem to face for scientists. External anatomy provides a large amount of information about morphology and allows for inferring about lifestyle and evolution but only represents a part of all the information that can be available from a specimen. The more details we can observe on a specimen, the most accurate will be the conclusion about all the questions we can ask about this specimen. Physical access to internal anatomy is not an easy path. It requires a lot of caution to avoid any damage during the manipulation, preservation and extraction of the structure of interest. The development of imaging techniques permits observation of inner characteristics of a specimen with reducing the risk of damages. These methods also enable to observe higher level of details. Improvements of visualisation techniques helped to increase the quality of observation and our understanding of biological organisms.

The origin of these visualisation methods takes place during the 19th century, when Röntgen noticed that when X-rays comes through an object with differential composition, it was possible to acquire differential transmission of the X-rays depending on the density of the different components of the object and inform on the internal properties of a sample. The first use of the methods based on differential contrast was on medical purpose, observing internal anatomy of individuals and highlighting any issue inside the body of a person. A limitation of clinical radiography is that observation are limited to 2D projections, which can hide some details if the problem occurs in the projection axis of other structures. This problem started to be tackled with the development of X-ray computerized tomography

(CT). The use of CT is nowadays the golden standard for non-destructive study of the internal structures of large biological samples (Hounsfield 1973). CT gives very good reconstructions of mineralised tissues (teeth, bones...) but possesses low contrast for soft tissues imaging (Chen et al. 2012). The low contrast of X-ray images of soft tissues can be enhanced by contrast agent administration on dead specimens. If carefully selected and applied, the contrast agent can induce density contrast among the different tissues of interest; however, contrast enhancement is not always sufficient and the use of advanced imaging techniques and processing are needed for further enhancement of the contrast or semi- automatic selection of these structures. One of the possible solutions for sufficient contrast enhancement

33 of internal structures on X-ray images needed for precise segmentation could be implementation of bi- energy imaging using contrast agent combined with the high sensitivity of propagation phase contrast based methods. On the contrary, MR imaging protocols are providing optimal contrast of soft tissues but low contrast for mineralised tissues.

II-Use of contrast agent and bi-energy scans

Basically, an organism contains two kinds of tissues that can be visualised, mineralised and soft tissues. Mineralised tissues, such as bones and teeth, can be easily visualised using X-ray based techniques thanks to their high density compared to soft tissues. A main issue for imaging soft tissue is the low contrast difference between the different tissue, especially when mineralised tissues are imaged at the same time. This requires to develop specific techniques in order to enhance the contrast between these structures.

One of the solution is the use of contrast agent that increase the density of selected soft tissues to increase their visibility (Wallingford 1953, Harris et al. 1979). Osmium tetraoxyde is used for fixation on cell membrane as well as on lipid rich structures such as nerves (Metscher 2009), phosphotungstic acid (PTA) is fixed on proteins like collagen and other connective tissues (Hayat 1970, Kiernan 1990) where some iodine-based contrast agent are binding on lipids (Gignac and Kley 2014). PTA as also been described as a good discriminant for separating tissues and organs (Descamps et al. 2014), despite the fact that it is an acid which can cause decalcification.

The methods described hereafter are based on the use of sodium polytungstate (NaWO3) as contrast agent. They benefit from the differential absorption depending on energy and the K-edge of the element selected as contrast agent (tungsten in the present case). The k-edge subtraction technique is based on the fact that there is discontinuity in the linear attenuation coefficient of photons with energy just above the binding energy of the K shell electron of the atoms, which interact with the photons

(Kruger et al. 1977, Zentai 2009); the discontinuous increase in attenuation of these photons is due to photoelectric effect. An abrupt increase of the X-rays absorption by the contrast agent within the sample

34 occurs when X-ray photons of energy just above this K-edge interact with the tungsten (Roessl and

Proksa 2007). The principle of K-edge subtraction consists then into capturing a picture at two different energies, below and above the K-edge of the element to be isolated. The k-edge subtraction technique has been used for many years, in the medical field including angiography (Rubenstein et al. 1987,

Fukagawa et al. 1989, Schultke et al. 2005), mammography, or detection of cancerous tumours

(Bornefalk et al. 2006). In K-edge subtraction the two selected energies have to be as close as possible of the K-edge. Nevertheless, when using high Z contrast agent, bi-energy with much more different energies (one below the K-edge, and one clearly above it) can also be used with very similar results, thanks to slightly different calculations during the processing of the data.

For the experiment described later we selected below K-edge energy at 68 KeV and 70 KeV or

123 KeV for above K-edge energies (for respectively K-edge subtraction and bi-energy imaging).

Sodium polytungstate have been mainly used as a contrast agent in hydrology (Nakashima 2013) but also on biological samples (Jirák et al. 2015). This method provides differential absorption of the biological material and the contrast agent between the two energies and depending on marked tissues, which allow good separation of tissues within a biological sample. The contrast agent concentration in the staining solution was set at 50g/L. The contrast agent is spread through the sample by passive diffusion, which last depending on the size and permability of the external teguments of the specimen, from a few hours for small specimens such as crocodile embryos, to almost a year for the largest one such as complete ostrich head.

After acquiring the two scans and having reconstructed the corresponding volumes, they are combined mathematically in order to automatically detect the presence of the contrast agent to separate the different kind of tissues. Depending on the energy, absorption varies a lot between soft tissues, hard structures and other kind of tissues. The first combination of energy is the association 68-70 KeV (Figure

II-1). Both energy are really close to the K-edge jump of tungsten. In this conditions, absorption for non- tungsten marked tissues does not vary between the two energies, the absorption only varies for structures on which the tungsten have been fixed. The subtraction of these two images gives a mapping of tungsten deposition on the tissues of the specimen. This method refers to the classical K-edge subtraction (Figure

II-3). The other combination of energies, known as a bi-energy imaging method, is still using the same below K-edge energy value, but the above energy is not taken right after the K-edge for having absorption differences but at the same absorption level than the below K-edge energy for the contrast agent, which justify the use of a picture realised at 123 KeV (Figure II-2). For this two pictures, tissues marked with sodium polytugnstate have the same absorption even if it is at different energies. The difference happens in non-marked tissues which show different absorption, which create an inverse map of the k-edge imaging methods previously described (Figure II-3).

Figure II-1. K-edge imaging absorption versus energy relationship. Images were taken at 68 and 70

KeV. W1 and W2 represent absorption values at the different energies for sodium polytungstate marked specimen, A1/A2 and B1/B2 represent absorption respectively for tissue 1 and 2 at the same energies.

Figure II-2. Equivalent absorption imaging absorption versus energy relationship. Images were taken at 68 and 123 KeV. W1 and W2 represent absorption values at the different energies for sodium polytungstate marked specimen, A1/A2 and B1/B2 represent absorption respectively for tissue 1 and 2 at the same energies. Purple line represents absorption level between the two energies.

One of the main problems which we faced concerns the homogeneous dissemination of the contrast agent. Diffusion in the sample is slow at macroscopic scale and required time for efficient contrast agent penetration. This time varies with the size of the specimen and its overall surface permeability. If the contrast agent is not present in sufficient concentration for a long period, it is impossible to separate the cerebral structures. The use of K-edge or bi energy imaging techniques based only on absorption contrast also has a limitation in overall picture quality, because of a low signal to noise ratio, which limit the resolution of borders between structures and does not reveal the small ones.

Considering MR imaging protocol, the addition of sodium polytungstate as a contrast agent did not impair the quality of MR image. Some brain structures, based on visual inspection, are better visualized after using this contrast agent.

Figure II-3. Differential contrasts of skull structures at different energies on the head of Phasianus colchicus. Each horizontal pair of pictures represent energy associated with each scanning methods, K- edge with 69 KeV (a) and 70 KeV (b), showing contrast equivalence of bones, bi-energy with 69 KeV

III-Propagation phase contrast

Propagation phase contrast, as the other computed tomography techniques, relies on variation of the transmitted beam through the sample (Snigirev et al. 1995, Cloetens et al. 1996). Whereas conventional scanning techniques are based on attenuation of the transmitted beam by absorption of photons into the sample, propagation phase contrast relies on interference based on differences in phase caused by differences of density inside the sample. This interference pattern is related to distortion of the wave front geometry due to phase boundaries between two materials within the object. This differential refraction at the media fringes can highlight internal structures in the sample. The increase of propagation distance reveals finer phase shifts until a limit at which single phase fringes typical of the edge detection regime start to be become multiple fringes typical of the holographic regime. The optimal distance between the sample and the detector depends on the detector resolution, on the energy used during the scanning experiment, and on the coherence level of the beam used to perform the experiment. Propagation Phase contrast μCT has become the golden standard for synchrotron imaging in paleontology (Tafforeau et al. 2006), for instance for separation of the bony structures from sediment in the study dealing with fossils. It also allows to increase the contrast between the inner structures of a biological sample for better separation of the different tissues, including those with low contrasts

(adipose tissue, cartilage, blood vessels, nerves,…) (Arfelli et al. 1998, Beckmann et al. 1999, Li et al.

2003, Lewis et al. 2005, Zhang et al. 2008). The technique is particularly efficient on samples presenting very low absorption contrast. In addition to the basic edge detection regime, the application of a phase retrieval process, such as the one proposed by Paganin et al. 2002, modified later by Sanchez et al. 2012, makes possible to reach a much higher signal to noise ratio than absorption, without being limited to increased visibility of boundaries only. In the case of K-edge subtraction or bi-energy approaches, this phase retrieval process is mandatory to be able to perform the image calculations.

IV-Combined use of K-edge/bi-energy and propagation phase contrast imaging techniques

The combined used of bi-energy imaging and single distance propagation phase contrast with phase retrieval allies the best qualities of both techniques, by coupling the high quality results obtained

39 from phase-contrast with the possibility for automatic segmentation and enhanced contrasts of soft parts permitted by the use of the dual energy on the contrast agent. This is not the first use of propagation phase contrast combined with technique contrast agent (Khonsari et al. 2014, Raj et al. 2014), but it is the first time that the dual-energy approach is used in combination with propagation phase contrast, as well as the first time it is done using sodium polytungstate. Combination of such approaches allow for semi-automatic segmentation, which results in very accurate and rapid extraction of the different structures of the sample (Figure II-4, Figure II-5). Conventional scanning methods would require much more time for segmenting the data and would never reach similar level of data quality and precision.

The presented method allows for automatic segmentation, using Matlab program for separating the different tissues depending on how they were marked by the contrast agent, which is a much quicker process than other segmenting methods.

It has been noticed that even if these approaches are optimised for monochromatic beam, it is possible to reach similar results by using polychromatic beams with fine tuning of the spectrum properties. This possibility brings much higher quality in term of propagation phase contrast as the beam coherence is higher without using a monochromator, and allows for much faster scans. Sensibility to the contrast agent is a bit reduced, but it does not impact the capabilities for semi-automatic segmentations.

Figure II-4. Results of the automatic segmentation of the head of Phasianus colchicus based on K- edge subtraction (69/70 KeV, monochromatic, ID17). a-Skull bones, b-Fat, air and cartilage tissues,

40 c-Tissues marked by the contrast agent, d-3D reconstruction of the skull, e-3D reconstruction of the fat, air and cartilage tissue of the head, f-3D reconstruction of the tissues marked by the contrast agent. (scale bar : A-B-C 9 mm ; D-E-F 8,5 mm).

Figure II-5. Separation of tissues based on the combination of bi-energy (69-123 KeV monochromatic, ID17) and propagation phase contrast of a head of a juvenile Struthio camelus. a-Muscles and eyes, b-Fat and cartilage, c-brain, d-Skin, e-Skull bones (scale bar 15 mm).

The use of sodium polytungstate as a contrast agent in MR and synchrotron imaging does not make any differences in volumes calculated, showing that there are no shrinking of the tissues because of the agent. Concerning specific brain anatomy, synchrotron based images provides enhanced contrast between the different main brain structures with a special focus on the boarder of external and internal cavities of the endocast, due to the high reconstruction of mineralised tissues (also reinforced by the addition of propagation phase contrast) (Figure II-6). On the contrary, MR gives superior contrast within the brain structures, allowing more precise definition of the different brain layers (Figure II-6).

Figure II-6. Results comparisons of the use of sodium polytungstate as contrast agent in MR and synchrotron scanning techniques. Results for MR scans are presented in horizontal (a), coronal (b) and sagittal view (c). Synchrotron results (in addition with propagation phase contrast) are presented in horizontal (d), coronal (e) and sagittal view (f). (Scale bar : 8,5 mm).

V-Application to neuroanatomy

We used heads of birds belonging to 3 different species and different ranges of sizes. The smallest specimens were Ficedula albicollis, medium Phasianus colchicus and largest Struthio camelus.

The specimens were prepared by immersing them in a 4% formalin solution containing sodium polytungstate with a concentration of 50g per liter (TC-Tungsten Compounds, Grub am Forst, Germany) for different periods according to the size of the sample (from a few days for the flycatchers to almost a year for adult ostriches). Pheasants and ostriches were provided by farms in Czech Republic (BAS, s.r.o,

Skuheř, Kamenice, Czech Republic), flycatchers were provided by Prof. Bures from Palacky University,

Olomouc, Czech Republic. The specimens were mounted in column and scanned on the beamlines ID19,

ID17 and BM05 (Table II-1). The propagation distance was set at 13 m on ID19, 11 m on ID17 and 4,5 m on BM05 in order to use the maximum available phase contrast effect for these three beamlines.

Figure II-7. Soft tissues separation on the head of pheasant (Phasianus colchicus). Internal anatomy of the head in dorsal (a), frontal (b) and lateral view (c). 3D rendering of the head, with (d) and without skin representation (e). Brain (in blue), muscles (in red) and bones (in white) are represented (e). [Bo-

Bone; Ce-Cerebellum; Co-Chiasma opticum; Di-Diencephalon; Hi-Hindbrain; Me-Mesencephalon; Ot-

Optic tectum; Sc-Spinal chord; Sr-Scleral ring; Te-Telencephalon]. (Scale 8.5mm (a, b, c) and 8mm (d, e)).

Figure II-8. Soft tissues separation on the head of flycatcher (Ficedula albicollis). Internal anatomy of the head in dorsal (a), frontal (b) and lateral view (c). 3D rendering of the head, with (d) and without skin representation (e). Brain (in blue), muscles (in red) and bones (in white) are represented (e). [Bo-

Bone; Ce-Cerebellum; Co-Chiasma opticum; Di-Diencephalon; Hi-Hindbrain; Me-Mesencephalon; Ot-

Optic tectum; Sc-Spinal chord; Sr-Scleral ring; Te-Telencephalon]. (Scale 2.5 mm (a, b, c) and 4 mm

(d, e)).

Two series of two scans were used depending on the size of the specimen. For small specimens, scans were done below (68 KeV) and above the k-edge (70 KeV). In the contrary, in large specimen, in addition with the below k-edge picture, the second picture was made at 123 KeV, because of the high absorption of these large specimens just above the K-edge that was leading to nearly complete absorption of the beam. The combined use of both pictures after processing allows better separation of hard and soft tissue (Figure II-7, II-8, II-9), which simplifies the possibilities of segmentation of different cranial structures, including the brain anatomy and surrounding structures and cavities (Figure II-10, II-

11, II-12).

Figure II-9. Soft tissues separation on the head of an ostrich (Struthio camelus). Internal anatomy of the head in dorsal (a), frontal (b) and lateral view (c). 3D rendering of the head, with (d) and without skin representation (e). Brain (in blue), muscles (in red) and bones (in white) are represented (e). [Bo-

Bone; Ce-Cerebellum; Co-Chiasma opticum; Di-Diencephalon; Hi-Hindbrain; Me-Mesencephalon; Ot-

Optic tectum; Sc-Spinal chord; Sr-Scleral ring; Te-Telencephalon]. (Scale bar15 mm).

Figure II-10. 3D rendering of cerebral and endocranial structures of Phasianus colchicus. a-

External 3D rendering of the head with skin and feathers insertion b-Brain position within the skull (the skull is in white and the brain is blue); c-Details of the internal cavities (in dark blue); d- Details of the external cavities (in red). Differences between brain and external cavities (in red) representing areas where brain differ from the endocast in dorsal (e,f) and lateral view (g,h) (Colorization made with

VGStudio Max on the 3D rendering). Scale 8mm (a, b, c, d) and 5mm (e, f, g, h)

Figure II-11. 3D rendering of cerebral and endocranial structures of Ficedula albicollis. a-External

3D rendering of the head with skin and feathers insertion; b-Brain position within the skull (the skull is in white and the brain is blue); c, e-Details of the internal cavities (in dark blue); d, f- Details of the

47 external cavities (in red) (Colorization made with VGStudio Max on the 3D rendering). (Scale bar 4 mm

(a, b, c, d) and 2 mm (e, f)).

Figure II-12. 3D rendering of cerebral and endocranial structures of Struthio camelus. a-External

3D rendering of the head with skin and feathers insertion; b-Brain position within the skull (the skull is in white and the brain is blue); c-Details of the internal cavities (in dark blue); d- Details of the external cavities (in red) (Colorization made with VGStudio Max on the 3D rendering). (Scale bar 15 mm (a, b) and 4,5 mm (c, d)).

The conbined use of bi-energy and propagation phase contrast from synchrotron sources allow for clear and quick extraction of cerebral borders and cerebral cavities, permitting clear definition of the brain/endocast relation, important in the study of the evolution of brain within archosaurs.

Chapter III Fossils

When studying the evolution of brain shape in the bird line, some specimens present a key position. Compsognathus longipes is an important specimen due to its phylogenetical position, close to the origin of the Maniraptoriformes, the clade from which birds evolved. Halszkaraptor escuillei is placed at the origin of Dromaeosauridae and present an endocranial shape unexpected in such group and described in the following. Finally, Archaeopteryx, based on its supposed basal position at the root of the bird line and because of its morphological avian features, is an important specimen to look at when focusing on the relation between brain shape and flight evolution.

Figure III-1. Simplified phylogeny of the specimen mentioned below (Compsognathus longipes,

Halszkaraptor escuillei, Archaeopteryx lithographica) (modified from Cau et al. 2017)

I-Compsognathus longipes

Compsognathidae is a group of dinosaurs defined by Cope in 1871 and which represents one of the oldest group of theropod dinosaurs. They appeared during the Jurassic (Wagner 1861, Michard 1991,

Peyer 2004) and survived until the Cretaceous (Dal Sasso and Signore 1998, Ji et al. 2007, Naish et al.

2004). These small body size carnivorous dinosaurs preserved their body shape and size along their evolution. The existence of bird-like features, like feathers (Chen et al. 1998, Holtz 1998, Fucheng 2006) inspired possible relationship between Compsognathidae and early bird lineages. One of the main issues with compsognathids classification is the uncertainty of the developmental age of describer specimens, most specimen being considered as juvenile individuals. This can weaken the strength of diagnosic characters and as a consequence, can increase uncertainties on the relationships between the different compsognathids species (Callison and Quimby 1984, Hwang et al. 2004).

Figure III-2. Holotype of Compsognahtus longipes (B.S.P. A.S. I 563).

The first noticeable compsognathid specimen discovered is the Jurassic Compsognathus longipes (Wagner 1861), that has been widely described since then (Huxley 1868, Nopcsa 1903, Ostrom

1978). This species is represented by a unique fairly well-preserved specimen found during the 19th century in the Solnhofen limestone in Germany. Until the discovery of smaller specimen from this group

(Currie et al. 1994, Karhu and Rautian 1996, Xu and Norell 2004), C.longipes have long been considered being the smallest representative of this group, between 70 and 97 cm depending on the estimation

(Ostrom 1978, Paul 1988, Therrien and Henderson 2007). Another specimen was found in the Jurassic of South France, Compsognathus corrallestris, which was first considered as a synonymous of

C.longipes (Ostrom 1978, Norman 1990, Michard 1991, Glut 1997). Nevertheless, several features led to the attribution to another species, Compsognathus corrallestris (Bidar et al. 1992, Peyer 2004, Peyer

2006).

The skeletton of this specimen of C.longipes (B.S.P. A.S. I 563) is almost complete, only few vertebras, femur and parts of other long bones are missing (Figure III-2). Bones are generally well preserved with the exception of some cracks on long bones. The skull looks complete even if it is totally disarticulated and partially flattened. Despite the lack of anatomical contacts between cranial bones, the relative position of each bone against the others. The specimen is preserved lying on its right side and contrary to the skull the rest of the skeletton is not disarticulated, except for the ribs and the hand elements. Part of it (skull, bones diaphysis, and dorsal vertebrae) have been scanned at the beamline

BM05 and ID19 with various resolutions for the need of this PhD and the one of Dennis Voeten.

Unfortunately, due to technical limitations on both beamlines, no complete scan of the specimen was performed.

Save for the dislocation mentioned above, the skull bones are quite well preserved, considering that the integrity of most of them is preserved, and the fact that relative position of every bones is quite maintained (Figure III-2). In his description of C.longipes skull, Ostrom (1978) suggested two possibilities for explaining this dislocation level: this skull deformation might be related either to high kinetism or bones being loosely linked together. In addition with bone microstructure (Voeten et al.

2018), this skull organisation would suggest that this specimen is a juvenile.

Figure III-3. Reconstruction of the skull of Compsognathus longipes. a-Skull of C.longipes on the slab; b-Virtual reconstruction of the slab surface with bones highlighted (in red) ; c-d-Virtually extracted bones in external (c) and internal view (d). (Scale bar: 10 mm for a-b, 15 mm for c-d).

The main aim of this extraction of bone was to recreate a 3D view of the skull in order to access the braincase and study the endocast. As mentioned previously, despite the dislocation, bones are generally well preserved which allowed to virtually replace them in anatomical position (Figure III-4).

The main components of the braincase accessible on this specimen are the frontals, the parietal and the occipital region (described by Ostrom as the « braincase »). The possible suture that can be observed on the dorsal view from the slab is much more visible in ventral view which suggest that both frontals were not fully fused. The parietals are still present but too much deformed to make the same assertion about their possible non-fusion. The suture between frontals and parietal is not certain as the anterior part is broken. The occipital region cannot be described more precisely as the articulation between the different bones cannot be observed precisely. Furthermore, this occipital region has experienced an important anteroposterior compression that does not allow any observation on the depth of the structure (Figure

III-3).

Figure III-4. Skull reconstruction of C.longipes. a-Skull reconstruction modified from Ostrom (1978), b-c-3D skull reconstruction from synchrotron data in right (a) and left (b) view (Scale bar : a-10 mm ; b-c-15 mm).

The endocranial reconstruction allowed by the reconstructed skull is limited, due to the incompleteness of the braincase area (Figure III-5). Only the dorsal part, in contact with the cranial roof and the occipital region are preserved. The dorsal part presents the surface of the olfactory tracts and the telencephalon. A ridge can be observed on the olfactory tracts, defining them as paired organs, contrary to most of the dinosaur endocast except Non-tyrannosauroid Coelurosauria. They also present on their anterior end a bulge, which can be interpreted as the olfactory bulb. The damages on the parietal and the absence of preservation of the fronto-parietal boundary does not allow clear observations on this part.

There is no evidence of a ridge between the telencephalic hemisphere, even if a small portion of the anterior part of the telencephalon presents a ridge, in the continuity with the olfactory tracts. This does not permit any further interpretation on cerebral representativity of the endocast, which could be suggested by the clear definition of the ridge between olfactory tracts. As previously mentioned, the occipital region cannot really be described precisely. The foramen magnum tends to be more posterior than ventral, which suggest a low coiling of the endocast, which might be similar to what is observed in most of dinosaurs, except Maniraptoriforms. But to consider this positioning of the foramen magnum in life position requires to consider that the occipital region had only experienced antero-posterior compression. The compression of the other bones, close to a dorso-ventral compression and the posterior rotation of the occipital region tend to suggest that the antero posterior compression was not the only deformation experienced by this area.

Figure III-5. Virtual reconstruction of the endocast of Compsognathus longipes. In dorsal (a), lateral

(b) and posterior view (c). Scale bar : 4 mm.

The experiments realised on this specimen, with scans of the skull and long bones, will also be an important specimen for redescribing Compsognathidae. The observation made after realising scans will add more morphological informations and help to define which characters describing this group are diagnosic. This will allow to make a reappraisal of compsognathids, which specimens rely on this group and what are the main characters defining this clade.

II-Haslzkaraptor escuillei

Halszkaraptor escuillei is considered as being a sister taxa of Eudromaeosauridae (Figure III-

6). This specimen is the type species of a new dromaeosaurid subfamily, Halszkaraptorinae, which also include Hulsanpes perlei (Osmolská 1982) and Mahakala omnogovae (Turner et al. 2011). This specimen possesses very peculiar postcranial morphology, related to its ecology, which were not expected considering that it belongs to dromaeosauridae. These postcranial characters and inferrence on its ecomorphology are presented in chapter 5 (Cau et al. 2017). As the specimen is still embedded in its lithic matrix, some characters might not be accessible despite the exquisite preservation on the surface of the slab. Moreover, as the specimen have been lost for science during a long period and navigated between several private collections, it was difficult to know which works have been realised in order to increase the aesthetic quality of the object. The use of synchrotron scanning performed on the beamlines

ID19 and BM05 allowed to extract the complete skeleton (Figure III-6) and to check which part of the specimen are original fossils and which have been reconstructed, which allow unbiased scientific analysis and observations.

The skull of H.escuillei is quite well preserved and almost complete, except a lateral deformation that results in a misalignement between the skull and the mandible. Even the internal anatomy of the skull, not observable on the specimen because it is still embedded on the slab, is retained, with the presence of the parasphenoid and the preservation of the ventral part of the braincase, allowing a relatively accurate reconstruction of the endocast.

Figure III-6. Reconstruction of the skeletton of Halszkaraptor escuillei. Original specimen (a), 3D rendering of the skeleton in the rock matrix (b), skeleton extracted (c). Scale bar : 70 mm (b and c modified from Cau et al. 2017).

The nostrils are positioned posteriorly compared to what is observed in dromaeosaurids. It refers more to the nasal anatomy of piscivorous dinosaurs, like Spinosauridae (Holtz 1998, Ibrahim et al.

2014). Another important feature visible in this skull on lateral view is the curved fronto-nasal region

(Figure III-7), which is more straight in eudromaeosaurs. Furthermore, the parieto-occipital region is more curved than the bended shape observed in other dromaeosaurian dinosaurs.

Figure III-7. 3D representation of the skull of Halszkaraptor escuillei. 3D visualisation of the skull in right (a), left (b), ventral (c) and dorsal view (d) with schemes of skull reconstruction in left (e) and dorsal view (f). Scale bar 9 mm.

The teeth of H.escuillei are presenting peculiar characteristics. Typically, dinosaurs only show one kind of teeth morphology, even if simple shape variations can be observed within a set of teeth

(Smith 2005). This homodonty usually reflects specialised dietary behaviours (carnivory, herbivory, piscivory,…). Heterodonty have been noted in few Dinosauria such as Lycorhinus consors (Thulborn

1974) presenting abrasive and resistant diet with particular replacement pattern, not a continuous replacement as supposed in most on dinosaurian groups, but with only replacement periods limited to a short time in the year. Heterodonty have also been observed Eoraptor lunensis (Sereno et al. 1993), suggesting omnivorous diet. In Masiakasaurus knopfleri (Sampson et al. 2001) tend to suggest a divergence from the usually observed theropod diet. The heterodonty of Incisivosaurus gauthieri (Xu et

58 al. 2002) suggest a possible herbivory, features fewly observed in theropods (Barrett 2005, Zanno and

Makovicky 2010). H.escuillei present two types of teeth, depending of their position in the mouth with a brutal separation between these two kind of teeth at the boarder between the premaxilla and the maxilla. The anterior teeth, positioned on the premaxilla, are elongated, tubiform and relatively straight

(Figure III-8 A-B-C). On the contrary, posterior teeth along the maxilla and the preserved part of the dentary are closer to typical dromaeosaur-like shape, with labio-lingually compressed and anteriorly curved teeth (Figure III-8 D-E-F). We mentioned that the dentary teeth are more dromaeosaur-like but it is necessary to notice that the most anterior part of the dentary are not preserved, so we cannot assess of the shape of the anterior lower teeth. Not only the shape, but also the replacement pattern tends to be different between the two types of teeth. Anterior teeth have a very large root and a replacement tooth every three to four teeth already in place, contrary to the very thin root of posterior teeth, which present a replacement tooth for every tooth in place. Such kind of shape observed in maxillary teeth, symmetrical and unserrated has already been observed in Fukuivenator paradoxus and seem to show a dietary modification, from the typical carnivorous to a more omnivorous diet (Azuma et al. 2016).

The snout of H.escuillei also present unusual structures on its premaxilla (Figure III-9), anteriorly to the nostrils. Those small holes visible on the surface of the bones, are connected together by a complex web of nerves joining all together on the posterior part of the premaxilla (Chapter 5, Figure

2, Supplementary Figure 6). This kind of structures is quite common in aquatic piscivorous archosaurs such as crocodiles (Chapter 4, Supplementary Figure 8) (Leitch and Catania 2012), and aquatic reptiles

(Foffa et al. 2014), but also in Spinosaurids (Ibrahim et al. 2014) and other theropods groups (Berker et al. 2017), that have been interpreted as piscivorous animals. It is the first occurrence of such structure in a non-spinosaurid dinosaurs. As the two previously mentioned groups are semi-aquatic species or at least using aquatic environment for feeding, these observations led to suggest that H. escuillei had a semi-aquatic lifestyle (later strengthened by other postcranial characteristics mentioned in Chapter 5).

Figure III-8. Teeth morphology of Halszkaraptor escuillei. a-c-Premaxillary teeth; 2d slide on top view (a, scale 0.2mm); lateral view (b, 0.6mm); transparency and root morphology (c, 0.65mm). d-f-

Maxillary teeth; 2d slide on top view (d, 0.15mm); lateral view (e, 0.8mm); transparency and root morphology (f, 1 mm).

a b

c d

e f

Figure III-9. 3D visualisation of the snout and teeth arrangement of Halszkaraptor escuillei. In lateral view with (a) and without the snout bones (b), in frontal view with (c) and without snout bones

(d), teeth organisation in dorsal (e) and ventral view (f). (Scale bar 1,5 mm).

The endocast of Halszkaraptor escuillei is relatively well preserved (Figure III-10). The globular shape is clearly defined and the borders between structures, despite some preservation artefacts linked to the granular rock matrix, can be accurately observed. The limits of the globular optic tectum is very visible, especially on the left side, which help to define extension of the cerebellum and telencephalon. The olfactory tracts are very elongated but narrow. They seem to be fused but the low preservation of this area does not allow to precisely define if they are separated or not. The anterior preservation of the olfactory tracts does not allow any observation on the olfactory bulbs. The rhombencephalon allows the observation of the rounded shaped cerebellum and expand laterally close to the extreme lateral expansion of the optic lobes and the cerebral hemispheres, but the distinction between the cerebellum and the medulla oblongata is not clear. Despite some deformation, the foramen magnum is well preserved, positioned posteriorly to the skull but related to the rounded shape of the skull, it is more ventrally positioned than in any other non-avian dinosaur endocast (Witmer and Ridgely

2009, Balanoff et al. 2014,). In accordance with other Maniraptoriformes and avian taxa, the interface between the telencephalon and the cerebellum lacks a dural peak (Lautenschlager and Hübner 2013).

Due to the low preservation of bone continuity related to bone dissolution observed, cranial nerves (with the exception of the olfactory tracts previously mentioned), cerebellar flocculus and semicircular canals are not visible. The globular shape of H.escuillei is closer to the shape observed in the avialan lineage, and especially Archaeopteryx (Alonso et al. 2004, Kawabe et al. 2013, Walsh et al. 2016) than what is observed in any other dinosaurian lineage (Hopson 1979, Hurlburt 1994, Zheng 1996, Larsson 2001,

Franzosa 2004, Sanders and Smith 2005, Saveliev and Alifanov 2007, Sampson and Witmer 2007,

Evans et al. 2009, Paulina Carabajal and Canale 2010, Bever et al. 2011, Knoll et al. 2012, Farke et al.

2013, Lautenschlager and Hubner 2013, Lauters et al. 2013, Paulina-Carabajal 2014, Xing et al. 2014,

Leahey 2015, Thomas 2015, Paulina-Carabajal 2016), even within sister maniraptoran lineages of

Halszkaraptorinae (Witmer and Ridgely 2009, Tahara and Larsson 2011, Balanoff et al. 2013, Cuff and

Rayfield 2015). This endocranial shape and organisation tend to suggest that H.escuillei already experienced more advanced cerebral encephalisation than most of the other Maniraptoriformes.

Figure III-10. Endocast anatomy of Halszkaraptor escuillei. Endocast of Halszkaraptor escuillei in left (a), posterior (b), right (c), anterior (d), ventral (e) and dorsal view (f). Organisation of cerebral component represented in the endocast in lateral (g) and dorsal (h) view (Telencephalon=orange, Optic tectum=red, Cerebellum=yellow, Medulla oblongata=green) (Scale bar= 4 mm). Arrows present the upper (blue) and lower (yellow) borders of the foramen magnum

III-Archaeopteryx

Considered as the most basal ancestor of avialan (Owen 1862, Ostrom 1973) even if this position have been challenged (Chatterjee 1991, Witmer 2011), Archaeopteryx have also been considered as the first potential flying bird (Heptonstall 1970, Cox 1974, Burgers and Chiappe 1991, Speakman 1993,

Padian and Chiappe 1998, Long et al. 2003, Meseguer et al. 2012) based on the existence of post-cranial avian characteristics like wings (Paul 1984, Thulborn and Hamley 1984, Burgers and Chiappe 1991), feathers (Harrison 1976, Ji et al. 2001, Dyke 2010, Nudds and Dyke 2010, Longrich et al. 2012, Foth et al. 2014), pectoral girdle anatomy (Olson and Feduccia 1979) or long bones cross-sections shape and organisation (Voeten et al. 2018).

Figure III-11. Archaeopteryx skulls and endocast used for this study. Archaeopteryx lithographica

BMNH 37001 (a) (modified from Alonso et al. 2004), Archaeopteryx simiensii BSP 1999 I 20 (b)

(modified from Rauhut 2014), Archaeopteryx BSPG VN-2010/1 (c) and Archaeopteryx recurve JM

2257 (also named Jurapteryx recurve) (d) (modified from Xu and Pol 2013).

Cognitive requirements that a individual have to achieve to perform complex flight is an important topic to address for understanding evolution of flight, as such cerebral organisation is a key structure to study in order to understand how flight evolve within bird lineage. Because of its basal position in the avialan lineage, a particular attention on Archaeopteryx neuroanatomy. First observation made on an Archaeopteryx endocast placed it closer to other reptilies than to birds (Edinger 1926, De

Beer 1954). Since then, the organisation of the Archaeopteryx endocast has been considered as an intermediate state between dinosaurs and birds (Jerison 1968, Alonso et al. 2004, Witmer 2004, Balanoff et al. 2013).

Since the discovery of the Archaeopteryx holotype in 1861, 12 specimens have been unearthed.

4 of these specimens, preserving skulls (Figure III-11), were scanned at the ESRF.

The second Archaeopteryx specimen (BMNH 37001) is named Archaeopteryx lithographica, and defined as the holotype of the Archaeopteryx genera (Whybrow 1982) and referred as the “London specimen”. The skull with partially exposed endocast was separated from the rest of the specimen on the slab, which helps making observations, even without the modern scanning methods (Figure III-11a).

This endocast presents the natural cast of the endocranial cavity on its right side and half of the braincase on the left side. Bones, mainly the frontals and parietals, are well preserved and help to reconstruct the endocranial characters of the specimen, the bones forming the occipital region are difficult to separate.

The good preservation level of the bone helped to preserve the semicircular canals (Figure III-12).

Broken bones on the parietal area led to misinterpretation of the presence of the wulst on this specimen

(Balanoff et al. 2013, Chapter 6 of the present thesis). The endocast of the “London specimen” presents two pyriforms telencephalic hemispheres. On the most anterior part of these hemispheres, the olfactory tracts are paired and not fused contrary observed in most of the other non-maniraptoriform theropod dinosaurs, and make it much closer to avian-like endocranial shape. Furthermore, the suture between the two cerebral hemispheres is clearly visible. This endocast presents two large optic tecta on the antero- posterior position, visible in lateral view. This is also a cerebral feature shared with the avian lineage.

Contrary to birds, the foramen magnum, and as such the interface between the medulla oblongata and the spinal chord is not as ventral but not as posterior as other non-avialan dinosaurs, except from some

Maniraptoriformes. Cerebral vascularisation can be observed on the ventral part of both cerebral hemisphere (Figure III-13 A).

Ce Cb Ce Cb ee b Ce e Cb b Ce

ee e OT Olt ee Ce Cbee OTe ee eee e ee e

Olt

Ce ee OT ee e Olt Cb ee ee e ee e e

Ce ee OT

Figure III-12. Endocrania and braincase anatomy of the Archaeopteryxee lithographica BMNH e 37001. Specimen is presented with and without the braincase, in left (a-b), right (c-d) and dorsal view

(e-f). The bones composing the braincase are represented in red, the semicircular canals are visualised in green, the yellow part represents the endocast. Ce: Cerebrum; Cb: Cerebellum; OT: Optic tectum, olt:

Olfactory tracts (Scale bar = 3,5 mm).

Figure III-13. Endocranial vascularisation in Archaeopteryx specimens. For the Archaeopteryx lithographica BMNH 37001 (A, Scale bar = 1,5 mm) and Archaeopteryx simiensii BSP 1999 I 50 (B,

Scale bar = 6,5 mm). White arrows indicate some of the vascularisation traces.

The fifth Archaeopteryx specimen (JM 2257), named Archaeopteryx recurve (synonymous

Jurapteryx recurve) (Howgate 1984), is referred as the “Eichstätt specimen”. This specimen experienced an important dorso-lateral compression which does not allow any measurements on the extracted endocast (Figure III-14 A). Despite these deformations, some observation can still be made on the shape of some cerebral components. The pyriform shape of the telencephalic hemisphere is preserved, on both hemispheres, even if the right one is better preserved. The preservation of the skull roof on the frontal allow to observe the telencephalic suture between both hemispheres (Figure III-14 C). The shape of the optic tectums is well preserved even if their position, relative to other cerebral components, is not perfectly retained. The right optic tectum is still preserved in the antero ventral position of the cerebral hemisphere but the deformation can have changed its anatomical positioning. The compression of the occipital area does not permit any anatomical observation on the rhombencephalon. The parietal experienced a hard dissolution event which removed most of the bones. The natural endocast is still accessible but this lack of bones does allow for any observation about the presence of vascularisation and wulst.

ee Olt

e Ce ee e Olb Ce eee OT ee e ee Figure III-14. Endocranial anatomy of the Archaeopteryx recurva JM 2257. 3D rendering of the e skull of the Eichstätt Archaeopteryx (A); Skull in transparency with the position of the endocast (B),

Endocast anatomy (C). Ce: Cerebrum; OT: Optic tectum, Olt:Olfactory tracts, Olb:Olfactory bulbs

(Scale bar= A-B 5 mm; C 3 mm)

The seventh Archaeopteryx specimen (BSP 1999 I 50), named Archaeopteryx simiensii (Mayr et al. 2007) is referred as the “Munich specimen” or “Solenhofer-Aktien-Verein Specimen”. This specimen has also been described as Archaeopteryx bavarica (Wellnhofer 2008). This specimen only presents a partial endocast (Figure III-15). From the braincase, only the left parietal is preserved which only allow incomplete reconstruction of the left hemisphere and the upper part of the left optic tectum.

The few endocranial parts presented in this specimen tend to have a similar shape and relative position

68 compare to what is observed on the “London specimen”. As well as this specimen, the “Munich specimen” shows evidence of cerebral vascularisation (Figure III-15 B) and the lack of wulst.

Ce ee

OT ee

Figure III-15. Skull and endocranial anatomy of archaeopteryx simiensii (BSP 1999 I 50). 3D view of the partial skull of the Munich Archaeopteryx (A), Endocast in lateral view (B), Endocast and skull in transparency (C), Reconstruction of the full Munich endocast based on the shape of the London specimen (D). Ce: Cerebrum; OT: Optic tectum (Scale 3.5mm).

The eigth Archaeopteryx specimen (BSPG VN-2010/1), named Archaeopteryx sp. is also referred as the “Daiting specimen” (Tischlinger 2009). The skull of this specimen, even if it is still almost complete, have been very flattened and crushed by taphonomical events. As well as for the

“Eichstätt specimen” any 3D measurements is impossible due to this compression (Figure III-15).

Despite these deformation, the endocast presents a possible separation between the two telencephalic hemispheres, which, as well as the previously mentioned Archaeopteryx specimens, present a pyriform shape. The posterior region of the endocast is too much crushed to allow observations, except the presence of the left optic tectum, in antero-ventral position, even its real position might be a bit different than what the endocast is presenting, because of the deformation that occurred during fossilisation. The deformation experienced by the specimen also caused extreme fracturation of the parietal with does not permit very precise anatomical observation such as the presence or absence of endocranial vascularisation or wulst.

Ce ee Ol te e OT ee

Figure III-16. Skull and endocranial anatomy of archaeopteryx sp. (BSPG VN-2010/1). 3D rendering of the skull of the Daiting Archaeopteryx (A); Skull in transparency with the position of the endocast (B), Endocast anatomy (C).Ce: Cerebrum; OT: Optic tectum; Olt: Olfactory tracts. (Scale bar

A-B 2,5 mm; C 1,5 mm).

The addition of several other Archaeopteryx specimen, despite some issues related to preservation, allows to confirm the first observations realised on the London specimen. It confirms the separation and the shape of the two hemispheres, the large visibility of the different cerebral structures as well as the absence of wulst, contrary to what have been previously suggested (Balanoff et al . 2013).

Chapter IV

Synchrotron scanning reveals amphibious ecomorphology in a new

clade of bird-like dinosaurs

Letter doi:10.1038/nature24679

Synchrotron scanning reveals amphibious

ecomorphology in a new clade of bird-like dinosaurs Andrea Cau1, Vincent Beyrand2,3, Dennis F. A. E. Voeten2,3, Vincent Fernandez2, Paul Tafforeau2, Koen Stein4, Rinchen Barsbold5, Khishigjav Tsogtbaatar6, Philip J. Currie7 & Pascal Godefroit8

Maniraptora includes birds and their closest relatives among Locality and horizon. Bayn Dzak Member, Djadokhta Formation theropod dinosaurs1–5. During the Cretaceous period, several (Campanian, ~75–71 Mya), Ukhaa Tolgod, Mongolia (see maniraptoran lineages diverged from the ancestral coelurosaurian Supplementary Information). bauplan and evolved novel ecomorphologies, including active Diagnosis. Autapomorphies are marked by asterisks; differential 2 3 4 5 flight , gigantism , cursoriality and herbivory . Propagation X- •diagnosis can be found in Supplementary Information. Platyrostral ray phase-contrast synchrotron microtomography of a well- premaxilla that forms 32% of snout length*and bears 11 teeth*; preserved maniraptoran from Mongolia, still partially embedded in the rock matrix, revealed a mosaic of features, most of them external naris posterior to the premaxillary oral margin; rod-like jugal absent among non-avian maniraptorans but shared by reptilian with an ascending process excluded from the orbital margin that forms and avian groups with aquatic or semiaquatic ecologies6–14. This only 10% of the postorbital bar*; rod-like ventral ramus of the new theropod, Halszkaraptor escuilliei gen. et sp. nov., is related to postorbital; other enigmatic Late Cretaceous maniraptorans from 22 presacral vertebrae; neck forms 50% of snout–sacrum length*; Mongolia15,16 in a novel clade at the root of Dromaeosauridae17. absence of epipophyses*; ridge-like cervical neural spines restricted to This lineage adds an amphibious ecomorphology to those evolved by maniraptorans: it acquired a predatory mode that relied the 2nd–5th vertebrae*; postzygapophyses on cervicals 2–5 are fused mainly on neck hyperelongation for food procurement, it coupled medially and form single lobate processes*; pleurocoels restricted to the obligatory bipedalism of theropods with forelimb proportions cervicals 7–9; tuber-like neural spines in tail are restricted to the 1st– that may support a swimming function, and it developed postural 3rd vertebrae*; proximal-most chevrons large and pentagonal*; adaptations convergent with short-tailed birds. transition point in 7th–8th caudals; 3rd finger longer than 2nd; elongate Theropoda Marsh, 1881 pedal phalanx III-1 is 47% of the length of metatarsal III*. Maniraptora Gauthier, 1986 We performed multi-resolution scanning at the European Dromaeosauridae Matthew and Brown, 1922 Synchrotron Radiation Facility using BM05 and ID19 beamlines; this Halszkaraptorinae subfam. nov. revealed all the elements that were still embedded in matrix and

Definition. The most inclusive clade that contains Halszkaraptor demonstrated the integrity of the specimen (Supplementary escuilliei gen. et sp. nov., but not Dromaeosaurus albertensis, Information, Extended Data Figs 1–3). Histological analysis indi-cates Unenlagia comahuensis, Saurornithoides mongoliensis or Vultur that MPCD-102/109 was a subadult individual (Supplementary gryphus. Taxa included: Halszkaraptor escuilliei, Hulsanpes perlei15 Information, Extended Data Figs 4, 5). The platyrostral premaxilla with and Mahakala omnogovae16. Type species: Halszkaraptor escuilliei. a dorsolaterally oriented external naris that is retracted beyond the oral Diagnosis. Long-necked dromaeosaurids with proximal caudal margin is unique among theropods, although in its elonga-tion, the 8 •vertebrae that have horizontally oriented zygapophyses and premaxilla is similar to those of spinosaurids (Fig. 2a–g, Extended prominent• zygodiapophyseal laminae; flattened ulna with a sharp Data Figs 6, 8). A hypertrophied network of neurovascular chambers posterior •margin; metacarpal III shaft transversely as thick as that of penetrates throughout the premaxilla. This condition is also seen in aquatic reptiles, such as plesiosaurs12 and crocodiles (Fig. 2e, f, metacarpal• II; ilium with a shelf-like supratrochanteric process; Extended Data Fig. 8), whereas in other theropods this neuro-vascular posterodistal surface of femoral shaft with an elongate fossa bound by network resides exclusively in the lateral half of the •premaxilla13. a lateral crest; proximal half of metatarsal III unconstricted and Each premaxilla bears 11 teeth (Fig. 2g, Extended Data Figs 6, 7), markedly convex anteriorly. which is the highest number found in any dinosaur. Spinosaurids and Halszkaraptor escuilliei gen. et sp. nov. Pelecanimimus approach Halszkaraptor in having six or seven premaxil• lary teeth8, whereas most theropods have four. Both the Etymology. Halszka, a Latinized form of archaic Polish Halżka, maxilla and the dentary bear 20–25 teeth; this is comparable to the honours Halszka Osmólska (1930–2008) for her contributions to condition seen in unenlagiines17 and baryonychines8. Although some theropod palaeontology,• which include the description of the first maniraptori-forms carry a total of over 30 small maxillary and/or halszkarap-torine species found (Hulsanpes perlei)15; raptor, ‘robber’ •dentary teeth5, most theropods have fewer than 20. The heterodont (Latin). The specific name escuilliei refers to François Escuillié, who dentition of Halszkaraptor involves closely packed premaxillary teeth returned the poached holotype to Mongolia. with long roots and incisiviform crowns, and a labiolingually compressed pos-terior dentition with shorter roots and concave distal Holotype. MPC (Institute of Paleontology and Geology, Mongolian crown margins (Fig. 3d, Extended Data Fig. 7). All teeth lack Academy of Sciences, Ulaanbaatar, Mongolia) D-102/109 (Figs 1, 2, serrations, as is the case in most paravians7, spinosaurines8 and a few 3a–f, Extended Data Figs 2–8, Supplementary Table 1); an articulated other theropods. Synchrotron scanning revealed a delayed replacement and almost complete skeleton preserved three-dimensionally. pattern in the anterior dentition14, whereas the majority of the posterior teeth are associated with a replacement tooth.

1Geological and Palaeontological Museum ‘Giovanni Capellini’, I-40126 Bologna, Italy. 2European Synchrotron Radiation Facility, F-38043 Grenoble, France. 3Department of Zoology and Laboratory of Ornithology, Palacký University, CS-40220 Olomouc, Czech Republic. 4Earth System Science – AMGC Vrije Universiteit Brussel, B-1050 Brussels, Belgium. 5Palaeontological Center, Mongolian Academy of Sciences, Ulaanbaatar 201-351, Mongolia. 6Institute of Palaeontology and Geology, Mongolian Academy of Sciences, Ulaanbaatar 210-351, Mongolia. 7Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada. 8Directorate Earth & History of Life, Royal Belgian Institute of Natural Sciences, B-1000 Brussels, Belgium.

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Figure 1 | H. escuilliei MPC D -102/109. a, 3D rendering of synchrotron data proximal end of right ulna (g), right ulna mid-shaft (h) and left tibia mid- that provides an overview of the exposed skeleton with plaster-restored parts shaft (i). All are oriented with their lateral margin at the bottom. j, removed. d1, first dorsal vertebra. b, Exposed skull in lateral view with restored Exposed pelvis and hindlimbs. k, Proximal caudal vertebrae in dorsal elements in blue. c, Cervical vertebrae 2–4 in dorsal view. Poz, view. ch, chevron; pz, prezygapophysis; ri, rib. l, Skeletal reconstruction postzygapophysis. d, 3D rendering of left forelimb. Note splints of bone with missing elements in grey. Numbers in e–i indicate cortical/cross- (marked as ‘s’) near metacarpal III and adjacent phalanx that are still embedded sectional area ratios. Scale bars, 70 mm (a), 30 mm (b), 20 mm (c, d, j, in the main slab (Supplementary Information). e–i, Virtual cross-sections of k), 2 mm (e–i) and 100 mm (l). right humerus mid-shaft (e), right radius mid-shaft (f),

Compared to body size, the neck is elongate and forms 50% of the non-scansoriopterygid theropods20 in the progressive elongation of snout–sacrum length; this is the highest value found among Mesozoic 18,19 the lateral fingers, with the third being the longest and most robust paravians thus far. Cervical centra 2 to 10 are low, elongate and (Figs 1d, 3e). In the ilium, the iliofibularis muscle origin is hypertro- transversely compressed towards their ventral edges (Figs 1a, 1c, 3e). phied and shelf-like, as is the case in Mahakala16. The 76-mm-long Cervical neural spines are poorly developed and remain limited to the femur has a large trochanteric crest, a tuber-like 4th trochanter and an first five vertebrae (Fig. 1c). The first five neural arches are also unique elongate posterolateral ridge that distally bounds an elongate ansa among theropods in their lack of inter-postzygapophyseal spaces: iliofibularis; the last feature is shared exclusively with Mahakala16. instead, each pair of postzygapophyses forms a single planar surface The metatarsus lacks cursorial adaptations and measures 80% of that faces ventrally and has a convex posterior margin. This femoral length; in the comparably sized Mahakala, the metatarsus is morphology• is also seen in some long-necked chelonians7 and a few longer than the femur16. The distal ends of metatarsals II and III are birds (for example, Cygnus, Fig. 3h–j). No epipophyses are present and ginglymoidal (Fig. 3e), as is the case in many dromaeosaurids15– pneumatic recesses are present only in the 7th–9th cervical centra•. 17,21,22. As is the condition in the other halszkaraptorines and in many The diapophyses are positioned at the anterolateral corners of all basal avialans22, the proximal half of metatarsal III is not constricted •vertebrae, at the bases of the prezygapophyses. The robust cervical and dorsally convex. The distal shaft of metatarsal III differs from ribs are fused to both the parapophyses and the diapophyses, as is the those of Hulsanpes and Mahakala in that it does not overlap case in Mahakala16. The proximal tail vertebrae (Fig. 1k) share with metatarsal II and lacks a distinct transverse constriction proximal to 15,16 those of Mahakala the combination of elongate centra, wide and the trochlea . The distal end of the first toe reaches the level of the horizontally oriented zygapophyses, and prominent zygodiapophyseal articular facet of the second ungual. The phalanges of the second-to- laminae that form lateral shelves16. The caudal neural spines are fourth toes shorten toward the distal ends of the toes. The second toe is half the length of the third (Fig. 3e),with a stout phalanx II-2 and a reduced, tuber-like and restricted to the first three vertebrae. The 17,21,22 proximal chevrons are pentagonal and plate-like. The large sternal large falciform ungual, similar to those in other paravians . Phalanx III-1 is slender and elongate (47% of the length of metatarsal plates are unfused medially. In the exposed forelimb bones, cortical thickness decreases towards III). The third and fourth unguals are only slightly recurved. the epiphyseal ends and culminates in extremities that are almost Phylogenetic analyses place Halszkaraptor within a new and basal completely dissolved (Fig. 1d). This preservation pattern is also seen clade of dromaeosaurids here described as Halszkaraptorinae, which in Mahakala16. The whole ulna is flattened and possesses an acute also includes the hitherto enigmatic Hulsanpes and Mahakala (Fig 3a– posterior margin (Fig. 1g–h), traits that are also similar to Mahakala, f, Extended Data Figs 9, 10, Supplementary Information). The unusual but which differ from other paravians16,17. The hand differs from morphology of Halszkaraptor suggests a semiaquatic ecology. Piscivory, 3 9 6 | N A T U R E | V O L 5 5 2 | 2 1 / 2 8 D E C E M B E R 2 0 1 7

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Figure 2 | Skull of H. escuilliei MPC D-102/109. a– d, 3D visualization of the rostral terminations of the maxillary branch of the trigeminal nerves. g, skull in right lateral (a), left lateral (b), ventral (c ) and dorsal (d) views. e, f, 3D rendering of preantorbital part of skull in palatal view. p11, 11th Synchrotron scan segmentation of the snout in dorsal view (f) that shows the premaxillary tooth. h, i, Skeletal reconstruction of skull in lateral (h) and enlarged bony chambers (e) that house the blood vessels and dorsal (i) views. Scale bars, 9 mm (a–d) and 3 mm (e–g). documented among basal dromaeosaurids23,24, is inferred from sev- Halszkaraptor is interpreted as an amphibious theropod: an obligatory eral features of Halszkaraptor, including a platyrostral •premaxilla8, biped on land and a swimmer that used its forelimbs to manoeuvre in narial retraction8, an extensively developed neurovascular plexus in water and that relied on its long neck for foraging. The hyper-•elongate the premaxilla12, an increase in the number of teeth8, and a pattern of neck of Halszkaraptor, countered by a less-elongated tail, suggests that protracted• replacement in anterior dentition14, all of which are shared its centre of mass was shifted anterior to the hip region. Although by aquatic predators. Neck elongation is widespread among saurop- the forward centre-of-mass position is functionally adaptive during sids that use an ambush mode of predation in water6, and the cervical swimming27, it challenges the obligate bipedal posture of theropods morphology of Halszkaraptor (unique among non-avian theropods) that requires the centre of mass to be near the hip joint28. During their is exclusively shared with semiaquatic lineages such as araripemydid evolution, short-tailed birds have compensated for a similar anterior turtles7 and some long-necked anatids (Fig. 3g–i). The horizontally shift of their centres of mass by increasing hip extension ability28. The oriented• zygapophyses in the neck and tail vertebrae of halszkarap- shelf-like supratrochanteric process of the ilium and the •posterolateral torines would have permitted the axial undulatory swimming mode fossa–crest complex in the femur, which are synapomorphies of that is typical of taxa with axially elongated body shapes6. The unusual halszkaraptorines16, indicate an increased hip extension moment arm forelimb morphology is not inconsistent with a semiaquatic ecology. for the iliofibularis muscle28; this would have supported a body •posture Although the fragmentary preservation of the pectoral region prevents that was more erect on land, which is analogous to the postures of a detailed reconstruction of forelimb range of motion, on the basis of modern birds. phylogenetic bracketing17,26 we infer that the glenoid in Halszkaraptor The ecomorphology of the Halszkaraptorinae markedly deviates faces laterally, as it does in forelimb-assisted swimming tetrapods25. from those of other maniraptorans and may represent the first case The upper limb exhibits flattening of the long bones, which resulted among non-avian dinosaurs of a double locomotory module29 that in a forearm and distal humerus that possess ellipsoid cross-•sections includes forelimb-assisted swimming. It illustrates how much of the (Fig. 1e–h). This condition is widespread among secondarily diversity of Dinosauria remains undiscovered, even in intensely studied aquatic amniotes9–11. Morphometric comparison of the forelimb of regions such as Mongolia.

Halszkaraptor with those of terrestrial, aquatic and flying sauropsids gliding adaptations20; instead, the proportions of Halszkaraptor cluster supports the idea that this theropod possessed swimming adaptations with those of long-necked aquatic reptiles (Fig. 4a). (Fig. 4, Supplementary Information). Among the disparate locomotory morphologies of birds, the forelimb of Halszkaraptor clusters with those of wing-propelled swimming birds, with parameters intermediate• between those of penguins and those of other aquatic birds (Fig. 4b). The asymmetrical digital elongation in Halszkaraptor exceeds known maniraptoran conditions and differs from the extreme propor-tions of scansoriopterygids, which have been interpreted as

urn:lsid:zoobank.org:act:B14CF603-F0E9-4DC6-9BB1-D215549B6D4F; and for Data Availability This published work and the nomenclatural acts it contains H. escuilliei, LSID urn:lsid:zoobank.org:act:6C4BFD0B-DAF7-4B94-B97E- have been registered in ZooBank. The ZooBank life science •identifiers can 6F9423EB6D35. The phylogenetic and morphometric data •supporting the be resolved and the associated information viewed by •appending the life findings of this study are available within the paper and its Supplementary science identifiers to the prefix http://zoobank.org/. The life science identifier Information. The synchrotron data used in this study are available on the ESRF for this publication is LSID urn:lsid:•zoobank.org:pub:7FE47556-61CD- open access database at http://paleo.esrf.fr. 4A25-AAD6-A469DA664480; for Halszkaraptorinae, LSID urn:lsid:zoobank. org:act:12E4325C-D1DA-4EAF-8539-25C90B028B7C; for Halszkaraptor, LSID

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dm 0.6 e f 0.4 Mesozoic sp gm 0.2 Non-avialan Non-tetanuran birds tetanurans bipedal dinosaurs 0.75 1.00 1.25 1.50 1.75 2.00 2.25 2.50 2.75 Ratio nger II:I na b Foot propelled Foot-and-wing propelled 0.8 0.4 g h i j 0

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3 Hulsanpes Halszkaraptorinae Mahakala –0.4 Austroraptor Neuquenraptor component –0.8

Wing propelled Buitreraptor Unenlagiinae

Unenlagia comahuensis 1 3 –1.2 Unenlagia paynemili 1 Surface swimmer Shanag 1

Principa l Zhanjuanlong –1.6 Microraptor

Sinornithosaurus –2.0 3 4 Changyuraptor Microraptorinae 4 Plunger Hesperonychus 4 –2.4 Halszkaraptor Graciliraptor NGMC91 Non swimmer Bambiraptor –2.8 Tianyuraptor Achillobator –0.8 –0.4 0 0.4 0.8 1.2 1.6 2.0 2.4 Dromaeosaurus Utahraptor Principal component 2 Eudromaeosauria 2 Adasaurus 2 Deinonychus 2 Saurornitholestes Figure 4 | Morphometric analyses of aquatic adaptations in the Velociraptor Linheraptor Halszkaraptor forelimb. a, Binary plot of length ratios among manual Tsaagan digits I–III in aquatic and terrestrial sauropsids (n = 84): Halszkaraptor clusters with long- necked aquatic reptiles. b, Binary plot of principal Figure 3 | H. escuilliei phylogenetic affinities and comparisons components 2 and 3 from a morphometric analysis of ten skeletal for its unique postcranial features. a–e, Dromaeosaurid synapomorphies in characters of the forelimb and sternum in birds (n = 246; principal Halszkaraptor. a, Skull in occipital view. fm, foramen magnum; component 1 describes body size variation and is therefore not po, postorbital; pf, enlarged paraquadrate fenestra. b, Premaxilla and considered; see Supplementary Information): Halszkaraptor clusters with maxilla in lateral view. ep, elongate pre -antorbital part of maxilla; mf, wing-propelled swimming birds. Silhouettes in a provided by D. dorsally placed maxillary fenestra. c , Mandible in lateral view. dm, Bonadonna and L. Panzarin. dentary ventral and dorsal margins subparallel. d, Dentary tooth in lingual view. cd, concave distal margin of crown; ub, unconstricted crown base. e, Neck in ventrolateral view. na, neural arch extended to level of intercentral facet. f , Feet in extensor view. gm, ginglymoidal distal end of metatarsal 6. Massare, J. A. Swimming capabilities of Mesozoic marine reptiles: II; sp, short and stout phalanges of second toe. g, Phylogenetic position of implications for method of predation. Paleobiology 14, 187–205 (1988). 7. Meylan, P. A. Skeletal morphology and relationships of the early Halszkaraptor among Maniraptora, on the basis of parsimony analysis Cretaceous side-necked turtle, Araripemys barretoi (Testudines: 30 22 using TNT software on two independently developed datasets (for Pelomedusoides: Araripemydidae), from the Santana Formation of complete topologies and tree statistics, see Supplementary Information). h– Brazil. J. Vertebr. Paleontol. 16, 20–33 (1996). j, Dorsal view of anterior cervical vertebrae of Cygnus (h), the fresh- water 8. Charig, A. J. & Milner, A. C. Baryonyx walkeri, a fish-eating dinosaur from the 7 Wealden of Surrey. Bull. Nat. Hist. Mus. Lond. (Geol.) 53, 11–70 (1997). chelonian Araripemys (i) and Halszkaraptor (j). These vertebrae share a 9. Caldwell, M. W. From fins to limbs to fins: limb evolution in fossil combination of features: marine reptiles. Am. J. Med. Genet. 112, 236–249 (2002). (1) elongate neural arches with reduced ridge-like neural spines; 10. Thewissen, J. G. M. & Taylor, M. A. in Fins into Limbs: Evolution, Development, and (2) merged postzygapophyses that form a lobate process; (3) ribs fused Transformation (ed. Hall, B. K.) 310–322 (Univ. Chicago Press, 2007). 11. Habib, M. The structural mechanics and evolution of aquaflying birds. Biol. to vertebra; and (4) horizontally oriented zygapophyseal facets. Scale J. Linn. Soc. 99, 687–698 (2010). bars, 9 mm (a, c), 3 mm (b); 1 mm (d) and 30 mm (e, f). 12. Foffa, D., Sassoon, J., Cuff, A. R., Mavrogordato, M. N. & Benton, M. J. Complex rostral neurovascular system in a giant pliosaur. Naturwissenschaften 101, 453–456 (2014). Online Content Methods, along with any additional Extended Data display items and 13. Barker, C. T., Naish, D., Newham, E., Katsamenis, O. L. & Dyke, G. Source Data, are available in the online version of the paper; references unique to these Complex neuroanatomy in the rostrum of the Isle of Wight theropod sections appear only in the online paper. Neovenator salerii. Sci. Rep. 7, 3749 (2017). 14. Kear, B. P., Larsson, D., Lindgren, J. & Kundrát, M. Exceptionally prolonged tooth received 21 August; accepted 1 November 2017. formation in elasmosaurid plesiosaurians. PLoS ONE 12, e0172759 (2017). Published online 6 December 2017. 15. Osmólska, H. Hulsanpes perlei n.g. n.sp. (Deinonychosauria, Saurischia, Dinosauria) from the Upper Cretaceous Barun Goyot Formation of 1. Gauthier, J. Saurischian monophyly and the origin of birds. Memoirs Cal. Mongolia. Neues Jahrb. Geol. Paläontol. Monat. 7, 440–448 (1982). Acad. Sci. 8, 1–55 (1986). 16. Turner, A. H., Pol, D. & Norell, M. A. Anatomy of Mahakala omnogovae 2. Witmer, L. M. in Mesozoic Birds: Above the Heads of Dinosaurs (eds (Theropoda: Dromaeosauridae), Tögrögiin Shiree, Mongolia. Am. Mus. Chiappe, L. M. & Witmer, L. M.) 3–30 (Univ. California Press, 2002). Nov. 3722, 1–66 (2011). 3. Xu, X., Tan, Q., Wang, J., Zhao, X. & Tan, L. A gigantic bird-like dinosaur 17. Turner, A. H., Makovicky, P. J. & Norell, M. A. A review of from the Late Cretaceous of China. Nature 447, 844–847 (2007). dromaeosaurid systematics and paravian phylogeny. Bull. Am. Mus. 4. Holtz, T. R. Jr. The arctometatarsalian pes, an unusual structure of Nat. Hist. 371, 1–206 (2012). the metatarsus of Cretaceous Theropoda (Dinosauria: Saurischia). J. 18. Osmólska, H., Roniewicz, E. & Barsbold, R. A new dinosaur, Gallimimus Vertebr. Paleontol. 14, 480–519 (1995). bullatus n. gen., n. sp. (Ornithomimidae) from the Upper Cretaceous of 5. Zanno, L. E. & Makovicky, P. J. Herbivorous ecomorphology and Mongolia. Palaeontol. Pol. 27, 103–143 (1972). specialization patterns in theropod dinosaur evolution. Proc. Natl Acad. 19. Balanoff, A. M. & Norell, M. A. Osteology of Khaan mckennai (Oviraptorosauria: Sci. USA 108, 232–237 (2011). Theropoda). Bull. Am. Mus. Nat. Hist. 372, 1–77 (2012)

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Supplementary Information is available in the online version of the paper. 20. Xu, X. et al. A bizarre Jurassic maniraptoran theropod with preserved evidence of membranous wings. Nature 521, 70–73 (2015). Acknowledgements We thank the European Synchrotron Radiation Facility for 21. Ostrom, J. H. Osteology of Deinonychus antirrhopus, an unusual theropod granting us beam time at ID19 and BM05 beamlines; Y. Pommery for his work on from the Lower Cretaceous of Montana. Peabody Mus. Nat. Hist. Bull. 30, teeth segmentation; T. Hubin for photographs; A. Halamski and D. 1–165 (1969). Madzia for information on Hulsanpes holotype; and M. Auditore for the skeletal 22. Cau, A., Brougham, T. & Naish, D. The phylogenetic affinities of the bizarre reconstructions. U. Lefèvre and L. Van Bossuyt took conventional X-ray pictures at the Late Cretaceous Romanian theropod Balaur bondoc (Dinosauria, Veterinary School of Liège University. Silhouettes in Fig. 4a were provided by D. Maniraptora): dromaeosaurid or flightless bird? PeerJ 3, e1032 (2015). Bonadonna and L. Panzarin and are used with their permission. The program TNT 23. Gianechini, F. A., Makovicky, P. J. & Apesteguía, S. The teeth of the was made available by the sponsorship of the Willi Hennig Society. unenlagiine theropod Buitreraptor from the Cretaceous of Patagonia, Argentina, and the unusual dentition of the Gondwanan dromaeosaurids. Author Contributions A.C. and P.G. designed the project. P.G. supervised the Acta Palaeontol. Pol. 56, 279–290 (2011). preparation of the specimen. P.T., V.B., D.F.A.E.V. and V.F. performed 24. Xing, L. et al. Piscivory in the feathered dinosaur Microraptor. synchrotron scanning, data processing and segmentation, and created the 2D Evolution 67, 2441–2445 (2013). and 3D renderings. K.S. conducted the histological analysis. R.B., K.T. and 25. Carpenter, K., Sanders, F., Reed, B., Reed, J. & Larson, P. Plesiosaur P.J.C. provided information on Mongolian theropods and geological setting. A.C. swimming as interpreted from skeletal analysis and experimental results. conducted the phylogenetic analyses. A.C. wrote the manuscript with input from Trans. Kans. Acad. Sci. 113, 1–34 (2010). all other authors. 26. Senter, P. Comparison of forelimb function between Deinonychus and Bambiraptor J. Vertebr. Paleontol. (Theropoda: Dromaeosauridae). 26, Author Information Reprints and permissions information is available at

897–906 (2006). www.nature.com/reprints. The authors declare no competing financial interests. 27. Ribak, G., Weihs, D. & Arad, Z. How do cormorants counter buoyancy Readers are welcome to comment on the online version of the paper. during submerged swimming? J. Exp. Biol. 207, 2101–2114 (2004). Publisher’s note: Springer Nature remains neutral with regard to jurisdictional 28. Hutchinson, J. R. The evolution of femoral osteology and soft tissues on the claims in published maps and institutional affiliations. Correspondence and line to extant birds (Neornithes). Zool. J. Linn. Soc. 131, 169–197 (2001). requests for materials should be addressed to A.C. ([email protected]). 29. Gatesy, S. M. & Dial, K. P. Locomotor modules and the evolution of avian flight. Evolution 50, 331–340 (1996). Reviewer Information Nature thanks T. Holtz Jr and the other anonymous 30. Goloboff, P., Farris, J. S. & Nixon, K. C. TNT, a free program for reviewer(s) for their contribution to the peer review of this work. phylogenetic analysis. Cladistics 24, 774–786 (2008).

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Extended Data Figure 1 | Example of data processed with texture section along the longitudinal axis of the cranium on dataset corrected for enhancement and metallic-inclusion correction algorithms. a, Virtual metallic inclusions. f, Detail of e. g, Same virtual section as in e, on data section or the original dataset. b, Detail of a. c, Virtual section from the processed with the texture enhancement algorithm. h, Detail of g. In the dataset corrected for metallic inclusions. d, Detail of c. Histograms along processed data (g, h), homogenous parts (for example, bone or plaster) the blue and red lines demonstrate how metallic inclusions prevent adjusting appear dark and the sediment reveals features that were barely visible the contrast to focus on the bone–matrix contact. e, Virtual prior to processing (e, f).

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Extended Data Figure 2 | Sectional slices that illustrate the integrity of matrix along main slab. e, Overview of MPC-D102/109 indicating the MPC-D102/109. a, Detail of anterior end of neck and posterior half of skull curved virtual slice along a polyline (materialized above a 3D rendering) that shows continuity of the craniocervical transition. b, Detail of neck and with slices at 5 mm on each side of this line every 1 mm. The line follows skull that shows continuity between bones and matrix. c, Detail of proximal the axial column in order to show the continuity of the vertebral series. caudal series that shows the glued crack that crosses both matrix and bone Scale bar, 70 mm. The renderings are generated using scan data that have (arrow), which confirms continuity between the sacrum and tail. d, Selected been corrected for the absorbing metallic oxide infilling. series of slices that show the continuity of bones and

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Extended Data Figure 3 | Cross-sectional slices that illustrate the integrity of the left manus in MPC-D102/109. a, Overview of MPC- D102/109 that indicates the location (red line) of the virtual sample for the slice shown in b. b, Dorsoventral cross-section of p2-I, p1-II and mc III; referred elements were stabilized close to their original position as indicated by the proximity of p2-I (grey arrow) to a small splint of p2-I that remained in the matrix (white arrow). Coloured lines indicate transects shown in c (blue), d (green) and e (purple). c, Mediolateral cross- section of manus with restored p2- I (grey arrow) indicated. d, Mediolateral cross-section of manus with in situ splint of p2-I (white arrow) indicated. e, Ventromedial–dorsolateral cross-section of manus with in situ splint of p2-I (white arrow) indicated. Scale bars, 20 mm. Sections in b–e were extracted from the dataset with an isotropic voxel size of 53.58 μm and volume reconstruction that followed a phase retrieval approach; b represents a single slice extracted from the digital volume and c–e were obtained through the thick-slab mode, with slab thickness set to 0.8 mm in ‘Maximum’ combine mode (VGStudio MAX 2.2.6, Volume Graphics).

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Extended Data Figure 4 | Cross-sectional slices reveal the consistent presence of a single line of arrested growth in the mandible and appendicular skeleton of MPC-D102/109. a, Longitudinal sections of skull (left) and left mandibular ramus (right) of MPC-D102/109 that indicate the locations of the virtual samples for slices shown in b (blue) and c (red). b, Transverse section of left mandibular ramus. c, Longitudinal cross-section of left mandibular ramus in dorsoventral plane. d, Cross- section of left humerus at mid-shaft. e, Cross-section of right femur shaft. f, Cross-section of left femur shaft. g, h, Cross-sections of right tibia distal shaft. i, Cross-section of left tibia proximal shaft. j, Cross-section of right metatarsal IV proximal shaft. White arrows indicate lines of arrested growth (LAGs). Scale bars, 2 mm (a–c), 0.8 mm (d), 1 mm (e–h) and 0.9 mm (j). Sections in a–c were extracted from the dataset with an isotropic voxel size of 2.25 μm, and volume reconstruction that followed a phase retrieval approach, as single slices in VGStudio MAX 2.2.6. The section in d was extracted from the dataset with an isotropic voxel size of 2.2 μm and volume reconstruction that followed a phase retrieval approach, and then recoded for improved contrast with the thick-slab mode set to 100 μm in the ‘minimum’ combine algorithm of VGStudio MAX 2.2.6. Sections in e–j were extracted from the dataset with an isotropic voxel size of 53.58 μm and volume reconstruction that followed a phase retrieval approach, with the thick-slab mode set to 100 μm in the ‘minimum’ combine algorithm of VGStudio 3.0.2.

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Extended Data Figure 5 | Histology of MPC-D102/109 left tibia and fibula. a, Interpretative histological drawing of tibia and fibula. b, Photomicrograph under cross-polarized light of boxed area in a. c, Cortical bone of the tibia under cross-polarized light with lambda waveplate, which reveals a LAG. d, Cortical bone of the tibia under cross-polarized light with lambda waveplate; this cross-section shows clearly the sharp cementing line boundary between the innermost remodelled and the outermost primary cortex. e, Close-up of the boxed area in d , with primary parallel-fibred bone with predominantly longitudinal canals and one LAG (white arrow) indicated. The cementing line that separates the outermost primary from the innermost remodelled cortex lies directly below the LAG. In the remodelled cortex, woven-bone osteocyte lacunae are visible in the lower left corner. No outer circumferential lamellae are visible. f, Close-up of the boxed area in d, with remodelled bone (black arrow) indicated. Several of the secondary osteons are surrounded by woven-bone osteocyte lacunae. A patch of inner circumferential lamellae is visible in the lower left corner. In panels a and d, b–f refer to their corresponding panels in the figure. Scale bars, 2 mm (a), 0.85 mm (b) and 0.35 mm (c–f).

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Extended Data Figure 6 | 3D rendering of preantorbital part of the skull naris; mr, maxillary recess; pms, premaxillo-maxillary suture. e, Semi- of MPC-D102/109. a, Dorsal view. b, Palatal view. p11, 11th premaxillary transparent right lateral view that shows dentition. f , Right lateral view. en, tooth; m16, 16th maxillary alveolus. c, Semi -transparent left lateral view that external naris; nf, neurovascular foramina. Scale bars, 3 mm. shows dentition. d, Left lateral view. af, antorbital fossa; en, external

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Extended Data Figure 7 | 3D rendering of dentition of MPC-D102/109. a, Premaxillary teeth in labial view. b, Premaxillary teeth in lingual view. c, Maxillary teeth in labial view. d, Maxillary teeth in lingual view. e, Maxillary teeth in basal view. f, Dentary teeth in lingual view. rt, replacement tooth. Scale bars, 1 mm.

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Extended Data Figure 8 | Comparison between synchrotron scan branch of the trigeminal nerves (red) in the snouts of a two-year-old segmentations of the snouts of Crocodylus niloticus and H. escuilliei. a– C. niloticus (a, b), a twenty-year-old C. niloticus (c, d) and H. escuilliei f, Synchrotron scan segments that show the enlarged bony chambers that MPC-D102/109 (e, f). Dorsal (a, c, e) and lateral views (b, d, f) are house the blood vessels and the rostral terminations of the maxillary shown. Scale bar, 1.5 mm (a, b, e, f), 10 mm (c, d).

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Extended Data Figure 9 | Strict consensus of the shortest trees found Hulsanpes and Shanag were pruned. DROMAEOSAUR., Dromaeosauridae; by the analysis of first dataset. a, Non-paravian taxa. b, Paraves. EUDRO., Eudromaeosauria; HALSZKAR., Halszkaraptorinae; MICROR., Numbers adjacent to nodes indicate decay index values >1 calculated when Microraptorinae; UNENLAG., Unenlagiinae.

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Extended Data Figure 10 | Reduced strict consensus of the shortest trees found by the analysis of the second dataset. a, Non-pennaraptoran taxa; b, Pennaraptora. Numbers adjacent to nodes indicate decay index values >1.

Chapter V

Geometric morphometrics analysis and

cerebral information reflecting evolutionary history of archosaurs and

development of flight

I-Geometric morphometrics and applications in paleontology

Geometric morphometrics is a set of methods of conformation, which include shape and size.

These methods can be applied on all or parts of organisms in order to observe intra- (Perez et al.

2006, Cordero-Estrela et al. 2006, Kaliontzopoulou et al. 2010) and inter-specific variations (Neige and Boletzky 1997, Klingenberg and Ekau 1997), as well as visualising shape modifications of ontogenetic series (Rohlf 1998, Mitteroecker et al. 2005). Several methods, in either two- and three- dimensions, are used for quantifying shape of an object. The main way used in the following results of this chapter is landmarks based analysis with performance of procrustes fits.

The fact that brains are not only an entire entity but also an addition of structure that coevolve together, studying this organ requires general measurements on the brain itself. Volumes variation is usually the most common topic studied (Rogers 1999, Larsson et al. 2000, Brochu 2000, Witmer et al. 2008,), but neuroanatomical studies also requires the addition of information of brain shape changes of the different cerebral components (Larsson et al. 2000, Witmer et al. 2003, Alonso et al.

2004, Burish et al. 2004) and their relation with other brain areas as well as skull structures

(Richtsmeier et al. 2006, , Hu et al. 2009, Marcucio et al. 2011, Richtsmeier and Flaherty 2013,

Koyabu et al. 2014, Fabbri et al. 2017). As such, the use of three-dimensional geometric morphometrics methods are largely used for understanding these changes and how they influence the ecology of the animals (Hopson 1977, Witmer et al. 2003, Burish et al. 2004, Rogers 2005,

Witmer 2008, 2009,).

The main aim of the studies realised in the following chapter and in chapter 6 is to understand which mechanisms occurred within archosaurian groups and how these changes were related to behavioural modifications in extant and extinct, with a major focus on the evolution of their flying abilities.

II-Three-dimensional geometric morphometric analysis

The dataset for this analysis consisted in 193 specimens of extant bird species. The majority of the specimens were scanned at the ESRF and at the Institute of Clinical and Experimental

Medicine (IKEM, Prague, Czech Republic). These dataset were supplemented with data provided by Digimorph. As the main aim of this analysis was to understand the relationship between cerebral shape and flight abilities, two pterosaurs (Araripesaurus santanae and Tropeognathus mesembrinus) and the London specimen of Archaeopteryx were also included in this dataset. Most of the specimens were only represented by their skulls, which only allowed for endocranial observation. Heads of specimens still preserving their soft tissues were submitted to K-edge and bi- energy scanning technics (See Chapter 2), but the data from brains were not used for the morphometrics study. They were used primarily for checking that endocasts are in good accordance with brain morphology in birds. Endocasts from scanned specimens were segmented and visualised using VGStudio Max 2.2 (Volume Graphics GmbH, Germany).

27 homologuous landmarks and 3 semilandmarks (landmarks 8-9-21) were digitized on each endocast (Table IV-1), using a 3D landmark editor developed using Open Inventor by Dr. Jiří

Janáček from the department of Physiology and Biomathematics, Prague, Czech Republic. The 3D landmarks were selected in order to separate the four main structures of the brain (cerebrum, optic tectum, cerebellum and medulla oblongata), to visualise how the changes of a structure influence and is influenced by the other ones (Figure IV-1). Defining the boundaries of endocranial structures can be a difficult task as by using the endocast we cannot access the internal structures of the brain, as endocranial boundaries does not necessarily reflect the anatomical limits of the structures.

Luckily, as the endocast of birds are really representative of the real brain shape (Iwaniuk and

Nelson 2002, present study using bi-energy with contrast agent), we can consider that the definition of the structures based on the endocast are accurate. The 3D landmarks coordinates were subjected to Generalised Procrustes fit (Rohlf and Slice 1990) using MorphoJ package software (Klingenberg

2011). Generalised Procrustes fit are used for minimising distances between landmarks by translating, rotating and scaling the set of landmarks to a single reference, common to all of the specimens. The aim is to remove effects of size and orientation in order to only preserve information related to shape. The only size information preserved is the centroid size (Bookstein 1991), size information removed are isometric effects.

The use of Procrustes alignment scale all the specimen to similar size but does not remove the effect of size on shape variation. As such, any geometric morphometric analysis will express shape and size variation as an output. When the study is only about shape variation, it is necessary to exclude this size effect in order to only preserve the signal related to shape changes independent of size. A way to take out this effect is to use size-adjusted dataset, based on the regression between

Symmetric component of the shape and a size index such as Centroid size or its log-transformed expression (Rohlf and Bookstein 1987) (Figure IV-2).

Figure IV-1. 3D geometric morphometric landmarks positions on a bird endocast

(Ephippiorhynchus senegalensis). The endocast is presented in lateral (A), posterior (B) and ventral view (C). Coloured areas represent the main cerebral areas, telencephalon (orange), optic tectum (red), cerebellum (yellow) and medulla oblongata (green).

Landmark Definition of the landmarks

1 Median anterior tip of the telencephalon

2 Median junction between telencephalon and cerebellum

3 Median dorsal point of foramen magnum

4 Median ventral point of foramen magnum

5 Median junction between hypophysis and mesencephalon

6 Median junction between optic nerve and hypophysis

7 Median junction between telencephalon and optic nerve

8* Perpendicular at midpoint between landmarks 1 and 2 to dorsal margin of the

telencephalon in lateral view, right

9* Perpendicular at midpoint between landmarks 2 and 3 to dorsal margin of cerebellum

in lateral view

10* Perpendicular at midpoint between landmarks 4 and 5 to ventral margin of

mesencephalon in lateral view

11 Median ventral tip of hypophysis

12 Intersection of telencephalon, optic lobe and diencephalon, right

13 Intersection of telencephalon, cerebellum and optic lobe, right

14 Intersection of cerebellum, myelencephalon and optic lobe, right

15 Intersection of optic lobe, myelencephalon and diencephalon, right

16 Posterior intersection of cerebellum and myelencephalon, right

17 Dorsal root of flocular lobe, right

18 Ventral root of flocular lobe, right

19 Most lateral point of the widest part of telencephalon, right

20 Most lateral point of the widest part of the optic lobe, right

21 Perpendicular at midpoint between landmarks 0 and 1 to dorsal margin of the

telencephalon in lateral view, left

22 Intersection of telencephalon, optic lobe and diencephalon, left

23 Intersection of telencephalon, cerebellum and optic lobe, left

24 Intersection of cerebellum, myelencephalon and optic lobe, left

25 Intersection of optic lobe, myelencephalon and diencephalon, left

26 Posterior intersection of cerebellum and myelencephalon, left

27 Dorsal root of flocular lobe, left

28 Ventral root of flocular lobe, left

29 Most lateral point of the widest part of telencephalon, left

30 Most lateral point of the widest part of the optic lobe, left

Table IV-1. List of 3D landmarks used in the geometric morphometric analysis. Numbers refers in the order of positioning on the surface of the endocast and will be use to refer to the corresponding landmarks and the following description of the results and discussion. * indicates constructed landmarks.

Figure IV-2. Bivariate plot of the regression between symmetric components based on 3D landmarks visualisation versus log-transformed centroid size of the bird dataset. Residuals of this regression were used as size-free dataset.

A strong relationship is observed between size and shape (p-value<0,001), size explaining

6.96% of shape variation. The fact that a significant allometric relationship is explaining part of the shape variation is a key aspect to address before going into further investigation is to describe which parameters can also influence shape variation within birds. We then need to adress if one of this parameters can help replacing extinct flying archosaurs (such as Archaeopteryx and Pterosauria) and trying to assess their behaviour. Two other important parameters that have been considered for influencing brain shape within birds, in addition with size, are phylogenetic effect (Charvet and

Striedter 2009, Kawabe et al. 2014, Wylie et al. 2015) and behavioural aspects (Garamszegi et al.

2007, Hall and Ross 2007,Hall et al. 2013, Carril et al. 2015).

Size-free residuals of the regression were subsequently submitted to Principal Components Analysis in order to have a first overview of signal related explanation of the brain shape (Figure IV-3).

Principal Component 1 represents 33% of the information whereas Principal Component 2 explain

27% of the variation. Fossil specimen like Archaeopteryx and pterosaurs were used as additional specimen and they do not participate to the realisation of the PCA.

Figure IV-3. Plots of the Principal Components Analysis (PCA) of the brain shape of modern birds, Archaeopteryx and pterosaurs as supplementary individuals. Coloured hulls represent phylogenetic taxa.

The results of the PCA express unseparated phylogenetic and behavioural signal.

Accipitriformes, except Cathartidae, and Falconiformes, which are phylogenetically phylogenetically independent are related together in the PCA plot. This can be explained by their common hunting behaviour, as both are diurnal hunter in flight. Cathartidae, even if they are members of Accipitriformes, are separated from their relatives, as a consequence of their dietary changes compare to other Accipitriformes, because Cathartidae are scavengers. The flight mode might also play a role in this separation as other Accipitriformes are active flyers contrary to

Cathartidae, which are passive gliders.

Phylogenetically related to Accipitriformes, Strigiformes are separated from them. The major shape change between these two groups are based on the expansion of the wulst in Strigiformes, that might be explained by the luminosity conditions in which these groups are hunting.

Accipitriformes are mainly diurnal birds of prey where as Strigiformes are nocturnal predators.

Another point aiming to justify these relations between wulst hyperdevelopment and nocturnal behaviour is that Caprimulgiformes (only represented by Podargus strigoides) are plotting within the hull of Strigiformes. These two groups are not usually considered as phylogenetically related

(Prum et al. 2015), even if some studies have made them closely related (Sibley and Ahlquist 1990,

Livezey and Zusi 2001) but present the same nocturnally hunting mode of predation and as such may have experienced evolutionary convergence, leading to highly expanded wulst, which might improve vision in a low light environment. It also seems that this wulst enlargement might have been related to the increase of stereoscopic vision in both groups (Iwaniuk and Wylie 2006).

Paleognathae are not plotting together with in the PCA plots but are separated all along the plot. This group present a large variety of brain shape (see Chapter 6), which can be a consequence of their behavioural diversification, size increase and maybe the conservation of cognitive abilities of their direct flying ancestors by preservation of their brain shape. Archaeopteryx and Pterosauria are plotting quite far from extant birds, which can express either the phylogenetic distance between these groups or differences in behaviours.

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Figure IV-4. Variation in brain shape in Principal Components (PC). Only shape variation in

PC1 (a) and PC2 (b) are represented. Brains are divided in three main areas: Telencephalon (orange),

optic tectum (red) and rhombencephalon (cerebellum and medulla oblongata, yellow).

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Principal Component 1 (Figure IV-4a) express an increase of the coiling of the brain, as a consequence of an antero-posterior flattening of the telencephalon, which tend to be more posterior but with a dorsal expansion (that might be related to the increase of the size of the wulst).

Rhombencephalon experienced a ventro-dorsal rotation, with the foramen magnum getting more posterior prior to the rest of the brain and in addition with an anterior displacement of the optic tectum associated with a decrease of its size. Principal Component 2 (Figure IV-4b) present a lateral compression of the telencephalic hemispheres associated with a posterior extension of the optic tectum which causes the elongation of the brain by pushing more posteriorly the cerebellum. In general, bird brain changes are related to variation in telencephalic expansion, mainly due to dorsal expansion, in relation with wulst enlargement. The antero-posterior movement of the optic tectum seems to be related to size variations. Rotation of the cerebellum is causing modification of the position of the foramen magnum (also influenced by, or influencing the neck to skull joint at the foramen magnum), which should reflect variation in head posture or general body posture.

Phylogenetic effect has been tested by mapping scores of the Principal Components Analysis on the phylogeny of birds. This mapping has been realised at the species (Figure IV-5a) and order

(Figure IV-5b) levels. Mapping and statistical inference of the phylogenetic signal have been realised on MorphoJ (Klingenberg 2011). The phylogeny used for such comparison was based on general phylogenies (Prum et al. 2015) for the order level and more specialised phylogenies for the species level (Wink 1995, Livezey 1996, Donne-Goussé et al. 2002, Barker et al. 2004, Lovette and

Rubenstein 2007, Arnaiz-Villena et al. 2009, Gelang et al. 2009, Wink et al. 2009, Smith and Clark

2011, Smith 2011, Haring et al. 2012, Ramirez et al. 2012, Gonzalez et al. 2013). Phylogenies from literature were supplemented with trees from the Tree of Life (Maddison and Schulz 2009). Results of phylogenetic tests for species (p-value<0,0001) and order level (p-value=0,0006) suggest the

102 existence of an important phylogenetic signal on brain shape variation. This signal has not been fully quantified during the time of this thesis.

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Figure IV-5. Phylogenetic relationships plotted against PC scores of Principal Components 1 and 2 at the species and order level. Phylogenetic trees were mapped on PC scores for species (a) and order (b) levels.

A previously observed, specimens subjected to PCA are forming groups that seemed to be related to their common behaviours (Figure IV-3). To test this behavioural and ecological relationships between taxa, PC scores were submitted to Linear Discriminant Analysis (LDA), after defining two main series of groups based on flying abilities on one hand and on their dietary behaviours on the other hand. Mahalanobis and Procrustes distances were used to statistically characterise significant differences between selected groups. Mahalanobis distances are measuring the distance between a point, representing a specimen and the distribution of points in which this specimen is included, by calculating the mean of the distribution and calculating the standard deviation of the specimen from this mean. When the specimen is at the mean along the principal component, so the distance is equal to 0. The further the specimen differ from the mean, the higher the distance increase (Mahalanobis 1936). This can be generalised by considering how the specimen differs from the others. Procrustes distances are defined as the distance between shapes of specimens after processing Procrustes superimposition (Small 1996). This distance is calculated by the sum of the distance between homologuous landmarks of two shapes and might be considered as an index for visualising the magnitude of shape changes. All the graphical and statistical output following have been performed using Past 3.0 (Hammer et al. 2001).

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Figure IV-6. Graphical representation of the Linear Discriminant Analysis of three-

dimensional shapes discriminated by flight modes. With 80% of the information, only LDA axis

1 versus axis 2 (a) and axis 1 versus axis 3 (b) were considered. Convex hull represent the dispersion

of specimen of each flying groups (flap gliding in red, soaring in purple, burst in orange, non volant

bipedal in brown, non volant diving in dark blue and continuous flap in green). Red stars represent

105 fossil specimen secondarily included in the graph, Archaeopteryx, Araripesaurus and

Tropeognathus.

Six flight modes were defined for characterising locomotion styles within birds, with continuous flappers, flap gliders, non-volant bipedals, non-volant divers, burst flyers and soarers.

All specimens were associated to one of the subgroups previously defined, except Archaeopteryx and the two Pterosauria. By not including directly in this analysis, the aim was to consider them as objects with missing information and to check on which of the pre-existing sub-groups they were mainly associated. The first three axis were retained as the express 80% of the information

(respectively 40,8% 24,7% and 14,5%). The graphical representation of the LDA tend to suggest that there is no clear separation between flight modes (Figure IV-6).

Burst Continuous Flap Flap Gliding NV Bipedal NV Diving

Continuous Flap 3,4443 (<.0001) Flap Gliding 3,1292 2,6494 (<.0001) (<.0001) NV Bipedal 5,0317 4,1155 4,0732 (<.0001) (<.0001) (<.0001) NV Diving 5,4136 4,1549 4,4366 5,2037 (0,0001) (<.0001) (<.0001) (0,0054) Soaring 4,6957 4,0591 3,1429 4,5080 4,9612 (<.0001) (<.0001) (0,0003) (0,0004) (0,0053) Table IV-2. Mahalanobis distances between flight modes. P-value obtained after 10.000 permutations are presented between parenthesis.

Mahalanobis (Table IV-2) and Procrustes (Table IV-4) distances tend to confirm the low significant differences of brain morphology between the different flight modes. These distances between groups are generally highly significant.

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Burst Continuous Flap Flap Gliding NV Bipedal NV Diving Continuous Flap 0,1103 (<.0001) Flap Gliding 0,0952 0,0976 (<.0001) (<.0001) NV Bipedal 0,0865 0,1021 0,0889 (0,0099) (0,0187) (0,0490) NV Diving 0,1141 0,0920 0,1126 0,0942 (0,0001) (0,1285) (0,0193) (0,1360) Soaring 0,1004 0,1142 0,0783 0,0773 0,0917 (0,0003) (0,0026) (0,0833) (0,3158) (0,0815)

Table IV-3. Procrustes distances between flight modes. P-value obtained after 10.000 permutation tests are presented between parenthesis.

Except along Axis 1, where both Pterosauria are classified as continuous flaps (Figure IV-

6a), extinct specimens of the dataset are systematically placed out of any hulls, which might reflect different flight styles than extant specimens of the dataset (but the fact that flight modes are not clearly segregated in the graphical output cannot significantly support or go against this assertation).

Another explanation can be related to their phylogenetic position, outside the avian lineage, but such assertation might need the use of other archosaurian sample, like dinosaurs and crocodiles in order to verify the position of these extinct specimen within tan archosaurian behavioural trend.

107 a

Figure IV-7. Graphical representation of the Linear Discriminant Analysis of three- dimensional shapes discriminated by dietary strategies. With 63,6% of the information, only

LDA axis 1 versus axis 2 (a) and axis 1 versus axis 3 (b) were considered. Convex hulls represent the dispersion of specimen of each flying groups (subaquatic piscivorous in dark blue, wading in dark green, aquatic herbivorous in cyan, scavengers in dark red, diurnal hunter in light red, volant insectivorous in yellow, Aquatic piscivorous in purple, arboreal omnivorous in green, seedivorous

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in orange, terrestrial omnivorous in dark pink, terrestrial hunter in brown, arboreal frugivorous in

light green and nocturnal hunter in red). Red stars represent fossil specimen secondarily included in

the graphe, Archaeopteryx, Araripesaurus and Tropeognathus.

1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12.

2.Aquatic 5,23 (0,05) Piscivorous

3.Arboreal 5,55 5,59 (<.000 (0,006 Frugivorous 1) 7)

4.Arboreal 5,33 5,45 4,24 (<.000 (0,075 (<.000 Omnivorous 1) 4) 1)

5.Diurnal hunter 7,53 6,32 6,68 7,15 (<.000 (0,005 (<.000 (<.000 1) 9) 1) 1) 6.Nocturnal Hunter 7,95 6,97 6,38 7,47 7,34 (<.000 (0,019 (<.000 (0,000 (<.000 1) 6) 1) 2) 1) 7.Scavenger 6,11 4,78 5,96 5,82 4,69 6,84 (<.000 (0,541 (<.000 (0,001 (0,002 (0,000 1) 8) 1) 2) 5) 4) 8.Seedivorous 6,58 7,27 5,75 4,96 7,85 7,65 6,81 (0,007 (<.000 (0,000 (0,166 (0,000 (0,009 (0,031 2) 1) 7) 1) 6) 7) 6) 9.Subaquatic 4,93 4,23 5,55 5,15 6,42 7,99 5,07 7,24 (<.000 (0,642 (<.000 (<.000 (<.000 (<.000 (0,000 (0,005 Piscivorous 1) 3) 1) 1) 1) 1) 2) 6)

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10.Terrestrial 6,58 6,30 3,75 4,83 5,66 6,85 5,18 5,63 5,76 (<.000 (0,054 (<.000 (0,000 (<.000 (0,000 (0,010 (0,048 (<.000 Hunter 1) 6) 1) 7) 1) 2) 8) 6) 1)

11Terrestrial 4,80 4,91 3,7 3,50 5,51 6,48 4,71 4,90 4,45 3,37 (<.000 (0,123 (<.000 (<.000 (<.000 (<.000 (0,000 (0,131 (<.000 (0,004 omnivorous 1) 8) 1) 1) 1) 1) 1) 5) 1) 0)

12Volant 6,56 6,27 5,64 5,65 5,54 7,06 6,35 6,62 5,33 5,39 4,72 (<.000 (0,344 (<.000 (0,001 (0,000 (0,000 (0,000 (0,193 (<.000 (0,002 (<.000 Insectivorous 1) 1) 1) 4) 1) 1) 4) 8) 1) 1) 1)

13.Wading 3,72 4,67 5,14 4,99 5,38 7,13 4,29 5,93 4,90 4,96 3,79 6,11 (<.0001) (0,2058) (<.0001) (<.0001) (<.0001) (<.0001) (0,0014) (0,0055) (<.0001) (<.0001) (<.0001) (<.0001) Thirteen dietary strategies were defined for characterising dietary behaviours within the

dataset, with acquatic piscivorous, arboreal frugivorous, arboreal omnivorous, diurnal hunters,

nocturnal hunters, scavengers, seedivorous, subaquatic piscivorous, terrestrial hunters, terrestrial

omnivorous, volant insectivorous and wading. All specimens were associated to one of the

subgroups previously defined, except Archaeopteryx and the two Pterosauria. As for flight modes,

by not including directly in this analysis, the aim was to consider them as objects with missing

information and to check on which of the pre-existing sub-groups they were mainly associated. The

first three axis were retained as the express 63,6% of the information (respectively 26,1% 23,7%

and 13,8%). The graphical representation of the LDA tend to suggest that there is no clear separation

between flight modes (Figure IV-7).

Table IV-4. Mahalanobis distances between dietary strategies. P-value obtained after 10.000 permutation tests presented between parenthesis.

1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12.

2. Aquatic 0,15 (0,05) Piscivorous

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3.Arboreal 0,15 0,11 (<.0001) (0,1828) Frugivorous

4.Arboreal 0,19 0,15 0,10 (<.0001) (0,0732) (0,0020) Omnivorous

5. Diurnal hunter 0,29 0,21 0,21 0,21 (<.0001) (0,0071) (<.0001) (<.0001) 6.Nocturnal 0,25 0,19 0,14 0,14 0,17 (<.0001) (0,0198) (<.0001) (0,0002) (<.0001) Hunter

7. Scavenger 0,21 0,12 0,13 0,14 0,13 0,15 (0,0004) (0,4137) (0,0005) (0,0037) (0,0057) (0,0004) 8. Seedivorous 0,22 0,21 0,17 0,11 0,20 0,18 0,17 (0,0252) (0,3412) (0,0010) (0,2958) (0,0067) (0,0157) (0,0971) 9.Subaquatic 0,17 0,08 0,13 0,14 0,17 0,19 0,10 0,18 (0,0001) (0,6863) (<.0001) (<.0001) (<.0001) (<.0001) (0,0230) (0,0145) piscivorous

10.Terrestrial 0,24 0,15 0,13 0,14 0,13 0,14 0,10 0,19 0,12 (<.0001) (0,0446) (<.0001) (0,0001) (0,0002) (0,0002) (0,0968) (0,0367) (0,0005) Hunter

11.Terrestrial 0,19 0,12 0,10 0,10 0,14 0,15 0,09 0,14 0,08 0,08 (<.0001) (0,2298) (<.0001) (0,0042) (<.0001) (<.0001) (0,0607) (0,0890) (0,0019) (0,1049) omnivorous

12.Volant 0,27 0,22 0,21 0,18 0,10 0,17 0,16 0,16 0,17 0,16 0,14 (<.0001) (0,0336) (<.0001) (<.0001) (0,0001) (0,0001) (0,0262) (0,1558) (<.0001) (0,0009) (0,0006) insectivorous

13. Wading 0,12 0,08 0,10 0,14 0,19 0,18 0,11 0,18 0,09 0,14 0,09 0,19 (0,0002) (0,6753) (<.0001) (<.0001) (<.0001) (<.0001) (0,0365) (0,0161) (0,0014) (0,0013) (<.0001) (<.0001)

Table IV-5. Procrustes distances between dietary strategies. P-value obtained after 10.000

permutation tests are presented between parenthesis.

Dietary groups are poorly discriminated, except for nocturnal hunters. This separation of

nocturnal hunter, which are mainly composed by Strigiformes could be related to the wulst

enlargement observed in this taxa. Distances are contradictory. Whereas Mahalanobis distances

express significant short distances between groups, congruent with what is observed in the graphical

output (Table IV-4, Table IV-5). On the contrary, Procrustes distances are representing long

111 significant distances. It tend to suggest that there are no clear average shape for each behaviour as brain of the specimen of a group tend to be slightly different. This does not allow for any influence of dietary strategies on brain shape. As such, the fact that pterosaurs are presented as subaquatic piscivorous, as auks and penguins, from which they differ in their postcranial anatomy and the fact that Archaeopteryx is placed at the border between aquatic herbivorous and wading birds (contrary to their predicted position in volant insectivorous) does not make this placement being significant.

The relationship between phylogeny, flight mode and dietary strategies have been tested.

Results of the previous analysis have been supplemented to Khi2 test. The results tend to suggest that there is a strong relationship between the three parameters (p-value<2,2e-16), confirming the existence, sometimes short, between the different groups of behaviours previously defined.

As the development of flight abilities is a key step in the evolutionary history of archosaurs

(see Chapter 1), that appeared twice independently in this group, and considering the important cerebral requirements for dealing with such complex behaviours, a focus on the influence of the coevolution between brain shape and flying capabilities. The positioning of Archaeopteryx and the two pterosaurs, generally out of the hulls representing flight modes of modern avian taxa, seems to imply the use of more primitive specimens. This addition of extra fossils and extant dataset might help to understand the transition experienced by brain for reaching the required cognitive capabilities allowing for flight. As such, based on their early position in the phylogeny of archosaurs and comparable brain shape and organisation as what is observed in Lepidosauria, the sister taxa of archosaurs, the brain of crocodilians have been defined as the plesiomorphic status of archosaurian brain.

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As the fossil included in the dataset are intermediate forms on the transition from terrestrial to aerial locomotion mode, such analysis might require to include dinosaurian ancestors of birds.

The main issue is the preservation on dinosaurian endocast. During the taphonomic processes leading to fossilisation bones are experiencing high compression level. As a consequence, braincases and endocast extracted from them can be highly deformed, which does not allow the use of 3D geometric morphometrics for such specimen as non-representative shapes might introduce biases within the dataset. It requires the use of morphometric methods less sensitive to such

deformation.

Figure IV-8. Comparison of positioning of cerebral component between crocodilians and birds. The presented endocast correspond to the crocodilian Crocodylus niloticus (a) and the bird

Ficedula albicollis (b). Colours correspond to different cerebral components (telencephalon-orange, diencephalon-purple, optic tectum-red, cerebellum-yellow, medulla oblongata-green). Coloured dots correspond to the positioning of the landmarks 2 (blue) and 13/23 (green) (Scale bar: a-10 mm, b-1,5 mm).

Another issue addressed by using all of those different groups is the possibility for placing landmarks. Birds and Pterosaurs present the characteristics to have very clearly defined boundaries between brain structures. On the contrary, crocodilians and dinosaurs present very blurred

113 boundaries. In addition with this differential cerebral boundaries definition, the relative position of each cerebral structures is importantly varying. As an example, Landmark 2 (see Table IV-1), define for birds as the dorsal median intersection between cerebrum and cerebellum cannot be defined in crocodilians as the optic tectum is placed between the cerebrum and the cerebellum. This landmark cannot be defined as the posterior median part of the cerebellum, as it will be at the same position as landmarks 13 and 23, placed at the border between cerebrum, optic tectum and cerebellum, which is paired and placed laterally in birds but defined dorsally in crocodilians (Figure IV-8).

Furthermore, clear boundaries between cerebrum, optic tectum and cerebellum cannot be accurately defined which does not permit any accurate visualisation of such landmarks. These morphological differences do not allow for defining homologuous landmarks and as such, does not enable efficient comparison of these groups by applying three dimensional geometric morphometric methods.

Based on this, studying evolution of endocranial shape requires other methods, less sensitive to deformation, and capable of covering very diverse 3D topologies. As deformation are experienced in the three dimensions, a possibility to decrease their influence is to switch to two-dimensional geometric morphometric methods, that will capture shape variation in less dimension and preserve less parasitic signal related to deformation, at least when the major compression axis is lateral. As a consequence, these methods will also preserve only partially the full picture related to shape changes, but at this level, a trade-off between completeness and accuracy of the dataset is required.

In addition, based on the poor definition of cerebral components in some archosaurian taxa, and in order to compare homologuous observation between the different taxonomic groups, these methods might require to observe the general shape modifications of the brain instead of focusing on detailed variation of the different cerebral structures.

As observed in the 3D geometric morphometric analysis, visualisation of shape modifications in lateral view for birds shows variation of the doming of the endocast (Figure IV-4). As this doming

114 seems to change between crocodiles, dinosaurs, Archaeopteryx and modern birds, and considering that birds and pterosaurs seem to present the same level of doming, the question of the role of this coiling effect in the development of cognitive abilities required for flight can be addressed. This is the reason why an outline curve measurements have been defined for quantifying this effect after statiscal validation of the process based on two-dimensional geometric morphometric analysis (see

Chapter 6). Considering that paedomorphosis may have played an important role in the establishment of skull organisation of birds from their dinosaurian ancestor (Bhullar et al. 2012,

2016, Fabbri et al. 2017), and in order to test this effect of paedomorphosis for explaining the evolution of brain shape in Archosauria, the archosaurian dataset have been supplemented with a developmental series of Crocodylus niloticus.

III-Qualitative accuracy of endocranial representativity of brain anatomy

The difference of endocranial representativity over brain shape have been described as an issue for assessing brain shape and a problematic condition for using 3D geometric morphometrics methods as a visualising methods of shape changes within Archosauria, but this variation of representativity is also an important signal for understanding which process where driving cerebral evolution in this group.

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Figure IV-9. Evolution of endocranial representativity in ontogenetic series of C.niloticus.

Specimen are presented at different pre- and post-hatchling developmental level, 24-days embryo

(a), 33-days embryo (b), 41-days embryo (c), 70-days embryo (d), 93-days embryo (e), hatchling

(f), 1 year old juvenile (g), adult (h). a,b,c are brain segmented models, d to h models are endocranial models Scale bar: a-1,5 mm, b-2,5 mm, c-2,5 mm, d-3 mm, e-3 mm, f-2,5 mm, g-2,5mm, h-10 mm.

Endocranial representativity of brain shape in birds have been demonstrated (Iwaniuk et al. 2002).

On the contrary, the same assessment cannot be made in adult crocodiles, as brain is suggested to fill only 50 % of the endocranial cavity (Jerison 2004, Jirák and Janáček 2017), which is suggested to be also the case in non-avian dinosaurs (Hopson 1979) even if real quantification is not possible in this taxa. Based on this, it seems that a decrease of endocranial representativity is matching a decrease of endocranial infilling by the brain. Considering the ontogenetic serie of C.niloticus, a decrease of endocranial representativity along the in ovo development tend to reinforce this assertion

(Figure IV-9).

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The fact that brain and endocast are easily accessible for modern species allow for observation of the brain infilling within the cerebral cavity. A limitation is about the preservation aspects of the speciemns, as the use of formalin and ethanol can cause shrinking of soft tissues and as such can reduce the brain volume leading to misinterpretation. The absence of fully and three dimensionally preserved brain in nonavian dinosaurs does not allow for quantitative assessment of brain infilling, but based on the endocranial representativity as previously defined, it can be suggested that most of the dinosaurs represent an endocranial infilling similar to what is observed in crocodiles.

In addition to endocranial representativity, another aspect that can be observed and used as an evidence of high endocranial infilling is the presence or absence of vascular imprints on the surface of the endocast (Hopson 1979, Hurlburt 1996, Jerison et al. 2001). Such evidences of vascular imprints have been observed only on the telencephalic part in modern birds and Archaeopteryx

(Figure IV-10) as well as in Maniraptoriformes (Russell 1972, Currie 1985, Currie 1995, Osmólska

2004, Norell et al. 2004,). Such vascular expression on the endocranial surface is absent in most of other dinosaurs, except in juvenile theropods (Witmer and Ridgely 2009) but absent in their adult forms. They are observed in some pachycephalosaurids (Lambe 1902, Lambe 1918, Williamson and Carr 2003) but not in all preserved specimens of the same species (Evans 2005). Some hadrosaurid dinosaurs also present vascular imprints on the antero-superior part of their endocast

(Evans 2005). Further investigations on their developmental age must be conducted to discriminate adult to juvenile specimen and check for a relationship between endocranial filling and age.

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Figure IV-10. Preserved evidence of vascular imprints in Archaeopteryx. Vascular imprints in

Phasianus colchicus on endocranial (a) and brain (b) surface (e; scale bars: 2 mm). Vascular imprints of

Archaeopteryx expressed on the endocast surface in the London specimen (c; scale bar: 1.5 mm) and the

Munich specimen (d; scale bar 0.65 mm). White arrows indicate expression of vascular imprints on the cerebral (a) and endocranial (b-c-d) surface.

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Chapter VI Multiphase progenetic development shaped the brain of flying archosaurs

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Multiphase progenetic development shaped the brain of flying archosaurs

Vincent Beyrand1,2, Dennis F. A. E. Voeten1,2*, Stanislav Bureš2, Vincent Fernandez1, Jiří Janáček3,

Daniel Jirák4,5,Oliver Rauhut6, and Paul Tafforeau1

*[email protected]

1 European Synchrotron Radiation Facility, 71 Avenue des Martyrs, CS-40220, 38043 Grenoble

2 Department of Zoology and Laboratory of Ornithology, Palacký University, 17.listopadu.50,

77146 Olomouc, Czech Republic

3 Department of Biomathematics, Institute of Physiology of the Czech Academy of Sciences,

Vídeňská 1083, 142 20, Prague 4, Czech Republic

4 MR Unit, Department of Diagnostic and Interventional Radiology, Institute for Clinical and

Experimental Medicine, Vídeňská 1958/9, 142 21, Prague 4, Czech Republic

5 Institute of Biophysics and Informatics, 1st Medicine Faculty, Charles University, Salmovská 1,

120 00, Prague 2, Czech Republic

6 Department for Earth and Environmental Sciences and geoBioCenter, SNSB-Bayerische

Staatssammlung für Paläontologie und geologie, Ludwig-Maximilian-University Munich, Richard-

Wagner-Str. 10, 80333, Munich, Germany

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Abstract

The growing availability of virtual cranial endocasts of extinct and extant vertebrates has fueled the quest for endocranial characters that discriminate between phylogenetic groups and ecological strategies. We used geometric morphometrics to compare a phylogenetically and ecologically comprehensive data set of archosaurian endocasts along the deep evolutionary history of modern birds and found that this lineage experienced progressive elevation of encephalisation through several chapters of increased endocranial doming that we demonstrate to result from progenetic developments. Elevated encephalisation associated with progressive size reduction within

Maniraptoriformes was secondarily exapted for flight by stem avialans. Within Mesozoic Avialae, endocranial doming increased in at least some Ornithurae, yet remained relatively modest in early

Neornithes. During the Paleogene, volant non-neoavian birds retained ancestral levels of endocast doming where a broad neoavian niche diversification experienced heterochronic brain shape radiation, as did non-volant Palaeognathae. We infer comparable developments underlying the establishment of pterosaurian brain shapes.

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Among Sauropsida, the avian brain is uniquely enlarged relative to body size, which renders birds the only animal group that rivals the encephalisation of mammals1. Certain cognitive requirements of vertebrate flight, particularly those demanded in processing sensory input and controlling the intricate flight apparatus2,3,4,5, have been used to explain important changes in relative volume and organisation of the brain along the evolutionary pathway towards a “flight adapted” brain6.

Associated evolutionary patterns, including cranial shape shifts7,8,9 and overall body size reduction along the avian stem10, propose paedomorphosis as an important developmental mechanism underlying the establishment of characteristic properties of avian anatomy, including the inflated brain. Such overarching trends in the evolutionary lineage leading up to modern birds are consistent with the hypothesis that heterochronic developments were crucial towards the establishment of archosaurian volancy in general and dinosaurian flight in particular.

Detailed comparative investigations into brain shape and size at the very onset of dinosaurian flight have been incapable of identifying specific endocranial conditions unequivocally linked with dinosaurian volancy. It has been concluded that the brain of the early volant avialan Archaeopteryx, considered exemplary for the transition between non-volant and volant theropods11,12, did not present an anatomy profoundly contrasting those of non-volant Maniraptora1. Only a single cerebral structure, the wulst, until then only recognised in modern birds (Neornithes) but conclusively absent in non-volant maniraptorans and Mesozoic (non-avian) Ornithurae13,14, was found to also be potentially present in Archaeopteryx1. The apparent lack of unambiguous flight-related cerebral adaptations in the oldest volant avialan identified to date has confused our understanding of the relation between inferred dinosaurian volancy and the development of a correspondingly flight- capable brain15. Furthermore, because the variation in relative endocranial and cerebral volumes of modern birds and their non-avian ancestors was found to not primarily reflect to the presence or absence of powered flight16, other geometrical parameters are required to explain the evolution of the archosaurian brain in the context of volancy.

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Where early palaeoneurological investigations on lithified cranial fossils typically involved perilous physical casting and occasionally demanded sacrifice of complete osseous braincases, the advent and development of X-ray computed tomography techniques (CT) has enabled reliable and non- destructive reconstruction of the size and shape of endocranial cavity17. Although conventional CT setups typically allow for reliable endocranial visualisation of modern material, fossils encased in and filled with a sedimentary matrix may require the application of more elaborate tomographical techniques, especially when the fossil is preserved in a plate-like slab composed of a lithic substrate with a density comparable to that of the sample of interest. More advanced CT approaches do not only enable the visualisation of samples that cannot be confidently resolved otherwise, but will generally also offer improved contrast and spatial resolution to allow for more reliable reconstruction and comparison of homologous geometries across multiple samples and a better appreciation of deformation incurred during taphonomy. Synchrotron propagation phase-contrast

X-ray microtomography (PPC-SRµCT) in particular offers unparalleled contrast and detail in palaeontological data and has emerged as the pre-eminent approach to imaging challenging fossils today18,19,20,21,22.

Because brain tissue itself rarely fossilises23,24, palaeoneurology resorts to studying the cranial endocast that reflects the surface geometry of the endocranial cavity which housed the brain during life12,17. Non-avian dinosaurs generally exhibit an overall brain shape resembling the crocodilian brain more strongly than the modern avian brain25,26. We aimed to exploit the conservative preservation of the osseous braincase in both extinct and extant taxa while avoiding uncertainty regarding whole-brain volume or exact delimitation of cerebral components. Comparative analysis of endocast geometries covering a wide phylogenetic, size, and shape range confidently permits identification of broadly supported trends relevant to identifying the evolutionary processes that shaped the modern avian brain.

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To test the hypothesis that the endocranial cavities of extinct bird-line archosaurs conservatively documented the evolutionary pathway of the brain through time, we compiled a representative database of endocranial shapes encompassing the largest possible diversity of extant and extinct archosaurs, and included selected lepidosaurs as an outgroup. In order to evaluate the influence of developmental heterochrony on the evolutionary trajectory towards modern birds, we furthermore investigated ontogenetic series of extant crocodilians and birds to assess associated brain shape developments while bracketing non-avian dinosaurs phylogenetically27. PPC-SRµCT with optimised imaging protocols at beamlines BM05, ID17, and ID19 of the European Synchrotron

Radiation Facility (ESRF) ensured reliable yet non-destructive visualisation of the endocasts in multiple specimens of Archaeopteryx and other fossil as well as extant archosaurs18,28,29. The data set was supplemented with conventional CT data representing a sufficiently wide selection of modern avian endocasts to resolve endocranial variation across the ecological and body size range occupied by present-day birds. Shape variation was quantified through two-dimensional landmarking in lateral view and shape changes were subsequently analysed with Principal

Component Analysis (PCA). PCA identified dorsal endocast curvature, originating from brain axis flexure and relative telencephalic and cerebellar size, as the dominant shape variable in the data set.

The C/D parameter, defined as the ratio of dorsal endocast length following the convex hull between the anteriormost tip of the cerebrum and the opisthion (C) over the linear distance between those two locations (D; Extended Data Figure 3), was recovered as a straightforward geometric ratio conservatively capturing and quantifying endocast doming. We compared embryonic C/D development in Crocodylus niloticus, Gallus gallus, and Ficedula albicollis to characterise and compare developmental timing during their in ovo trajectories towards revealing heterochronic influences on embryonic ontogeny. We furthermore plotted endocast doming (C/D) against log(D) for all adult archosaurs subjected to PCA, but also included a broad selection of lepidosaurs, as an outgroup to archosaurs, and an ontogenetic growth series of Crocodylus niloticus. This resolved a

125 partially overlapping distribution of archosaurian endocranial shapes and sizes that can be directly comparable against the complete ontogenetic variability of C. niloticus.

Results

The PCA morphospaces for two-dimensional Type I landmarks and semi-landmarks assigned to archosaurian endocasts in lateral view (see Methods) exhibit broadly comparable shape distributions

(Figure 1a and 1c) that are strongly correlated together (93%, Extended Data Figure 1A). For both landmark types, PC1 explains the majority of shape variation (80% for Type I landmarks and 89% for semi-landmarks, Extended Data Figure 1B and 1C). In both Type I and semi-landmark morphospace, PC1 primarily captures whole-endocast shape changes in a pattern transforming a virtually straight dorsal endocast margin to a strongly dorsally domed endocast (Figure 1b and 1d).

This pattern arises through an overlapping succession of phylogenetic clusters representing, in order of increasing PC1 scores, crocodilians, non-maniraptoriform dinosaurs, non-avian maniraptoriforms, and neornithes. In Type I landmark morphospace, PC1 additionally captures endocast shape shifts that reflect intra-endocast shape variability in the cerebral domains roughly corresponding with the telencephalon and the rhombencephalon (Figure 1b). Although a relative progressive increase in telencephalic size appears to typically accompany increasing PC1 scores, the referred pattern involves several non-homologous morphological transformations and thereby fails to capture truly comparable shape shifts across the phylogenetically diverse archosaurian assemblage. This renders the semi-landmark set most appropriate for visualising and studying whole-endocast shape variation in the data set studied here.

The dominant shape shift in the semi-landmark set, reflected in PC1, can be reliably expressed as a ratio dividing the total distance of the dorsal margin of the endocast between the anteriormost point of the telencephalon and the dorsalmost point of the foramen magnum (C) over the shortest distance between these two points (D). The correlation between PC1 in semi-landmark PCA and the novel

126 geometrical ratio C/D was found to be substantial (88%) (Extended Data Table 1), which reinforces employment of this ratio as a straightforward yet robust measure of the dominant endocast shape variability in our data set.

Across the entire size range, adult lepidosaurs (C/D range 1.00 – 1.16) and crocodilians (C/D range

1.01 – 1.10) exhibit strongly elongated endocast shapes (average C/D = 1.04) that broadly overlap in morphospace (Figure 2, Extended Data Figure 2). Non-maniraptoriform dinosaurs (C/D range

1.04 – 1.30) are contained within a hull that marginally overlaps the shape ranges of lepidosaurs and crocodilians but generally corresponds to notably more domed endocasts (average C/D = 1.12). The hull for non-avian maniraptoriforms (C/D range 1.09 – 1.54, average C/D = 1.25) partially overlaps the upper range in endocast doming of non-maniraptoriforms but does not overlap the lepidosaurian or crocodilian hulls. Endocast curvature measures of this group furthermore largely agree with those recovered for pterosaurs (C/D range 1.13 – 1.34, average C/D = 1.25). Notably, the basal pterosaur

Rhamphorhynchus muensteri already exhibits a C/D of 1.24. Volant palaeognathous birds, including the Paleocene-Eocene genus Lithornis (C/D range 1.20 – 1.38, average C/D = 1.33), share a discrete domain in endocast shape and size with Galliformes (C/D range 1.17 – 1.48, average C/D = 1.30) and Anseriformes (C/D range 1.17 – 1.41, average C/D = 1.29) that partially overlaps the hulls for non-avian maniraptoriforms and pterosaurs. Sparsely available metrical and endocast data on a cranium of the Eocene anseriform Presbyornis sp. (USNM 299846)30,31 indicates a C/D ratio between 1.24 and 1.37 for this taxon, which is well within the range occupied by present-day anseriforms. Notably, the Late Cretaceous ornithurine Cerebavis cenomanica exhibits a C/D ratio in the range of modern volant neoavians (C/D = 1.54), which is higher than in any volant palaeognath, galliform, or anseriform. Non-volant palaeognaths (“ratites”) share their average degree of endocast doming with volant palaeognaths but encompass a comparably broad C/D range

(C/D range 1.10 – 1.71, average C/D = 1.34). The neoavian radiation spans a particularly broad

127 endocast shape variability (C/D range 1.08 – 2.15, average C/D = 1.49) that partially overlaps all other groups but also includes the highest C/D values recorded.

The non-volant dromaeosaur Halszkaraptor and the early volant avialan Archaeopteryx present comparable endocranial geometries that are intermediate between those of non-maniraptoriform dinosaurs and those found in modern birds6 (Figure 2). Halszkaraptor exhibits a C/D of 1.18, and precise measurements on the London Specimen of Archaeopteryx and conservative estimates obtained for the Munich Specimen of Archaeopteryx through its partially preserved left telencephalic hemisphere yielded C/D values of 1.16 and 1.17, respectively.

During in ovo embryonic development of Crocodylus niloticus, C/D values decrease from 2.13 on day 18 to (on average) 1.11 on day 93 (Figure 5). Although post-embryonic maturation does involve a certain degree of brain straightening32, post-hatching endocast doming in C. niloticus is always low. C. niloticus was found to exhibit C/D values upon hatching, thirteen days after hatching, and in the first and third year of life, of 1.09, 1.09, 1.06, and 1.04, respectively. Such values, up to C/D

= 1.10, were encountered in the adult crocodilian set as well. During embryonic development of C. niloticus, the brain and endocast long axis rotates anterodorsally from a nearly vertical orientation to the horizontal configuration seen in the adult condition (Figure 2, Figure 3).

Comparison of ontogenetic C/D development from early in ovo embryonic stages to adulthood between Crocodylus niloticus and Gallus gallus revealed shape trajectories with a statistically significant divergence (T value = 2.61, p = 0.0057, Supplementary Table 2). Different than in C. niloticus and G. gallus, ontogenetic C/D values obtained for Ficedula albicollis describe an in ovo shape trajectory including a stage during which C/D increases.

Contra previous reports1, a wulst is conclusively absent in Archaeopteryx (Extended Data Figure 4).

The “cerebral indentation” resolved on conventional tomographical data of the London Specimen and proposed to indicate the presence of a wulst homologous to those of Neornithes1 actually reflects a section of the braincase roof that has partially collapsed during taphonomy. High-quality PPC-

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SRμCT data on the London Specimen, but also those on the Munich, Daiting and Eichstätt specimens (Extended Data Figure 4), do not reflect anatomical indications for the presence of a wulst on the brain or a wulst-like projection on the cerebral endocast of Archaeopteryx.

Discussion

Crocodilians and birds, the only archosaurian groups with extant representatives, present morphological end members of adult archosaurian brain shape variation. The linear “crocodilian” brain exhibiting sequential arrangement of neuroanatomical domains and a caudally positioned connection to the spinal column accounts for the primitive archosaurian condition32 that is shared with the archosaurian outgroup Lepidosauria33,34 (Figure 2). In contrast, the avian brain (and to a lesser extent the pterosaur brain) exhibits a strongly domed brain geometry that results from a relatively inflated cerebrum, more complex spatial distribution of the neuroanatomical domains following stronger brain axis flexure, and a more ventrally positioned connection to the spinal column1 (Figure 2, Figure 3).

In crocodiles, ontogenetic progression has been demonstrated to involve an “unrollment” of the brain through a reduction of cephalic and pontine flexures and relative increase in cerebellar volume, olfactory tract length, and olfactory bulb size32. This is readily recognisable in endocast geometry as the embryo develops in ovo (Figure 3).

In association with progressive size reduction of bird-line dinosaurs10, analyses of cranial shape trajectories across archosaurian phylogeny have revealed relatively short ontogenetic trajectories in eumaniraptorans that are consistent with paedomorphosis by progenesis (where accelerated somatic maturation results in a truncated ontogeny relative to ancestral taxa) and explain the relative brain enlargement in Eumaniraptora as a paedomorphic feature7,35,36,37. Progressive progenetic progenetic expression recognized in the evolutionary history of bird-line dinosaurs can be related to a corresponding (and increasingly earlier) developmental stage in the crocodilian ontogenetic series

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(Figure3). Furthermore, the retained posteroventral rotation of the adult avian brain relative to those of crocodilians32, and non-avian dinosaurs38 such as Archaeopteryx11 (Figure 3), contributed importantly to the collapse of the facial region in birds7.

Progenesis has been argued to represent the most important heterochronic pathway in producing evolutionary novelties39,40. Comparison of endocranial shape through (early) ontogeny in

Crocodylus niloticus and Gallus gallus (Figure 5a) illustrates disparate C/D pathways most strongly diverging during embryonic development. C. niloticus and G. gallus hatchlings both immediately leave the egg without obligate parental assistance41,42,43,44. Despite different incubation periods

(circa 90 days for Crocodylus niloticus45 and circa 21 days for Gallus gallus46), this indicates that hatchlings of both taxa represent equivalent developmental stages upon hatchling, which is corroborated by the observation that near-adult C/D values are observed in the hatchlings of each species. In ovo embryonic reduction of C/D in G. gallus proceeds more rapidly than in C. niloticus in absolute time (Figure 5a) but occurs decelerated relative to C. niloticus when both trajectories are normalised to the same developmental stage (Figure 5b). In effect, in ovo decrease of C/D virtually halts upon hatching when (nearly) adult C/D ratios are achieved in G. gallus whereas embryonic

C/D decrease in C. niloticus proceeds below adult ratios of G. gallus towards values approaching those of the adult crocodilian condition upon hatching. As the progenetic signature recognised in overall cranial shape7, the divergence between C. niloticus and G. gallus in magnitude and timing of endocranial shape shifts during embryonic development is best explained by progenesis in bird- line archosaurs. This interpretation is reinforced by reduced olfactory tracts and bulbs, relatively smaller cerebellum, and posteroventral rotation of the adult avian brain relative to the crocodilian condition, as these characters are invariably shared with embryonic crocodilians but not with later crocodilian ontogenetic stages. C/D ratios obtained for the passerine Ficedula albicollis during in ovo development (Figure 5) suggest a substantially different in ovo C/D pathway characterised by a chapter of C/D increase rather than continuous decrease towards hatchling. This indicates a

130 developmental strategy (partially) uncoupled from the generalised non-neoavian archosaurian C/D curve and may have originated to meet the cognitive requirements required for elaborate flight in ecological niches adopted by passeriform Neoaves.

Halszkaraptor exhibits a high level of endocast coiling among non-avian maniraptoriform dinosaurs

(Figure 3), as does the small dromaeosaurid maniraptoriform Bambiraptor feinbergi47 (C/D=1.15).

Despite the clearly non-volant anatomy of Halszkaraptorinae and its ancestors28, Halszkaraptor does combine a body size within the range of flying birds with a degree of endocast coiling shared with some modern birds. Archaeopteryx also shows endocast coiling within the range of

Maniraptoriformes. The endocranial geometry of Archaeopteryx is broadly shared with small yet non-volant maniraptorans, particularly Halszkaraptor, indicating that its endocranial shape resulted mainly from heterochronic developments at the root of Paraves and did not arise in the context of its incipient dinosaurian volancy. Progenetic reduction in the relative size of the adult olfactory bulbs, as observed in modern birds, was not yet achieved in Archaeopteryx11, which has been used to infer an olfactory acuity ranging from “typical to high” in Archaeopteryx relative to Neornithes48.

This again illustrates that particular properties of the characteristic avian endocranial anatomy arose within already volant Avialae, implying they did not represent absolute functional prerequisites for flight but rather adaptations towards improved flight or other ecological demands.

The current avian phylogeny49, coupled with the recent recognition of a basal anseriform clade that originated before the end-Cretaceous extinction event50, indicates that the divergences between

Palaeognathae-Neognathae, Galloanserae-Neoaves, and Galliformes-Anseriformes all occurred during the Cretaceous51. This implies that at least four extant avian clades (Palaeognathae,

Galliformes, Anseriformes, and Neoaves) crossed the K-Pg boundary and subsequently negotiated an obligatory non-arboreal phase during the earliest Paleogene52. All living birds, including flightless palaeognaths, descended from volant stock53, although likely not from dexterous flyers comparable to aerial specialists within modern Neoaves. Furthermore, present-day palaeognathous

131 diversity originated exclusively during the Paleogene48. This group stemmed from a volant tinamou-like ancestor akin to the earliest Paleogene (and possible latest Mesozoic54) members of the clade Lithornithidae55,56, despite the true (but presently obscured) origin of Palaeognathae possibly having occurred as far back as the Early Cretaceous56.

Within Aves, galliforms, anseriforms, and volant palaeognaths occupy discrete, restricted, yet broadly overlapping hulls in C/D vs log(D) morphospace (Figure 2). This particular domain is also shared with small non-avialan Maniraptoriformes and Archaeopteryx, which indicates that these groups exhibit generally similar endocast doming levels at comparable endocast lengths. All referred taxa share essentially ground-dwelling ecologies57, which, for the referred avians, likely aided their survival of the K-Pg event (possibly in broadly “shorebird-like” ecologies58) and were retained after the earliest Paleogene recovery of arboreal habitats52. The overall C/D range shared by modern-day members of basal avian sister taxa that have occupied analogous habitats since the

K-Pg event suggests their level of endocast doming preserved the ancestral, Mesozoic condition for

Neornithes. This conclusion is supported by the pivotal positions of Lithornis and Presbyornis in

C/D versus log(D) morphospace (C/D of 1.20 for Lithornis and 1.23 for Presbyornis; see Extended

Data Table 1) close to those of tinamous and modern anseriforms, respectively, which were all recovered in relative proximity to those of Archaeopteryx. Notably, volant archosaurs that succumbed to extinction in the K-Pg event, such as non-avian members of Ornithurae (Ornithurae sensu59; e.g. Cerebavis), the Enantiornithes, and the Pterosauria, may have exhibited endocast coiling levels exceeding those of non-neoavian birds. Nevertheless, their physiological and ecological demands proved incompatible with the global short- and long-term effects of the

Chicxulub impact event52.

As such, the proportionally large endocast size and C/D range of secondarily non-volant extant

Palaeognathae reflects the Paleogene radiative colonisation of ecological niches by volant ancestors followed by independent evolutionary histories after these taxa became flightless60.

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Most striking is the large diversity in C/D across a broad range of endocast sizes seen in Neoaves, which dominates the C/D vs log(D) plot (Figure 2). Although Neoaves originated in the Mesozoic

49,52,61, no Mesozoic neoavians are presently known. The highly diverse and speciose distribution of present-day Neoaves arose during and following their explosive early Paleogene ecological radiation52,58. The Mesozoic ornithurine Cerebavis62 is only known from an incomplete and abraded skull preserving a sufficiently complete braincase to reliably reveal a brain shape involving strong flexure and a “stacked” geometry, similar to those of some extant Neornithes14. The light cranium itself was furthermore reported to exhibit a degree of fusion consistent with the advanced flight adaptations seen in Neoaves14. In a comparative context, we conclude that the degree of endocast doming in Cerebavis exceeding those of volant non-neoavians was achieved independently from the Paleogene neoavian radiation. This observation is consistent with an expression of cognitive challenges surpassing those of the largely ground-dwelling ecologies retained by non-neoavian birds included in our study, and may indicate progressive adaptation to more demanding aerial requirements in Cerebavis. Similar progenetic developments appear to have coincided with the origins of other volant archosaurian clades, such as earlier at the roof of Pygostylia, but also in

Pterosauria (Figure 4). Progenesis appears to have been involved in the establishment of anatomical prerequisites for archosaurian volancy on more than one occasion, albeit through exaptation of features that arose in a non-volant context. Secondary complexification of flying habits within these taxa may have stimulated progressive reorganization, such as reflected on the broad neoavian endocranial diversity. Nevertheless, Mesozoic chapters of basal avialan and, later, ornithurine brain inflation did not involve the development of a wulst of wulst-like homologue. Until a wulst is positively identified in a (Mesozoic) ornithurine closer to Neornithes than Cerebavis, the wulst is

14,17 again considered a uniquely neornithine synapomorphy .

Conclusions

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Among extant birds, volant palaeognaths, galliforms, and anseriforms share an ancestral level of endocast doming that remained close to those of some non-volant Maniraptoriformes, such as

Halzskaraptor, and their volant relatives including Archaeopteryx. This larger range includes the endocast size and degree of endocast doming corresponding to the first dinosaurian “flight-adapted” brain. Endocast doming was found to resolve the developmental strategies associated with the evolution from non-maniraptoriform dinosaurs to Avialae and the subsequent evolutionary pathway towards and into neoavian birds. Nevertheless, strong group overlap and limited phylogenetic resolution at the origin and during the early evolutionary history of Avialae prevents identification of discrete conditions resolvable in lateral whole-endocast shape that either enabled volancy or unambiguously indicate volancy. Volancy originated in a dinosaurian group characterised by reduced body sizes relative to their ancestral condition that achieved sufficient cognitive performance to permit aerial locomotion. However, this locomotory innovation did not preserve a characteristic morphological hallmark on the endocranium, rendering the recognition of (early) dinosaurian volancy through whole-endocast volume1 and geometry (this contribution) impossible on presently known material.

The whole-endocast geometries of volant palaeognaths, galliforms, and anseriforms quantified in this study have deep evolutionary histories, as corroborated by their general proportions shared with some Maniraptoriformes, including Archaeopteryx. Agreement with the endocast shapes of the

Paleocene volant palaeognath Lithornis and the Eocene anseriform Presbyornis furthermore indicate that these endocranial shapes are conservative relicts that do not represent (relatively) recent convergences. Among modern birds (Aves), volant palaeognaths, galliforms, and anseriforms are therefore concluded to preserve brain geometries most closely reflecting that of the avian ancestor, which renders them most appropriate for reconstructing early avian cerebral developments.

The large brain shape diversity of Neoaves is mostly the product of complex and progressive niche partitioning that started during the early Paleogene neoavian diversification phase52 and set the stage

134 for the exploitation of a broad ecological range exploited by present-day birds. This finding renders the explosive Paleogene avian niche expansion predominantly a neoavian affair, and opens up opportunities for studying endocranial shape variation in direct relation to avian ecological strategies. Nevertheless, it also challenges the employment of neoavian brain shape variation in reconstructing the early “flight-adapted” dinosaurian brain shape. Neoavian brain shape diversity reflects the influence of several successive developments resulting in a highly apomorphic brain shape range that has advanced beyond and thereby likely obscured informative morphological properties associated with the onset of dinosaurian volancy.

Following convergent progenetic developments associated with size reduction in the ancestral and early evolutionary histories of both birds and pterosaurs, we infer that certain evolutionary thresholds were negotiated in small-bodied ornithodirans that enabled the exploitation of volant ecologies, partially (but crucially) through exaptation of the available brain capacity (Figure 4).

After sufficient cerebral performance was allocated to enable aerial excursions, the evolutionary radiations of pterosaurs and birds both saw a complete decoupling of endocast doming and body size from the ancestral architecture. Within Pterosauria, progenetic effects on endocranial shape are particularly recognisable in derived ecologies, although increased flexure and cerebral enlargement were already recorded in the most basal pterosaurs studied herein. The origin of increased brain doming in the earliest volant dinosaurs was not intimately associated with volancy but rather with enhanced cerebral processing to enable increasingly complex behaviour. A secondary radiation within neoavian birds was recorded in an explosive diversification of endocranial shapes, which reflected the establishment of a broad ecological range with variable volant requirements. Although recent results propose that even Archaeopteryx may already have been capable of flight29, its brain was probably not yet capable of controlling the complex volancy seen in most modern birds.

135

Methods

A digital library of high-resolution tomographical data on crania of 15 adult lepidosaurs, an ontogenetic series including 42 specimens of Crocodylus niloticus, 72 additional adult crocodilian individuals, two adult pterosaurs, four non-avian dinosaurs, four specimens of Archaeopteryx, 190 adult specimens of Neornithes, and ontogenetic series of Gallus gallus, Phasianus colchicus,

Ficedula albicollis and Passer domesticus was created using synchrotron X-ray microtomography at beamlines BM05, ID17 and ID19 of the European Synchrotron Radiation Facility in Grenoble,

France. Synchrotron X-ray microtomography was conducted using an optimised polychromatic beam with sufficient coherence to allow the use of PPC-SRμCT. Three-dimensional volume reconstruction was conducted through filtered back-projection following a single distance phase retrieval protocol that relies on an assumption of homogeneity63,64. The synchrotron data set was supplemented with an additional Crocodylus niloticus cranium visualised with a medical tomograph at the Centre Hospitalier Universitaire in Grenoble, France, and crania of one specimen of

Paleosuchus palpebrosus and 146 adult Neornithes visualised using laboratory tomographical techniques at the Institute of Physiology and the Institute for Clinical and Experimental Medicine in Prague, Czech Republic. Additional cranial scanning data of 45 lepidosaurs, two crocodilians, and five Neornithes were accessed through DigiMorph (www.digimorph.com) and processed in tandem with the data obtained in the scope of this study. Material and data provenance as well as repositories curating the digital data are listed in Extended Data Table 1. Virtual three-dimensional endocasts were extracted from the reconstructed crania by adopting cranial bones as delimitating masks in VGStudio MAX 2.2 (Volume Graphics, Heidelberg, Germany). Additional appropriate endocasts visualised in lateral view were sourced from literature (Extended Data Table 1) and processed alongside the scanning data.

The endocast of the London Specimen of Archaeopteryx had already been visualised twice through conventional tomographical techniques1,6. The newly created endocasts of four specimens of

136

Archaeopteryx (Supplementary Figure 2), including the London Specimen, that were obtained through PPC-SRμCT allowed for a re-examination of the wulst; a morphological structure of which the presence has been proposed to represent an unambiguous synapomorphy shared by

Archaeopteryx and neornithes1. The London Specimen (BMNH 37001)11 is a nearly complete specimen of which most of the braincase was freed from the limestone slab. The left part of the natural cranial endocast remains largely delimited by cranial bones but the right side is directly observable because the corresponding part of the osseous braincase remains in the counterslab. Of the braincase in the Munich Specimen (BSP 1999 I 50)11, only a right parietal can be readily recognised, but more material may be present ex situ on and within the limestone plates. The Daiting and the Eichstätt (JM 2257)11 specimens both preserve a complete yet strongly compressed cranium that prevents reliable three-dimensional reconstruction but does allow for recognition of borders between structures in the interior braincase.

On all adult archosaurian endocasts, seven Type I landmarks were conservatively identified in lateral view at discrete morphological locations along the dorsal endocast contour between the anteriormost tip of the telencephalon and the dorsalmost point of the foramen magnum. Two- dimensional landmark digitisation was realised in lateral views. Three-dimensional landmark visualisation was considered tenuous, as dinosaurian endocasts typically do not accurately preserve three-dimensional shape throughout. The definition of Type I landmarks relies on recognition of homologuous borders between cerebral structures, which in turns depend on the cerebral representativity of the endocast. This property is generally much lower in crocodilian and dinosaurian specimens than in modern avian material, which renders direct comparison challenging.

Landmarks were placed on the borders between or extreme limits of cerebral structures (Extended

Data Figure 3c): 1-Anteriormost tip of telencephalon, 2-Border between telencephalon and cerebellum, 3-Dorsalmost tip of foramen magnum, 4-Ventralmost tip of foramen magnum, 5-

137

Dorsalmost limit of telencephalon, 6- External border of cerebellum, equidistant from landmarks 2 and 3, and 7-Ventralmost expansion of the medulla oblongata.

Semi-landmarks were placed at equidistant intervals along the dorsal endocast contour between the anteriormost tip of the telencephalon and the dorsalmost point of the foramen magnum in all studied adult archosaurian endocasts (Extended Data Figure 3d) to capture whole-endocast shape. All landmarking was conducted in TpSDig2. Landmark-based 2D geometric morphometrics (GM) was used to quantify endocast shape and shape variation using MorphoJ (version 1.06b)65 following

Procrustes superimposition. Shape analysis of the adult archosaurian subset was conducted by principal component analysis (PCA) in Morpho J to explore shape variation among endocrania of adult archosaurs.

PCA scores were transferred to PAST (version 3.20)66 for visualisation and analysis. The correlation between PCA of Type I and semi-landmarks was statistically assessed through regression analysis.

Based on assessment of the most representative reflection of whole-endocast variability across archosaurs, the optimal landmark set appropriately capturing dominant whole-endocast shape variation in the total sauropsid set was identified. The recovered dominant whole-endocast shape variability was translated into a simplified yet statistically warranted geometrical ratio. This novel shape ratio was calculated for the entire data set and plotted against log(endocast length) to visualise the associated endocast size variation. Relations and underlying patterns were assessed, interpreted, and discussed in relation to the evolutionary establishment of discrete archosaurian groups in the context of dinosaurian volancy (Extended Data Figure 1). The divergence between the ontogenetic trajectories of Crocodylus niloticus and Gallus gallus (Fig. 5) was statistically tested through shape space trajectory analysis67 in Microsoft Excel (Microsoft corporation, Redmond, Washington, USA; see Extended Data Table 1). Absolute age of the specimens was included as the log-transformed age in days after oviposition (Extended Data Table1, Figure 5a). Relative developmental age normalizes absolute age (after oviposition) to homologuous developmental stages relative to

138

hatchling (1) and the establishment of sexual maturity (2). As such, values between 0 and 1 reflect

in ovo developmental stages, whereas values between 1 and 2 indicate hatchling, juvenile, and

subadult to adult development (Extended Data Table 1, Figure 5b).

Towards defining birds, we follow Gauthier68 in recognising the synonymy of Neornithes and Aves.

In this definition, only the last common ancestor of modern birds and all of its descendants account

for the complete avian diversity. All dinosaurs with feathered wings used for flapping flight are

placed within Avialae68, which renders Avialae virtually synonymous with the younger but now

abandoned definition of Aves that encompasses the last of common ancestor of Archaeopteryx and

Passer domesticus, and all of its descendants69.

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Data availability Data are accessible through the ESRF Paleontological Database (http://paleo.esrf.fr) and Morphobank (http://morphobank.org).

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Acknowledgements The authors thank C. Berruyer for her assistance during experiments and acknowledge M. Kundrát (Pavol Jozek Safarik University, Kosice, Slovakia) for his role in the origin of the initial project. D. Berthet (Musée des Confluences, Lyon, France), Miroslav Procházka (Krokodýlí ZOO, Protivín, Czech Republic), S. Martin, E. Fernandez, A. Tomas and A. Soler (La Ferme aux Crocodiles, Pierrelatte, France), E. Woessner, C. Dubois and B. Chenet (Safari de Peaugres, Peaugres, France), S. Chapman (Natural History Museum, London, England), P. Candegabe (Museum d’Histoire Naturelle, Grenoble, France), T. Loeb ( Echirolles, France), L. Viriot, C. Charles and B. Thivichon-Prince (ENS, Lyon, France), R.David (Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany), B. de Klerk (Albany Museum, Grahamstown, South Africa) are acknowledged for providing access to the studied specimens. The authors are especially grateful to Per Ahlberg (Uppsala University, Sweden), Pascal Godefroit and Andrea Cau for their invaluable advice and help that made this study possible.

Author contributions V.B. and P.T. conceived the study and designed the experiments, V.B., D.F.A.E.V., P.T., and V.F. performed synchrotron scanning experiments, J.J. and D.J. performed the conventional CT experiments, V.B., D.F.A.E.V. and P.T. analysed the data, V.B. and D.F.A.E.V. wrote the manuscript with the help of P.T. S.B., V.F., J.J., D.J. and O.R. participated in the general discussions and edited the manuscript.

Author informations Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests. Readers are welcome to comment on the online version of the paper. Correspondence and request for materials should be addressed to D.F.A.E.V. ([email protected]). Funding This project was partially funded by the ESRF, by grant P302/12/2017 of the Czech Science Foundation, and by internal grant IGA_PrF_2017_023 of the Faculty of Science of Palacký University.

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Figure 1. PCA plots for Type I landmarks and semilandmarks, and associated dominant dorsal endocast shape changes. A-Principal Component Analysis plot for Type I landmarks ; B-Summary of endocranial shape change along PC1 for Type I landmarks; dorsal endocast contours on deformation grid from average ; C-Principal Component Analysis plot for semilandmarks ; D-

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Summary of endocranial shape change along PC1 for semilandmarks; dorsal endocast contours on deformation grid from average. Crocodilian specimens are indicated by blue points, the crocodilian distribution is delimited by a blue hull. Non-maniraptoriform dinosaurs are indicated with orange points, Maniraptoriformes with yellow points, Paleognathae with brown point, and Neognathae with green points. The avian distribution (Paleognathae+Neognathae) is delimited by a green hull. Endocast shape variations (B and D) include landmark positions as red points. Coloured hulls (in B) delimit cerebral domains occupied by the telencephalon (orange) and rhomboncephalon (yellow).

Figure 2. Bivariate plot of and endocranial doming (C/D) versus log-transformed endocast length (Log D). Blue indicates crocodilian pre-hatchling (dashed light blue line) and post-hatchling (continuous dark blue line) ontogenetic trajectories. Coloured hulls delimit sauropsid groups: Lepidosauria (grey), non-maniraptoriform dinosaurs (red), non-avian Maniraptoriformes (yellow), Pterosauria (dark green), volant non-neoavian birds (black), and non-volant Paleognathae and Neoaves (light green). The inset reflects the endocranial diversity of extant volant non-neoavian taxa: volant Paleognathae (brown), Anseriformes (dark blue), and Galliformes (dark pink). Dashed brown line visualises the addition of the extinct volant paleognath Lithornis plebius to extant flying Paleognathae. Visualised endocasts mark the positions of individual specimens: 1-Podarcis muralis; 2-Varanus exanthematicus; 3-Caiman crocodylus; 4-Crocodylus niloticus; 5-Alligator mississipiensis; 6-Heterodontosaurus tucki; 7-Psittacosaurus lujiatunensis; 8-Arcovenator escotae; 9-Tyrannosaurus rex; 10-Rhamphorhynchus muensteri; 11-Paraspicephalus purdoni; 12-

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Araripesaurus santanae; 13-Halszkaraptor escuillei (yellow star); 14-Incisivosaurus gauthieri; 15- Struthiomimus altus; 16-Archaeopteryx lithographica (orange stars); 17-Phasianus colchicus; 18- Leptoptilos crumeniferus; 19-Thalurania furcata; 20-Cerebavis cenomanica; 21-Ficedula albicollis;22-Strix nebulosa; 23-Struthio camelus.

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Figure 3. Selection of sauropsid endocasts used in this study. Endocasts arranged in rows by C/D clusters, the corresponding crocodilian ontogenetic stage is visualised through the associated endocast most right. Coiling value for each endocast provided in figure between brackets. Endocasts not to scale, individual scale bar lengths provided in caption. Stage 0: Podarcis muralis (1; scale bar 0.65 mm); Varanus exanthematicus (2; 5 mm); Caiman crocodylus (3; 5 mm); Alligator mississipiensis (4; 9.5 mm); Crocodylus niloticus hatchling (5; 2.5 mm). Stage 1: Heterodontosaurus tucki (6; 5 mm); Psittacosaurus lujiatunensis (7; 20 mm, modified from Zhou et al. 2007); Arcovenator escotae (8; 20 mm); Tyrannosaurus rex (9; 40 mm 33); 1 year-old C. niloticus (10; 2.5 mm). Stage 2: Archaeopteryx lithographica (11; 2.5 mm); Halszkaraptor escuillei (12; 3 mm); Incisivosaurus gauthieri (13; 10 mm66); Struthiomimus altus (14; 10 mm 33). Stage 3: Rhamphorhynchus muensteri (15; 5 mm106); Parapsicephalus purdoni (16; 10 mm78); Tropeognathus mesembrinus (17; 4.5 mm); Araripesaurus santanae (18; 4.5 mm); 68-day-old C. niloticus embryo (19; 2.5 mm). Phasianus colchicus (20; 3 mm); Tadorna tadorna (21; 5 mm); Dromaius novaehollandiae (22; 6 mm); Vultur gryphus (23; 6 mm); Ficedula albicollis (24; 1.5 mm); Cerebavis cenomanica (25; 5 mm14); Turdus philomelos (26; 2.5 mm); Strix nebulosa (27; 5 mm); 24-day-old C. niloticus embryo (28; 1.5 mm). Arrows indicate the positions of the anteriormost tip of the cerebrum (green) and the opishtion (red). Vertical black arrow indicates increase in endocast doming, horizontal black arrow indicates increase in body size.

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Figure 4. Heterochronic evolution of archosaurian endocranial geometry along the avian stem. Phylogeny of studied archosaurian groups and endocasts of key specimens visualised. Red lineages exhibit low endocast doming, orange lineages exhibit medium endocast doming, green lineages exhibit high endocast doming. Volant taxa indicated in bold, average group doming value or

measured specific doming value provided between brackets.

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Figure 5. Bivariate plots of developmental age versus endocranial doming for selected archosaurian taxa. Ages presented as log-transformed age in days (a) and as developmental-stage normalised ages relative to hatchling (1; b). Developmental series are divided in pre-hatchling (dashed line) and post-hatchling (continuous line) stages. Markers most right reflect the condition at sexual maturity.

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Extended Data Figure 1. Correlation plots between PC scores of Type I landmarks,

semilandmarks and endocranial doming (C/D). Correlation of PC Type I landmarks scores versus PC semilandmarks scores (A), C/D ratio versus PC Type I landmarks scores (B), C/D ratio versus PC semilandmarks scores (C).

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Extended Data Figure 2. Bivariate plot of log-transformed endocast length (Log D) versus endocranial doming (C/D) in all tested sauropsids. Small colour-coded circles represent phylogenetic groups: Lepidosauria (grey), crocodilians (blue), non-maniraptoriform dinosaurs (brown), Maniraptoriformes (yellow), Paleognathae (red), and Neognathae (green). Colour-coded stars represent key fossil endocasts of Pterosauria (grey), Cerebavis cenomanica (green), Archaeopteryx lithographica (red), Halszkaraptor escuillei (yellow), and Heterodontosaurus tucki (brown).

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Extended Data Figure 3. Exemplified measurements of endocranial doming. Illustrated measurements for a) Ficedula albicollis, and b) Crocodylus niloticus. Green line captures endocast length between the anteriormosttip of the telencephalon and the opisthion (“D”). Red line depicts the length between the same points measured as a convex hull along the dorsal surface of the endocast (“C”). Positioning of Type I (c) and semilandmarks (d). Type I landmarks envelope telencephalic shape (orange area) and rhomboncephalic shape (yellow area). Scale bar length: a) 1.5 mm, b) 10 mm, c) and d) 5mm.

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Extended Data Figure 4. Cerebral organisation of Archaeopteryx and wulst location in modern birds. A) Full left lateral view of the endocast of the London specimen of Archaeopteryx; B) Detailed left lateral view of the endocast of the London specimen of Archaeopteryx; C) Detailed right lateral view of the endocast of the London specimen of Archaeopteryx; D) Slice view through the braincase of the London specimen of Archaeopteryx at position of tentative “wulst”1; E) Reconstructed partial endocast of Munich specimen of Archaeopteryx superimposed on endocast

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silhouette of London specimen of Archaeopteryx in grey; F) Left lateral left view of the telencephalic region of the Munich specimen of Archaeopteryx endocast; G) Slice view of the braincase of the Munich specimen of Archaeopteryx at position of tentative “wulst”1; H) Reconstructed partial endocast of Daiting specimen of Archaeopteryx with discernible brain partitioning; I) Reconstructed partial endocast of Eichstätt specimen of Archaeopteryx with discernible brain partitioning; J) Three-dimensional visualisation of the endocast of the white owl Bubo scandiacus; K) Slice view of the braincase of the Daiting specimen of Archaeopteryx, location of possible wulst presence as described by Balanoff et al. 2013; L) Slide view of the braincase of the Eichstätt specimen of Archaeopteryx at position of tentative “wulst”1; M) Slice view of the braincase of B.scandiacus at position of wulst (W). Abbreviations: Cb-Cerebrum; Cbl-Cerebellum; OT-Optic tectum. Scale bar: A-E-3,5 mm; B-C-F-I-1,5 mm; D-0,3 mm; G-0,85 mm; H-3 mm; J-4 mm; K-0,8 mm; L-0,65 mm; M-0,25 mm.

F-Test for Equality of Two Variances t-test: Two-Sample Assuming Unequal Variances

Variable 1 Variable 2 Variable 1 Variable 2 Mean 1,55557807 1,32548981 Mean 1,55557807 1,32548981

Variance 0,10694632 0,07108515 Variance 0,10694632 0,07108515 Observations 13 46 Observations 13 46 df 12 45 Pooled Variance 0,07863487 Hypothesized Mean F 1,50448181 Difference 0

P(F<=f) one-tail 0,15808312 df 57 F Critical one- tail 1,97449795 t Stat 2,61223033 P(T<=t) one-tail 0,00573997 t Critical one-tail 1,67202889

P(T<=t) two-tail 0,01147995 t Critical two-tail 2,00246546

Supplementary Table 2. Statistics of F-Test for Equality of Two Variances and t-test for Two Samples Assuming Unequal Variances comparing the ontogenetic trajectories of Crocodylus niloticus and Gallus gallus.

Extended Data Table

157

Developmental Class Order Family Genus Species Data origin stage

Lepidosauria Amphisbaenia Rhineuridae Spathorhynchus fossorium CT Adult Lepidosauria Amphisbaenia Trogonophidae Diplometodon zarudnyi CT Adult Lepidosauria Lacertilia Agamidae Physignathus cocincinus CT Adult Lepidosauria Lacertilia Anguidae Anguis fragilis ESRF Adult Lepidosauria Lacertilia Anguidae Ophisaurus apodus CT Adult Lepidosauria Lacertilia Chamaeleonidae Chamaeleo calyptratus CT Adult Lepidosauria Lacertilia Cordylidae Platysaurus imperatus CT Adult Lepidosauria Lacertilia Gekkonidae Coleonyx variegatus CT Adult Lepidosauria Lacertilia Gekkonidae Gecko sp. ESRF Adult Lepidosauria Lacertilia Gekkonidae Gecko sp. ESRF Adult Lepidosauria Lacertilia Gerrhosauridae Zonosaurus ornatus CT Adult Lepidosauria Lacertilia Helodermatidae Heloderma horridum CT Adult Lepidosauria Lacertilia Helodermatidae Heloderma suspectum CT Adult Lepidosauria Lacertilia Iguanidae Anolis carolinensis CT Adult Lepidosauria Lacertilia Iguanidae Crotaphytus collaris CT Adult Lepidosauria Lacertilia Iguanidae Ctenosaura pectinata CT Adult Lepidosauria Lacertilia Iguanidae Dipsosaurus dorsalis CT Adult Lepidosauria Lacertilia Iguanidae Gambelia wislizenii CT Adult Lepidosauria Lacertilia Iguanidae Iguania sp. ESRF Adult Lepidosauria Lacertilia Iguanidae Sauromalus ater CT Adult Lepidosauria Lacertilia Iguanidae Uta stansburiana CT Adult Lepidosauria Lacertilia Lacertidae Podarcis muralis ESRF Adult Lepidosauria Lacertilia Lacertidae Podarcis muralis ESRF Adult Lepidosauria Lacertilia Lacertidae Podarcis muralis ESRF Adult Lepidosauria Lacertilia Lacertidae Podarcis muralis ESRF Adult Lepidosauria Lacertilia Lacertidae Podarcis muralis ESRF Adult Lepidosauria Lacertilia Lacertidae Podarcis muralis ESRF Adult Lepidosauria Lacertilia Lacertidae Podarcis muralis ESRF Adult Lepidosauria Lacertilia Lacertidae Podarcis muralis ESRF Adult Lepidosauria Lacertilia Lacertidae Podarcis muralis ESRF Adult Lepidosauria Lacertilia Lanthanotidae Lanthanotus borneensis CT Adult Lepidosauria Lacertilia Lanthanotidae Lanthanotus borneensis CT Adult Lepidosauria Lacertilia Scincidae Eumeces fasciatus CT Adult Lepidosauria Lacertilia Shinisauridae Shinisaurus crocodilurus CT Adult Lepidosauria Lacertilia Teiidae Tupinambis teguixin CT Adult Lepidosauria Lacertilia Tropiduriidae Uranoscodon superciliosus CT Adult Lepidosauria Lacertilia Varanidae Varanus exanthematicus CT Adult Lepidosauria Lacertilia Varanidae Varanus exanthematicus ESRF Adult Lepidosauria Lacertilia Xantusiidae Lepidophyma flavimaculatum CT Adult Lepidosauria Mosasauridae Mosasaurinae Plotosaurus bennisoni CT Adult Lepidosauria Rhynchocephalia Sphenodontidae Sphenodon punctatus CT Adult Lepidosauria Serpentes Anomochilidae Anomochilus leonardi CT Adult Lepidosauria Serpentes Boidae Boa constrictor CT Adult Lepidosauria Serpentes Boidae Calabaria reinhardtii CT Adult Lepidosauria Serpentes Boidae Eryx colibrinus CT Adult Lepidosauria Serpentes Bolyeriidae Casarea dussumieri CT Adult Lepidosauria Serpentes Colubridae Lampropeltis getula CT Adult Lepidosauria Serpentes Colubridae Thamnophis marcianus CT Adult Lepidosauria Serpentes Cylindrophiidae Cylindrophus ruffus CT Adult Lepidosauria Serpentes Elapidae Cobra sp. CT Adult Lepidosauria Serpentes Elapidae Micrurus fulvius CT Adult Lepidosauria Serpentes Elapidae Naja naja CT Adult Lepidosauria Serpentes Leptotyphlidae Leptotyphlops dulcis CT Adult Lepidosauria Serpentes Loxocemidae Loxocemus bicolor CT Adult Lepidosauria Serpentes Pythonidae Aspidites melanocephalus CT Adult Lepidosauria Serpentes Pythonidae Python molurus CT Adult

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Lepidosauria Serpentes Pythonidae Python sp. CT Adult Lepidosauria Serpentes Tropidophiidae Tropidophis haetianus CT Adult Lepidosauria Serpentes Viperidae Lachesis muta CT Adult Lepidosauria Serpentes Viperidae Vipera sp. ESRF Adult Lepidosauria Serpentes Uropeltidae Uropeltis woodmasoni CT Adult Lepidosauria Serpentes Xenopeltidae Xenopeltis unicolor CT Adult

Phytosauria Phytosauridae Ebrachosuchidae Ebrachosuchus neukami 1 Adult Phytosauria Phytosauridae Parasuchidae Parasuchus angustifrons 1 Adult Pseudosuchia Ornithosuchidae Aetosauridae Desmatosuchus spurensis 2 Adult Pseudosuchia Ornithosuchidae Riojasuchidae Riojasuchus tenuiceps 3 Adult

Crocodilomorpha Neosuchia Dyrosauridae Rhabdognathus sp. 4 Adult Crocodilomorpha Neosuchia Eusuchia Alligator mississipiensis 5 Adult Crocodilomorpha Neosuchia Eusuchia Alligator mississipiensis ESRF Adult Crocodilomorpha Neosuchia Eusuchia Alligator mississipiensis ESRF Adult Crocodilomorpha Neosuchia Eusuchia Alligator mississipiensis CT Adult Crocodilomorpha Neosuchia Eusuchia Alligator mississipiensis 4 Adult Crocodilomorpha Neosuchia Eusuchia Caiman crocodylus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Caiman crocodylus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Caiman crocodylus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Caiman crocodylus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Caiman crocodylus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Caiman crocodylus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Caiman crocodylus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Caiman crocodylus 3 Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus acutus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus cataphractus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus cataphractus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus johnstoni 4 Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus moreletti ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult

159

Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus CT Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus 4 Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus novaeguinae ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus porosus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus porosus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus porosus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Crocodylus sp. ESRF Adult Crocodilomorpha Neosuchia Eusuchia Leidyosuchus canadensis 4 Adult Crocodilomorpha Neosuchia Eusuchia Melanosuchus niger 4 Adult Crocodilomorpha Neosuchia Eusuchia Osteolaemus tetraspis ESRF Adult Crocodilomorpha Neosuchia Eusuchia Paleosuchus palpebrosus CT Adult Crocodilomorpha Neosuchia Eusuchia Paleosuchus trigonatus ESRF Adult Crocodilomorpha Neosuchia Eusuchia Tomistoma schlegelii CT Adult Crocodilomorpha Neosuchia Thalattosuchia Pelagosaurus typus 6 Adult Crocodilomorpha Notosuchia Peirosauridae Hamadasuchus rebouli 4 Adult Crocodilomorpha Notosuchia Sebecidae Sebecus icaeorhinus 2 Adult

Ornithodira Pterosauria Azdarchidae Araripesaurus santanae ESRF Adult Ornithodira Pterosauria Azdarchidae Tropeognathus mesembrinus ESRF Adult Ornithodira Pterosauria Breviquartossa Alkaruen koi 7 Adult Ornithodira Pterosauria Rhamphorhynchidae Parapsicephalus purdoni 2 Adult Ornithodira Pterosauria Rhamphorhynchidae Rhamphorhynchus muensteri 8 Adult

160

Ornithischia Ceratopsia Ceratopsidae Anchiceratops ornatus 2 Adult Ornithischia Ceratopsia Ceratopsidae Pachyrhinosaurus lakustai 9 Adult Ornithischia Ceratopsia Protoceratopsidae Protoceratops grangeri 2 Adult Ornithischia Ceratopsia Psittacosauridae Psittacosaurus lujiatnensis 10 Adult Ornithischia Ornithopoda Hadrosauridae Amurosaurus riabini 11 Adult Ornithischia Ornithopoda Hadrosauridae Corythosaurus sp. 12 Juvenile Ornithischia Ornithopoda Hadrosauridae Corythosaurus sp. 12 Subadult Ornithischia Ornithopoda Hadrosauridae Edmontosaurus sp. 13 Adult Ornithischia Ornithopoda Hadrosauridae Hypacrosaurus altispinus 12 Adult Ornithischia Ornithopoda Hadrosauridae Kritosaurus notabilis 2 Adult Ornithischia Ornithopoda Hadrosauridae Lambeosaurus sp. 12 Adult Ornithischia Ornithopoda Hadrosauridae Parasaurolophus sp. 14 Adult Ornithischia Ornithopoda Hadrosauridae Tenontosaurus tilleti 15 Adult Ornithischia Ornithopoda Heterodontosauridae Heterodontosaurus tucki ESRF Adult Ornithischia Ornithopoda Iguanodontidae Arenysaurus ardevoli 16 Adult Ornithischia Ornithopoda Iguanodontidae Dysalotosaurus lettowvorbecki 17 Juvenile Ornithischia Ornithopoda Iguanodontidae Dysalotosaurus lettowvorbecki 17 Subadult Ornithischia Ornithopoda Iguanodontidae Iguanodon bernissartensis 18 Adult Ornithischia Pachycephalosauria Pachycephalosauridae Pachycephalosaurus grangeri 2 Adult Ornithischia Pachycephalosauria Pachycephalosauridae Stegoceras validus 2 Adult Ornithischia Thyreophora Ankylosauridae Euoplocephalus tutus 19 Adult Ornithischia Thyreophora Ankylosauridae Kunbarrasaurus ieversi 20 Adult Ornithischia Thyreophora Ankylosauridae Pawpawsaurus campbelli 21 Adult Ornithischia Thyreophora Stegosauridae Stegosaurus armatus 2 Adult Ornithischia Thyreophora Stegosauridae Stegosaurus stenops 20 Adult

Saurischia Sauropoda Camarasauridae Camarasaurus lentus 22 Adult Saurischia Sauropoda Cetiosauridae Shunosaurus lii 22 Adult Saurischia Sauropoda Diplodocidae Amargasaurus cazani 23 Adult Saurischia Sauropoda Diplodocidae Diplodocus longus 24 Adult Saurischia Sauropoda Rebbachisauridae Nigersaurus taquetii 25 Adult Saurischia Sauropoda Saltasauridae Bonatitan reigni 26 Adult Saurischia Sauropoda Titanosauridae Ampelosaurus sp. 27 Adult Saurischia Sauropoda Vulcanodontidae Spinophorosaurus nigerensis 28 Adult Saurischia Theropoda Abelisauridae Arcovenator escotae ESRF Adult Saurischia Theropoda Abelisauridae Aucasaurus garridoi 29 Adult Saurischia Theropoda Abelisauridae Majungasaurus crenatissimus 30 Adult Saurischia Theropoda Allosauridae Allosaurus fragilis 24 Adult Saurischia Theropoda Carcharodontosauridae Acrocanthosaurus atokensis 31 Adult Saurischia Theropoda Carcharodontosauridae Carcharodontosaurus saharicus 32 Adult Saurischia Theropoda Carcharodontosauridae Giganotosaurus carolinii 33 Adult Saurischia Theropoda Ceratosauridae Ceratosaurus magnicornis 34 Adult Saurischia Theropoda Dilophosauridae Sinosaurus triassicus 35 Adult Saurischia Theropoda Metriacanthosauridae Sinraptor dongi 36 Adult Saurischia Theropoda Tyrannosauridae Alioramus altai 37 Adult Saurischia Theropoda Tyrannosauridae Gorgosaurus libratus 24 Adult Saurischia Theropoda Tyrannosauridae Nanotyrannus lancensis 24 Juvenile ? Saurischia Theropoda Tyrannosauridae Tarbosaurus bataar 38 Adult Saurischia Theropoda Tyrannosauridae Tyrannosaurus rex 24 Adult Saurischia Theropoda Tyrannosauridae Tyrannosaurus rex 24 Adult Saurischia Theropoda Tyrannosauridae Tyrannosaurus rex 24 Adult Saurischia Theropoda Therizinosauridae Erlikosaurus andrewsii 39 Adult Saurischia Theropoda Compsognathidae Compsognathus longipes ESRF subadult

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Saurischia Theropoda Ornithomimidae Garudimimus brevipes 40 Adult Saurischia Theropoda Ornithomimidae Ornithomimus edmontonicus 41 Adult Saurischia Theropoda Ornithomimidae Struthiomimus altus 24 Adult Saurischia Theropoda Oviraptoridae Citipati osmolskae 42 Adult Saurischia Theropoda Oviraptoridae Conchoraptor gracilis 42 Adult Saurischia Theropoda Oviraptoridae Incisivosaurus gauthieri 43 Adult Saurischia Theropoda Oviraptoridae Khaan mckennai 42 Adult Saurischia Theropoda Dromaeosauridae Bambiraptor feinbergi 44 Adult Saurischia Theropoda Dromaeosauridae Deinonychus anthirropus 24 Adult Saurischia Theropoda Troodontidae Zanabazar junior 42 Adult Saurischia Theropoda Halszkaraptorinae Halszkaraptor escuillei ESRF subadult Saurischia Theropoda Archaeopterygidae Archaeopteryx lithographica ESRF subadult Saurischia Theropoda Archaeopterygidae Archaeopteryx lithographica ESRF subadult Saurischia Theropoda Archaeopterygidae Archaeopteryx lithographica 45 subadult

Ornithuromorpha Ornithurae Cerebavis cenomanica 45 Adult

Paleognathae Aepyornithiformes Aepyornithidae Aepyornis maximus CT Adult Paleognathae Apterygiformes Apterygidae Apteryx owenii ESRF Adult Paleognathae Apterygiformes Apterygidae Apteryx mantelli CT Adult Paleognathae Casuariformes Casuariidae Casuarius casuarius CT Adult Paleognathae Casuariformes Dromaiidae Dromaius novaehollandiae CT Adult Paleognathae Casuariformes Dromaiidae Dromaius novaehollandiae ESRF Adult Paleognathae Dinornithiformes Dinornithidae Dinornis giganteus 47 Adult Paleognathae Dinornithiformes Dinornithidae Dinornis sp. ESRF Adult Paleognathae Dinornithiformes Dinornithidae Dinornis sp. ESRF Adult Paleognathae Dinornithiformes Emeidae Anomalopteryx didiformis 47 Adult Paleognathae Dinornithiformes Emeidae Emeus crassus 47 Adult Paleognathae Dinornithiformes Emeidae Emeus curtus 47 Adult Paleognathae Dinornithiformes Emeidae Emeus gravis 47 Adult Paleognathae Dinornithiformes Emeidae Emeus gravis 47 Adult Paleognathae Dinornithiformes Emeidae Pachyornis australis 47 Adult Paleognathae Dinornithiformes Emeidae Pachyornis elephantopus 47 Adult Paleognathae Lithornitiformes Lithornithidae Lithornis plebius 48 Adult Paleognathae Rheiformes Rheidae Rhea americana 49 Adult Paleognathae Rheiformes Rheidae Rhea americana CT Adult Paleognathae Rheiformes Rheidae Rhea americana CT Adult Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF Adult Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF Adult Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF Adult Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF Adult Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF Adult Paleognathae Tinamiformes Tinamidae Nothoprocta ornata 50 Adult Paleognathae Tinamiformes Tinamidae Nothura boraquira 50 Adult Paleognathae Tinamiformes Tinamidae Nothura darwinii 50 Adult Paleognathae Tinamiformes Tinamidae Rhynchotus rufescens 50 Adult Paleognathae Tinamiformes Tinamidae Tinamous major 50 Adult

Neognathae Accipitriformes Accipitridae Accipiter gentilis CT Adult Neognathae Accipitriformes Accipitridae Accipiter nisus CT Adult Neognathae Accipitriformes Accipitridae Buteo buteo CT Adult Neognathae Accipitriformes Accipitridae Buteo lagopus CT Adult Neognathae Accipitriformes Accipitridae Circaetus gallicus ESRF Adult

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Neognathae Accipitriformes Accipitridae Haliaeetus leucocephalus CT Adult Neognathae Accipitriformes Accipitridae Milvus aegypticus CT Adult Neognathae Accipitriformes Accipitridae Neophron percnopterus ESRF Adult Neognathae Accipitriformes Accipitridae Pernis apivorius ESRF Adult Neognathae Accipitriformes Accipitridae Stephanoaetus coronatus CT Adult Neognathae Accipitriformes Cathartidae Gyps fulvus ESRF Adult Neognathae Accipitriformes Cathartidae Cathartes aura CT Adult Neognathae Accipitriformes Cathartidae Coragyps atratus CT Adult Neognathae Accipitriformes Cathartidae Sarcoramphus papa ESRF Adult Neognathae Accipitriformes Cathartidae Vultur gryphus ESRF Adult Neognathae Accipitriformes Sagittaridae Sagittarius serpentarius CT Adult Neognathae Anseriformes Anatidae Anas clypeata CT Adult Neognathae Anseriformes Anatidae Anas crecca CT Adult Neognathae Anseriformes Anatidae Anas plathyrhynchos CT Adult Neognathae Anseriformes Anatidae Chenonetta jubata CT Adult Neognathae Anseriformes Anatidae Cygnus olor CT Adult Neognathae Anseriformes Anatidae Nettapus auritus CT Adult Neognathae Anseriformes Anatidae Oxyura leucocephala CT Adult Neognathae Anseriformes Anatidae Tadorna tadorna CT Adult Neognathae Anseriformes Anatidae Callonetta leucophrys CT Adult Neognathae Anseriformes Anatidae Cereopsis novaehollandiae CT Adult Neognathae Anseriformes Anhimidae Chauna chavaria ESRF Adult Neognathae Anseriformes Anseranatidae Anseranas semipalmata CT Adult Neognathae Anseriformes Anseridae Anser albifrons CT Adult Neognathae Anseriformes Anseridae Anser anser CT Adult Neognathae Anseriformes Anseridae Anser erythropus CT Adult Neognathae Anseriformes Anseridae Branta canadensis CT Adult Neognathae Anseriformes Presbyornithidae Presbyornis sp. 48 Neognathae Apodiformes Apodidae Apus pallidus ESRF Fledgeling Neognathae Apodiformes Apodidae Panyptila melanoleuca ESRF Adult Neognathae Apodiformes Trochilidae Thalurania furcata CT Adult Neognathae Bucerotiformes Bucerotidae Aceros corrigatus CT Adult Neognathae Bucerotiformes Bucerotidae Aceros plicatus CT Adult Neognathae Bucerotiformes Bucerotidae Anthracoceros malayanius CT Adult Neognathae Bucerotiformes Bucerotidae Bycanistes bucinator CT Adult Neognathae Bucerotiformes Bucerotidae Bycanistes cylindricus CT Adult Neognathae Bucerotiformes Bucerotidae Bycanistes fistulator CT Adult Neognathae Bucerotiformes Bucerotidae Bycanistes subcylindricus CT Adult Neognathae Bucerotiformes Bucerotidae Buceros cassidix CT Adult Neognathae Bucerotiformes Bucerotidae Ceratogymna atrata CT Adult Neognathae Bucerotiformes Bucerotidae Ceratogymna elata CT Adult Neognathae Bucerotiformes Bucerotidae Rhyticeros undulatus CT Adult Neognathae Bucerotiformes Bucerotidae Tockus deckeni CT Adult Neognathae Bucerotiformes Bucerotidae Tockus erythrorhynchus CT Adult Neognathae Bucerotiformes Bucorvidae Bucorvus abyssinicus ESRF Adult Neognathae Bucerotiformes Bucorvidae Bucorvus leadbeateri CT Adult Neognathae Bucerotiformes Upupidae Upupa epops CT Adult Neognathae Cariamiformes Cariamidae Cariama cristata CT Adult Neognathae Charadriiformes Alcidae Alca torda ESRF Adult Neognathae Charadriiformes Alcidae Alle alle CT Adult Neognathae Charadriiformes Alcidae Fratercula arctica CT Adult Neognathae Charadriiformes Alcidae Pinguinus impennis ESRF Adult Neognathae Charadriiformes Alcidae Uria aalge ESRF Adult Neognathae Charadriiformes Haematopidae Haematopus ostralegus CT Adult Neognathae Charadriiformes Jacanidae Actophilornis africanus CT Adult

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Neognathae Charadriiformes Laridae Chroicocephalus ridibundus CT Adult Neognathae Charadriiformes Laridae Larus argentatus ESRF Adult Neognathae Charadriiformes Laridae Larus marinus CT Adult Neognathae Charadriiformes Laridae Larus michaellis CT Adult Neognathae Charadriiformes Scolopacidae Gallinago gallinago CT Adult Neognathae Charadriiformes Scolopacidae Scolopax minor CT Adult Neognathae Charadriiformes Scolopacidae Scolopax rusticola CT Adult Neognathae Ciconiiformes Ciconidae Ciconia ciconia ESRF Adult Neognathae Ciconiiformes Ciconidae Ephippiorhynchus senegalensis CT Adult Neognathae Ciconiiformes Ciconidae Leptoptylos crumeniferus CT Adult Neognathae Ciconiiformes Ciconidae Mycteria ibis CT Adult Neognathae Columbiformes Columbinae Columba oenas CT Adult Neognathae Columbiformes Columbinae Gallicolumba luzonica CT Adult Neognathae Columbiformes Columbinae Ocyphaps lophotes CT Adult Neognathae Columbiformes Columbinae Phaps chalcoptera CT Adult Neognathae Columbiformes Columbinae Streptopelia tranquebarica CT Adult Neognathae Columbiformes Otidiphabinae Otidiphaps nobilis CT Adult Neognathae Columbiformes Raphinae Raphus cucullatus 51 Adult Neognathae Columbiformes Raphinae Pezophaps solitaria 51 Adult Neognathae Coraciiformes Alcedinidae Ceryle rudis ESRF Adult Neognathae Coraciiformes Meropidae Merops apiaster CT Adult Neognathae Coraciiformes Meropidae Merops viridis CT Adult Neognathae Cuculiformes Cuculidae Geococcyx californianus ESRF Adult Neognathae Cuculiformes Cuculidae Guira guira CT Adult Neognathae Cuculiformes Opisthocomidae Opisthocomus hoazin ESRF Adult Neognathae Falconiformes Falconidae Falco cherrug CT Adult Neognathae Falconiformes Falconidae Falco subbuteo CT Adult Neognathae Falconiformes Falconidae Falco tinnunculus CT Adult Neognathae Galliformes Cracidae Crax mitu ESRF Adult Neognathae Galliformes Numididae Acryllium vulturinum CT Adult Neognathae Galliformes Numididae Numida meleagris CT Adult Neognathae Galliformes Odontophoridae Callipepla squamata CT Adult Neognathae Galliformes Phasianidae Crossoptilon auritum CT Adult Neognathae Galliformes Phasianidae Gallus gallus ESRF Adult Neognathae Galliformes Phasianidae Lagopus mutus ESRF Adult Neognathae Galliformes Phasianidae Pavo cristatus CT Adult Neognathae Galliformes Phasianidae Perdix perdix CT Adult Neognathae Galliformes Phasianidae Phasianus colchicus ESRF Adult Neognathae Galliformes Phasianidae Rollulus rouloul CT Adult Neognathae Galliformes Phasianidae Tetrao tetryx CT Adult Neognathae Galliformes Phasianidae Tetrao urogallus CT Adult Neognathae Gruiformes Gruidae Balearica regulorum CT Adult Neognathae Gruiformes Gruidae Grus grus ESRF Adult Neognathae Gruiformes Gruidae Grus canadensis CT Adult Neognathae Passeriformes Corvidae Coloeus monedula CT Adult Neognathae Passeriformes Corvidae Corvus albicollis CT Adult Neognathae Passeriformes Corvidae Corvus corone CT Adult Neognathae Passeriformes Corvidae Corvus corax CT Adult Neognathae Passeriformes Corvidae Pica pica CT Adult Neognathae Passeriformes Emberizidae Emberiza citrinella CT Adult Neognathae Passeriformes Estrildidae Erythrura trichroa ESRF Adult Neognathae Passeriformes Estrildidae Lonchura punctulata CT Adult Neognathae Passeriformes Estrildidae Taeniopygia guttata CT Adult Neognathae Passeriformes Fringillidae Fringilla coelebs CT Adult Neognathae Passeriformes Fringillidae Loxia curvirostra CT Adult

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Neognathae Passeriformes Leiotrichidae Garrulax chinensis CT Adult Neognathae Passeriformes Leiotrichidae Liocichla omeiensis CT Adult Neognathae Passeriformes Muscicapidae Ficedula albicollis ESRF Adult Neognathae Passeriformes Muscicapidae Phoenicurus phoenicurus CT Adult Neognathae Passeriformes Panuridae Panurus biarmicus CT Adult Neognathae Passeriformes Paridae Cyanistes caeruleus ESRF Adult Neognathae Passeriformes Paridae Parus major Protivin Museum Adult Neognathae Passeriformes Passerida Passer domesticus ESRF Juvenile Neognathae Passeriformes Passerida Passer domesticus ESRF Juvenile Neognathae Passeriformes Passerida Passer domesticus ESRF Juvenile Neognathae Passeriformes Sturnidae Gracula religiosa CT Adult Neognathae Passeriformes Sturnidae Leucopsar rothschildii CT Adult Neognathae Passeriformes Sturnidae Scissirostrum dubium CT Adult Neognathae Passeriformes Sturnidae Sturnus vulgaris CT Adult Neognathae Passeriformes Turdidae Turdus philomelos CT Adult Neognathae Passeriformes Turdidae Zoothera citrina CT Adult Neognathae Pelecaniformes Ardeidae Ardea cinerea ESRF Adult Neognathae Pelecaniformes Ardeidae Bubulcus ibis ESRF Adult Neognathae Pelecaniformes Ardeidae Nycticorax nycticorax CT Adult Neognathae Pelecaniformes Pelecanidae Pelecanus crispus CT Adult Neognathae Pelecaniformes Threskiornithidae Geronticus eremita CT Adult Neognathae Pelecaniformes Threskiornithidae Platalea alba CT Adult Neognathae Pelecaniformes Threskiornithidae Plegadis falcinellus CT Adult Neognathae Pelecaniformes Threskiornithidae Threskiornis aethiopicus ESRF Adult Neognathae Pelecaniformes Threskiornithidae Threskiornis aethiopicus CT Adult Neognathae Phoenicopteriformes Phoenicopteridae Phoeniconaias minor CT Adult Neognathae Phoenicopteriformes Phoenicopteridae Phoenicopterus roseus CT Adult Neognathae Piciformes Megalaimidae Megalaima sp. ESRF Adult Neognathae Piciformes Picidae Dryocopus martius CT Adult Neognathae Piciformes Picidae Picus viridis CT Adult Neognathae Piciformes Rhamphastidae Pteroglossus aracari CT Adult Neognathae Piciformes Rhamphastidae Pteroglossus viridis CT Adult Neognathae Piciformes Rhamphastidae Rhamphastos vitellinus CT Adult Neognathae Podicipediformes Podicipedidae Podilymbus cristatus CT Adult Neognathae Podicipediformes Podicipedidae Tachybaptus ruficollis CT Adult Neognathae Procellariformes Diomedeidae Thalassarche melenophris CT Adult Neognathae Procellariformes Procellaridae Fulmarus glacialis ESRF Adult Neognathae Psittaciformes Cacatuidae Caccatua moluccensis CT Adult Neognathae Psittaciformes Cacatuidae Eolophus rosecapillus CT Adult Neognathae Psittaciformes Psittacidae Agapornis personatus CT Adult Neognathae Psittaciformes Psittacidae Alisterus scapularis CT Adult Neognathae Psittaciformes Psittacidae Amazona farinosa CT Adult Neognathae Psittaciformes Psittacidae Amazona leucocephala CT Adult Neognathae Psittaciformes Psittacidae Ara ararauna CT Adult Neognathae Psittaciformes Psittacidae Ara chloropterus CT Adult Neognathae Psittaciformes Psittacidae Ara militaris CT Adult Neognathae Psittaciformes Psittacidae Deroptyus accipitrinus CT Adult Neognathae Psittaciformes Psittacidae Loriculus galgulus CT Adult Neognathae Psittaciformes Psittacidae Melopsittacus undulatus CT Adult Neognathae Psittaciformes Psittacidae Orthopsittaca manilata CT Adult Neognathae Psittaciformes Psittacidae Psittacula eupatria CT Adult Neognathae Psittaciformes Psittacidae Psittacula krameri CT Adult Neognathae Psittaciformes Psittacidae Psittaculirostris desmarestii CT Adult Neognathae Psittaciformes Strigopidae Strigops habroptilus ESRF Adult Neognathae Sphenisciformes Spheniscidae Eudyptula minor CT Adult

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Neognathae Sphenisciformes Spheniscidae Eudyptula minor ESRF Adult Neognathae Sphenisciformes Spheniscidae Spheniscus demersus ESRF Adult Neognathae Sphenisciformes Spheniscidae Spheniscus humboldti CT Adult Neognathae Strigiformes Strigidae Asio otus CT Adult Neognathae Strigiformes Strigidae Bubo africanus CT Adult Neognathae Strigiformes Strigidae Bubo bubo CT Adult Neognathae Strigiformes Strigidae Bubo scandiacus CT Adult Neognathae Strigiformes Strigidae Bubo scandiacus ESRF Adult Neognathae Strigiformes Strigidae Otus scops CT Adult Neognathae Strigiformes Strigidae Strix nebulosa CT Adult Neognathae Strigiformes Tytonidae Tyto alba CT Adult Neognathae Suliformes Phalacrocoracidae Phalacrocorax capensis CT Adult Neognathae Suliformes Phalacrocoracidae Phalacrocorax carbo ESRF Adult Neognathae Suliformes Phalacrocoracidae Phalacrocorax penicillatus CT Adult Neognathae Suliformes Sulidae Sula bassanus ESRF Adult

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Inventory Number / Repository Genus Species institution Data availability D C

Spathorhynchus fossorium Digimorph www.digimorph.org 17,12 17,93

Diplometodon zarudnyi Digimorph www.digimorph.org 4,93 5,38

Physignathus cocincinus Digimorph www.digimorph.org 13,35 14,66 Anguis fragilis ESRF collection paleo.esrf.eu 7,41 7,45

Ophisaurus apodus Digimorph www.digimorph.org 18,10 18,49

Chamaeleo calyptratus Digimorph www.digimorph.org 17,34 17,76

Platysaurus imperatus Digimorph www.digimorph.org 12,03 12,57

Coleonyx variegatus Digimorph www.digimorph.org 6,39 6,58 Gecko sp. ESRF collection paleo.esrf.eu 4,95 5,07 Gecko sp. ESRF collection paleo.esrf.eu 20,00 20,98

Zonosaurus ornatus Digimorph www.digimorph.org 10,28 10,72

Heloderma horridum Digimorph www.digimorph.org 36,42 37,24

Heloderma suspectum Digimorph www.digimorph.org 23,08 24,63

Anolis carolinensis Digimorph www.digimorph.org 7,67 8,21

Crotaphytus collaris Digimorph www.digimorph.org 12,29 13,49

Ctenosaura pectinata Digimorph www.digimorph.org 21,68 21,92

Dipsosaurus dorsalis Digimorph www.digimorph.org 10,41 11,17

Gambelia wislizenii Digimorph www.digimorph.org 9,03 9,63 Iguania sp. LFAC paleo.esrf.eu 23,75 25,10

Sauromalus ater Digimorph www.digimorph.org 15,83 17,21

Uta stansburiana Digimorph www.digimorph.org 5,68 6,10 Podarcis muralis ESRF collection paleo.esrf.eu 7,58 8,05 Podarcis muralis ESRF collection paleo.esrf.eu 6,45 6,67 Podarcis muralis ESRF collection paleo.esrf.eu 8,55 8,79 Podarcis muralis ESRF collection paleo.esrf.eu 7,43 7,98 Podarcis muralis ESRF collection paleo.esrf.eu 4,92 5,14 Podarcis muralis ESRF collection paleo.esrf.eu 6,25 6,44 Podarcis muralis ESRF collection paleo.esrf.eu 5,06 5,29 Podarcis muralis ESRF collection paleo.esrf.eu 4,26 4,34 Podarcis muralis ESRF collection paleo.esrf.eu 5,50 5,84

Lanthanotus borneensis Digimorph www.digimorph.org 11,07 11,24

Lanthanotus borneensis Digimorph www.digimorph.org 12,10 12,37

Eumeces fasciatus Digimorph www.digimorph.org 5,60 5,70

Shinisaurus crocodilurus Digimorph www.digimorph.org 14,20 14,61

Tupinambis teguixin Digimorph www.digimorph.org 26,80 27,36

Uranoscodon superciliosus Digimorph www.digimorph.org 12,24 12,62

Varanus exanthematicus Digimorph www.digimorph.org 22,03 23,16 Varanus exanthematicus LFAC paleo.esrf.eu 40,26 41,81

Lepidophyma flavimaculatum Digimorph www.digimorph.org 11,63 11,93

Plotosaurus bennisoni Digimorph www.digimorph.org 161,33 171,51

Sphenodon punctatus Digimorph www.digimorph.org 21,40 22,87

Anomochilus leonardi Digimorph www.digimorph.org 5,23 5,44

Boa constrictor Digimorph www.digimorph.org 25,09 25,74

Calabaria reinhardtii Digimorph www.digimorph.org 13,09 13,73

Eryx colibrinus Digimorph www.digimorph.org 8,91 9,12

Casarea dussumieri Digimorph www.digimorph.org 8,34 8,42

Lampropeltis getula Digimorph www.digimorph.org 17,83 18,94

Thamnophis marcianus Digimorph www.digimorph.org 11,95 12,15

Cylindrophus ruffus Digimorph www.digimorph.org 9,94 9,95

Cobra sp. Digimorph www.digimorph.org 15,56 15,85

Micrurus fulvius Digimorph www.digimorph.org 11,71 11,83

Naja naja Digimorph www.digimorph.org 16,80 17,26

Leptotyphlops dulcis Digimorph www.digimorph.org 3,51 3,67

Loxocemus bicolor Digimorph www.digimorph.org 13,11 13,28

Aspidites melanocephalus Digimorph www.digimorph.org 24,10 25,11

Python molurus Digimorph www.digimorph.org 30,36 30,49

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Python sp. Digimorph www.digimorph.org 42,02 42,17

Tropidophis haetianus Digimorph www.digimorph.org 7,92 8,01

Lachesis muta Digimorph www.digimorph.org 24,18 25,31 Vipera sp. ESRF collection paleo.esrf.eu 8,71 8,77 Uropeltis woodmasoni Digimorph 4,10 4,19 Xenopeltis unicolor Digimorph 15,30 16,02

Ebrachosuchus neukami BSPG 1931 X 501 51,58 52,30 Parasuchus angustifrons BSPG 1931 X 502 56,76 58,24 Desmatosuchus spurensis U.M. 7476 92,51 99,30 Riojasuchus tenuiceps PVL 3827 92,22 98,63

Rhabdognathus sp. CNRST-SUNY-190 76,07 77,22 Alligator mississipiensis USNM 21 1232 186,55 194,96 Alligator mississipiensis TL paleo.esrf.eu 72,61 74,15 Alligator mississipiensis TL paleo.esrf.eu 83,34 84,47

Alligator mississipiensis Digimorph www.digimorph.org 43,80 45,81 Alligator mississipiensis AL016 68,14 73,93 Caiman crocodylus ESRF collection paleo.esrf.eu 44,76 46,65 Caiman crocodylus ENS / R9 paleo.esrf.eu 48,22 50,58 Caiman crocodylus LFAC paleo.esrf.eu 42,33 44,52 Caiman crocodylus TL paleo.esrf.eu 42,50 44,49 Caiman crocodylus TL paleo.esrf.eu 57,97 58,50 Caiman crocodylus MHN Grenoble / MHN.Gr.Os.2165 paleo.esrf.eu 52,83 55,42 Caiman crocodylus MHN Grenoble / MHN.Gr.Os.2166 paleo.esrf.eu 60,32 63,89 Caiman crocodylus 54,81 55,93 Crocodylus acutus ENS / R33 paleo.esrf.eu 48,66 51,79 Crocodylus cataphractus CCEC / 90001393 paleo.esrf.eu 61,36 63,91 Crocodylus cataphractus ENS / R11 paleo.esrf.eu 56,12 57,45 Crocodylus johnstoni OUVC 10425 54,33 56,44 Crocodylus moreletti LFAC paleo.esrf.eu 75,93 78,28 Crocodylus niloticus CCEC / 90001193 paleo.esrf.eu 45,26 46,14 Crocodylus niloticus CCEC / 90001337 paleo.esrf.eu 20,65 22,75 Crocodylus niloticus CCEC / 90001395 paleo.esrf.eu 52,19 52,62 Crocodylus niloticus CCEC / 90001850 paleo.esrf.eu 36,87 39,08 Crocodylus niloticus CCEC / 90001944 paleo.esrf.eu 76,91 78,88 Crocodylus niloticus CCEC / 90001948 paleo.esrf.eu 21,72 23,90 Crocodylus niloticus CCEC / 90001990 paleo.esrf.eu 20,82 22,93 Crocodylus niloticus CCEC / 90002004 paleo.esrf.eu 22,27 24,19 Crocodylus niloticus CCEC / 90002013 paleo.esrf.eu 19,96 21,89 Crocodylus niloticus CCEC / 90002022 paleo.esrf.eu 23,45 24,98 Crocodylus niloticus CCEC / 90002050 paleo.esrf.eu 20,57 22,53 Crocodylus niloticus CCEC / 90002054 paleo.esrf.eu 21,30 23,13 Crocodylus niloticus CCEC / 90002059 paleo.esrf.eu 21,62 23,29 Crocodylus niloticus CCEC / 90002088 paleo.esrf.eu 23,25 25,08 Crocodylus niloticus CCEC / 90002112 paleo.esrf.eu 21,95 23,54 Crocodylus niloticus CCEC / 90002113 paleo.esrf.eu 19,56 21,60 Crocodylus niloticus CCEC / 90002137 paleo.esrf.eu 21,48 23,50 Crocodylus niloticus CCEC / 90002138 paleo.esrf.eu 21,64 23,30 Crocodylus niloticus CCEC / 90001394 paleo.esrf.eu 80,37 82,57 Crocodylus niloticus CCEC / 90001838 paleo.esrf.eu 74,49 75,72 Crocodylus niloticus CCEC / 90001840 paleo.esrf.eu 83,88 84,65 Crocodylus niloticus CCEC / 90001842 paleo.esrf.eu 75,41 77,41

168

Crocodylus niloticus CCEC / 90001844 paleo.esrf.eu 57,78 58,59 Crocodylus niloticus CCEC / 90001852 paleo.esrf.eu 64,40 64,94 Crocodylus niloticus CCEC / 90001855 paleo.esrf.eu 41,24 43,01 Crocodylus niloticus CCEC / 90001856 paleo.esrf.eu 57,44 58,15 Crocodylus niloticus CCEC / 90001841 paleo.esrf.eu 83,04 84,14 Crocodylus niloticus LFAC paleo.esrf.eu 76,39 78,62 Crocodylus niloticus LFAC paleo.esrf.eu 67,13 67,89 Crocodylus niloticus LFAC paleo.esrf.eu 101,04 104,64 Crocodylus niloticus LFAC paleo.esrf.eu 113,92 115,16 Crocodylus niloticus LFAC paleo.esrf.eu 85,44 87,01 Crocodylus niloticus LFAC paleo.esrf.eu 114,57 115,15 Crocodylus niloticus TL paleo.esrf.eu 80,95 81,47 Crocodylus niloticus TL paleo.esrf.eu 80,36 82,11 Crocodylus niloticus TL paleo.esrf.eu 48,59 51,06 Crocodylus niloticus TL paleo.esrf.eu 45,71 47,68 Crocodylus niloticus TL paleo.esrf.eu 44,30 47,22 Crocodylus niloticus TL paleo.esrf.eu 51,47 53,62 Crocodylus niloticus ESRF collection paleo.esrf.eu 92,75 93,75 Crocodylus niloticus MHN Grenoble / MHN.Gr.Os.65 paleo.esrf.eu 116,84 120,19 Crocodylus niloticus MHN Grenoble / MHN.Gr.Os.67 paleo.esrf.eu 89,25 90,84 Crocodylus niloticus MHN Grenoble / MHN.Gr.Os.70 paleo.esrf.eu 82,30 83,70 Crocodylus niloticus 92,33 93,54 Crocodylus novaeguinae ENS paleo.esrf.eu 55,51 56,84 Crocodylus porosus CCEC paleo.esrf.eu 84,98 88,12 Crocodylus porosus MHN Grenoble / MHN.Gr.Os.64 paleo.esrf.eu 63,34 64,38 Crocodylus porosus MHN Grenoble / MHN.Gr.Os.66 paleo.esrf.eu 91,70 94,03 Crocodylus sp. CCEC / 90001389 paleo.esrf.eu 79,40 14,05 Crocodylus sp. CCEC / 90001399 paleo.esrf.eu 78,62 81,56 Crocodylus sp. CCEC / 90001401 paleo.esrf.eu 79,24 81,32 Crocodylus sp. CCEC / 90001985 paleo.esrf.eu 84,48 85,05 Crocodylus sp. CCEC / 90001388 paleo.esrf.eu 91,53 95,18 Crocodylus sp. CCEC / 90001392 paleo.esrf.eu 81,67 83,69 Crocodylus sp. CCEC / 90001400 paleo.esrf.eu 77,50 78,52 Crocodylus sp. CCEC / 90001387 paleo.esrf.eu 102,12 104,42 Crocodylus sp. CCEC / 90001402 paleo.esrf.eu 99,56 101,77 Crocodylus sp. CCEC / 90001403 paleo.esrf.eu 92,59 94,19 Crocodylus sp. CCEC / 90000 paleo.esrf.eu 97,96 102,42 Leidyosuchus canadensis ROM 1903 65,28 66,16 Melanosuchus niger 67,94 70,81 Osteolaemus tetraspis TL paleo.esrf.eu 42,02 44,39 Paleosuchus palpebrosus Protivin Museum Morphobank 37,79 41,44 Paleosuchus trigonatus CCEC paleo.esrf.eu 25,36 27,15

Tomistoma schlegelii Digimorph www.digimorph.org 62,47 64,47 Pelagosaurus typus M1413 43,69 44,09 Hamadasuchus rebouli ROM 52620 63,57 66,34 Sebecus icaeorhinus AMNH 3160 83,69 90,47

Araripesaurus santanae BSPG 1982 I 90 paleo.esrf.eu 52,75 70,10 Tropeognathus mesembrinus BSPG 1987 I 46 paleo.esrf.eu 15,49 20,77 Alkaruen koi MPEF-PV 3613 23,65 28,24 Parapsicephalus purdoni GSM 3166 26,21 29,62 Rhamphorhynchus muensteri CM 11434 18,72 23,38

169

Anchiceratops ornatus AMNH 5259 119,59 132,40 Pachyrhinosaurus lakustai TMP 1989.55.1243 95,91 99,37 Protoceratops grangeri AMNH 6466 79,19 86,99 Psittacosaurus lujiatnensis PKUP V1053 38,51 41,08 Amurosaurus riabini IRSNB R 279 142,27 150,88 Corythosaurus sp. ROM 759 89,80 116,87 Corythosaurus sp. CMN 34825 124,86 144,00 Edmontosaurus sp. 210,56 250,01 Hypacrosaurus altispinus ROM 702 148,57 162,97 Kritosaurus notabilis AMNH 5350 176,05 198,01 Lambeosaurus sp. ROM 758 103,94 121,75 Parasaurolophus sp. RAM 14000 37,27 45,49 Tenontosaurus tilleti OMNH 58340 87,47 99,46 Heterodontosaurus tucki The Albany Museum / AM4766 paleo.esrf.eu 40,34 43,43 Arenysaurus ardevoli MPZ2008/1 115,90 138,44 Dysalotosaurus lettowvorbecki BSPG AS I 834 33,70 36,70 Dysalotosaurus lettowvorbecki MB.R.137x 44,11 49,95 Iguanodon bernissartensis OUMNH T.127 115,89 131,00 Pachycephalosaurus grangeri AMNH 1696 110,50 119,96 Stegoceras validus ROM 803 42,59 51,98 Euoplocephalus tutus AMNH 5405 97,14 105,43 Kunbarrasaurus ieversi QM F18101 70,21 74,10 Pawpawsaurus campbelli FWMSH93B.00026 75,25 83,53 Stegosaurus armatus USNM 4936 128,41 137,45 Stegosaurus stenops CM 106 106,18 116,12

Camarasaurus lentus DNM28 45,11 53,04 Shunosaurus lii ZG65430 104,40 108,82 Amargasaurus cazani MACN-N 15 98,52 114,15 Diplodocus longus CM 3452 57,00 66,72 Nigersaurus taquetii MNN GAD512 74,19 86,01 Bonatitan reigni MACN 821 63,48 69,29 Ampelosaurus sp. MCCM-HUE-8741 73,85 79,29 Spinophorosaurus nigerensis GCP-CV-4229 105,52 113,94 Arcovenator escotae MHNA-PV-2011.1 paleo.esrf.eu 120,13 130,42 Aucasaurus garridoi MCF-PVPH 236 137,36 149,51 Majungasaurus crenatissimus FMNH PR2100 108,95 119,69 Allosaurus fragilis UMNH VP 18050 116,56 130,58 Acrocanthosaurus atokensis PMNH 10146 104,82 123,76 Carcharodontosaurus saharicus SGM Din-12 163,93 182,87 Giganotosaurus carolinii MUCP-CH 1 140,81 154,49 Ceratosaurus magnicornis MWC1 81,54 93,38 Sinosaurus triassicus ZLJT01 98,25 117,53 Sinraptor dongi 130,59 138,61 Alioramus altai IGM 100/184 106,02 117,00 Gorgosaurus libratus ROM 1247 131,98 142,33 Nanotyrannus lancensis CMNH 7541 142,75 171,71 Tarbosaurus bataar PIN 553-3/1 174,20 186,23 Tyrannosaurus rex AMNH FR 5117 177,13 200,58 Tyrannosaurus rex AMNHN FR 5029 199,12 221,46 Tyrannosaurus rex FMNH PR2081 200,23 227,48 Erlikosaurus andrewsii IGM 100/111 76,76 83,47 Compsognathus longipes BSP AS I 563 paleo.esrf.eu 25,22 26,82

170

Garudimimus brevipes GIN 100/13 61,24 81,20 Ornithomimus edmontonicus RTMP 95.110.1 81,95 102,48 Struthiomimus altus TMP 90.26.1 91,86 123,32 Citipati osmolskae IGM 100/978 67,83 84,51 Conchoraptor gracilis IGM 100/973 67,43 93,83 Incisivosaurus gauthieri IVPP V 13326 40,31 54,26 Khaan mckennai IGM 100/3006 61,60 70,75 Bambiraptor feinbergi 46,21 52,93 Deinonychus anthirropus MOR 747 57,61 65,58 Zanabazar junior IGM 100/1 73,51 98,82 Halszkaraptor escuillei MPCD-102/108 paleo.esrf.eu 23,40 27,57 Archaeopteryx lithographica BMNH 37001 paleo.esrf.eu 22,56 26,28 Archaeopteryx lithographica BSP 1999 I 50 paleo.esrf.eu 24,27 29,34 Archaeopteryx lithographica BMNH 37001 22,19 26,15

Cerebavis cenomanica PIN 5028/2 15,08 23,25

Aepyornis maximus MNHN paleo.esrf.eu 68,36 85,66 Apteryx owenii MHN Grenoble / MHN.Gr.Os. paleo.esrf.eu 29,90 48,49 Apteryx mantelli Protivin Museum morphobank.org 34,61 46,97 Casuarius casuarius Protivin Museum morphobank.org 59,14 75,03 Dromaius novaehollandiae Protivin Museum morphobank.org 56,66 75,38 Dromaius novaehollandiae CCEC / D paleo.esrf.eu 48,15 62,10 Dinornis giganteus AV29786 70,90 93,36 Dinornis sp. CCEC / QZ83 paleo.esrf.eu 52,81 58,56 Dinornis sp. CCEC / DR paleo.esrf.eu 51,79 58,12 Anomalopteryx didiformis AV8548 48,74 60,47 Emeus crassus AV8305 46,73 52,14 Emeus curtus AV3798 40,97 50,92 Emeus gravis AV3772 54,22 61,58 Emeus gravis AV9285 49,93 58,35 Pachyornis australis AV36430 59,90 65,66 Pachyornis elephantopus AV3680 54,94 62,40 Lithornis plebius 24,54 29,36 Rhea americana 23,01 30,26 Rhea americana Protivin Museum morphobank.org 29,76 44,14

Rhea americana Digimorph www.digimorph.org 27,85 39,61 Struthio camelus ESRF collection paleo.esrf.eu 61,40 95,02 Struthio camelus ESRF collection paleo.esrf.eu 57,39 95,03 Struthio camelus ESRF collection paleo.esrf.eu 58,36 90,78 Struthio camelus ESRF collection paleo.esrf.eu 60,60 88,87 Struthio camelus ESRF collection paleo.esrf.eu 47,62 81,22 Nothoprocta ornata To01 20,72 28,56 Nothura boraquira Tw01 19,97 26,68 Nothura darwinii Td01 17,63 24,33 Rhynchotus rufescens Tr01 24,74 32,84 Tinamous major Tg01 22,68 30,20

Accipiter gentilis Protivin Museum / 176 morphobank.org 31,72 50,78 Accipiter nisus Protivin Museum / 765 morphobank.org 21,16 34,71 Buteo buteo Protivin Museum / 763 morphobank.org 31,78 51,63 Buteo lagopus Protivin Museum / 462 morphobank.org 32,66 53,51 Circaetus gallicus CCEC / 50001528 paleo.esrf.eu 37,54 57,06

171

Haliaeetus leucocephalus Protivin Museum / 228 morphobank.org 41,94 63,54 Milvus aegypticus Protivin Museum / 508 morphobank.org 27,94 45,32 Neophron percnopterus CCEC / 50001484 paleo.esrf.eu 34,66 53,66 Pernis apivorius CCEC / 50001539 paleo.esrf.eu 32,04 48,83 Stephanoaetus coronatus Protivin Museum / 843 morphobank.org 32,91 50,29 Gyps fulvus CCEC / 50001652 paleo.esrf.eu 31,27 50,73 Cathartes aura Protivin Museum / 658 morphobank.org 36,13 52,27 Coragyps atratus Digimorph morphobank.org 36,66 53,74 Sarcoramphus papa CCEC / 50001668 paleo.esrf.eu 57,07 77,67 Vultur gryphus CCEC / 50001624 paleo.esrf.eu 55,48 75,10 Sagittarius serpentarius Protivin Museum / 457 morphobank.org 41,34 62,41 Anas clypeata Protivin Museum / 637 morphobank.org 24,21 32,59 Anas crecca Protivin Museum / 649 morphobank.org 21,95 31,04

Anas plathyrhynchos Digimorph www.digmorph.org 25,70 33,18 Chenonetta jubata Protivin Museum / 674 morphobank.org 26,25 33,76 Cygnus olor Protivin Museum / 266 morphobank.org 40,61 47,59 Nettapus auritus Protivin Museum / 1104 morphobank.org 22,33 28,61 Oxyura leucocephala Protivin Museum / 932 morphobank.org 25,72 34,22 Tadorna tadorna Protivin Museum / 673 morphobank.org 28,89 36,11 Callonetta leucophrys Protivin Museum / 916 morphobank.org 24,06 31,52 Cereopsis novaehollandiae Protivin Museum / 1111 morphobank.org 32,09 41,44 Chauna chavaria CCEC / 50001629 paleo.esrf.eu 37,47 48,26 Anseranas semipalmata Protivin Museum / 762 morphobank.org 33,69 41,20 Anser albifrons Protivin Museum / 1092 morphobank.org 31,62 41,04 Anser anser Protivin Museum / 1091 morphobank.org 37,31 47,27 Anser erythropus Protivin Museum / 917 morphobank.org 30,80 40,53 Branta canadensis Protivin Museum / 682 morphobank.org 36,84 46,16 Presbyornis sp. 14,93 18,36 Apus pallidus ESRF collection paleo.esrf.eu 11,93 19,99 Panyptila melanoleuca CCEC / 50001438 paleo.esrf.eu 11,90 21,90 Thalurania furcata MNHN 9,72 19,00 Aceros corrigatus Protivin Museum / 970 morphobank.org 37,08 49,33 Aceros plicatus Protivin Museum / 859 morphobank.org 36,86 52,63 Anthracoceros malayanius Protivin Museum / 585 morphobank.org 32,95 46,37 Bycanistes bucinator Protivin Museum / 870 morphobank.org 33,49 46,14 Bycanistes cylindricus Protivin Museum / 779 morphobank.org 39,24 53,57 Bycanistes fistulator Protivin Museum / 776 morphobank.org 37,58 49,51 Bycanistes subcylindricus Protivin Museum / 587 morphobank.org 36,26 54,40 Buceros cassidix Protivin Museum / 860 morphobank.org 38,18 51,59 Ceratogymna atrata Protivin Museum / 845 morphobank.org 37,46 53,04 Ceratogymna elata Protivin Museum / 777 morphobank.org 37,61 49,31 Rhyticeros undulatus Protivin Museum / 514 morphobank.org 42,12 57,68 Tockus deckeni Protivin Museum / 454 morphobank.org 25,04 36,48 Tockus erythrorhynchus Protivin Museum / 455 morphobank.org 24,91 34,84 Bucorvus abyssinicus CCEC / 50001648 paleo.esrf.eu 47,03 74,14 Bucorvus leadbeateri Protivin Museum / 586 morphobank.org 47,74 71,87 Upupa epops Protivin Museum / 524 morphobank.org 17,45 25,47 Cariama cristata Protivin Museum / 665 morphobank.org 35,09 48,67 Alca torda ESRF collection paleo.esrf.eu 30,28 45,22 Alle alle Protivin Museum / 1113 morphobank.org 20,26 28,25 Fratercula arctica Protivin Museum / 559 morphobank.org 23,76 34,75 Pinguinus impennis CCEC / 50001551 paleo.esrf.eu 38,86 53,77 Uria aalge ESRF collection paleo.esrf.eu 29,14 39,71 Haematopus ostralegus Protivin Museum / 941 morphobank.org 23,96 39,61 Actophilornis africanus Protivin Museum / 642 morphobank.org 18,74 23,58

172

Chroicocephalus ridibundus Protivin Museum / 645 morphobank.org 24,40 34,20 Larus argentatus ESRF collection paleo.esrf.eu 28,69 40,50 Larus marinus Protivin Museum / 247 morphobank.org 31,18 44,73 Larus michaellis Protivin Museum / 957 morphobank.org 31,94 43,29 Gallinago gallinago Protivin Museum / 517 morphobank.org 17,75 27,88 Scolopax minor Protivin Museum / 684 morphobank.org 18,06 32,08 Scolopax rusticola Protivin Museum / 516 morphobank.org 21,71 35,30 Ciconia ciconia Peaugres paleo.esrf.eu 38,24 56,83 Ephippiorhynchus senegalensis Protivin Museum / 663 morphobank.org 43,81 61,57 Leptoptylos crumeniferus Protivin Museum / 201 morphobank.org 47,01 67,50 Mycteria ibis Protivin Museum / 394 morphobank.org 36,44 58,40 Columba oenas Protivin Museum / 647 morphobank.org 20,14 29,35 Gallicolumba luzonica Protivin Museum / 929 morphobank.org 18,34 25,50 Ocyphaps lophotes Protivin Museum / 1118 morphobank.org 18,62 27,57 Phaps chalcoptera Protivin Museum / 849 morphobank.org 20,36 27,69 Streptopelia tranquebarica Protivin Museum / 785 morphobank.org 18,90 27,27 Otidiphaps nobilis Protivin Museum / 1076 morphobank.org 21,23 31,48 Raphus cucullatus 42,72 51,16 Pezophaps solitaria 40,78 48,39 Ceryle rudis CCEC / 50001485 paleo.esrf.eu 17,96 27,57 Merops apiaster Protivin Museum / 877 morphobank.org 13,24 25,44 Merops viridis Protivin Museum / 963 morphobank.org 12,68 25,61 Geococcyx californianus MNHN paleo.esrf.eu 23,57 33,36 Guira guira Protivin Museum / 961 morphobank.org 19,94 28,13 Opisthocomus hoazin MNHN paleo.esrf.eu 27,41 38,61 Falco cherrug Protivin Museum / 150 morphobank.org 29,37 51,59 Falco subbuteo Protivin Museum / 640 morphobank.org 22,08 37,93 Falco tinnunculus Protivin Museum / 278 morphobank.org 23,91 38,07 Crax mitu CCEC / 50001661 paleo.esrf.eu 36,73 70,00 Acryllium vulturinum Protivin Museum / 979 morphobank.org 28,22 36,95 Numida meleagris Protivin Museum / 813 morphobank.org 27,06 35,68 Callipepla squamata Protivin Museum / 1151 morphobank.org 16,05 23,69 Crossoptilon auritum Protivin Museum / 659 morphobank.org 32,67 42,46 Gallus gallus ESRF collection paleo.esrf.eu 28,58 33,56 Lagopus mutus CCEC / 50001538 paleo.esrf.eu 24,40 32,87 Pavo cristatus Protivin Museum / 755 morphobank.org 32,15 41,50 Perdix perdix Protivin Museum / 639 morphobank.org 20,59 27,05 Phasianus colchicus ESRF collection paleo.esrf.eu 27,71 36,06 Rollulus rouloul Protivin Museum / 176 morphobank.org 19,93 26,62 Tetrao tetryx Protivin Museum / 935 morphobank.org 26,31 34,49 Tetrao urogallus Protivin Museum / 143 morphobank.org 30,06 35,96 Balearica regulorum Protivin Museum / 520 morphobank.org 41,37 52,74 Grus grus CCEC / 50001675 paleo.esrf.eu 46,81 60,74

Grus canadensis Digimorph www.digimorph.org 38,28 56,06 Coloeus monedula Protivin Museum / 432 morphobank.org 24,30 37,92 Corvus albicollis Protivin Museum / 443 morphobank.org 34,09 53,94 Corvus corone Protivin Museum / 1124 morphobank.org 28,96 45,69 Corvus corax Protivin Museum / 766 morphobank.org 35,25 55,77 Pica pica Protivin Museum / 938 morphobank.org 24,98 40,15 Emberiza citrinella Protivin Museum / 1057 morphobank.org 13,81 20,16 Erythrura trichroa LFAC paleo.esrf.eu 11,21 17,55 Lonchura punctulata Protivin Museum / 484 morphobank.org 11,35 17,87 Taeniopygia guttata Protivin Museum / 869 morphobank.org 10,66 16,52 Fringilla coelebs Protivin Museum / 928 morphobank.org 13,21 20,00 Loxia curvirostra Protivin Museum / 767 morphobank.org 18,94 27,36

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Garrulax chinensis Protivin Museum / 808 morphobank.org 20,31 28,38 Liocichla omeiensis Protivin Museum / 920 morphobank.org 11,28 17,89 Ficedula albicollis ESRF collection paleo.esrf.eu 10,70 18,36 Phoenicurus phoenicurus Protivin Museum / 707 morphobank.org 12,60 18,54 Panurus biarmicus Protivin Museum / 784 morphobank.org 12,15 17,71 Cyanistes caeruleus ESRF collection paleo.esrf.eu 11,78 20,98 Parus major Protivin Museum / 1138 morphobank.org 12,54 21,63 Passer domesticus ESRF collection paleo.esrf.eu 7,78 11,00 Passer domesticus ESRF collection paleo.esrf.eu 12,61 18,90 Passer domesticus ESRF collection paleo.esrf.eu 10,95 16,28 Gracula religiosa Protivin Museum / 494 morphobank.org 26,10 35,31 Leucopsar rothschildii Protivin Museum / 641 morphobank.org 19,70 29,33 Scissirostrum dubium Protivin Museum / 523 morphobank.org 16,12 24,84 Sturnus vulgaris Protivin Museum / 102 morphobank.org 19,47 28,71 Turdus philomelos Protivin Museum / 956 morphobank.org 17,76 25,91 Zoothera citrina Protivin Museum / 983 morphobank.org 17,05 25,25 Ardea cinerea CCEC / 50001645 paleo.esrf.eu 33,30 50,27 Bubulcus ibis LFAC paleo.esrf.eu 24,86 32,18 Nycticorax nycticorax Protivin Museum / 911 morphobank.org 34,76 37,58 Pelecanus crispus Protivin Museum / 689 morphobank.org 43,42 57,17 Geronticus eremita Protivin Museum / 476 morphobank.org 32,08 49,76 Platalea alba Protivin Museum / 491 morphobank.org 34,52 54,10 Plegadis falcinellus Protivin Museum / 896 morphobank.org 27,84 40,45 Threskiornis aethiopicus LFAC paleo.esrf.eu 33,20 50,86 Threskiornis aethiopicus Protivin Museum / 160 morphobank.org 35,88 52,72 Phoeniconaias minor Protivin Museum / 959 morphobank.org 35,77 45,30 Phoenicopterus roseus Protivin Museum / 871 morphobank.org 38,65 49,98 Megalaima sp. CCEC / 50001574 paleo.esrf.eu 14,19 21,47 Dryocopus martius Protivin Museum / 736 morphobank.org 28,35 47,80 Picus viridis Protivin Museum / 759 morphobank.org 24,50 38,99 Pteroglossus aracari Protivin Museum / 980 morphobank.org 24,57 34,08 Pteroglossus viridis Protivin Museum / 584 morphobank.org 20,28 25,91 Rhamphastos vitellinus Protivin Museum / 583 morphobank.org 27,32 38,15

Podilymbus cristatus Digimorph www.digimorph.org 19,57 22,99 Tachybaptus ruficollis Protivin Museum / 1013 Morphobank 19,63 22,79 Thalassarche melenophris Protivin Museum / 822 Morphobank 43,19 61,94 Fulmarus glacialis ESRF collection paleo.esrf.eu 29,82 42,97 Caccatua moluccensis Protivin Museum / 378 morphobank.org 44,86 60,33 Eolophus rosecapillus Protivin Museum / 505 morphobank.org 30,23 45,21 Agapornis personatus Protivin Museum / 974 morphobank.org 19,99 31,25 Alisterus scapularis Protivin Museum / 271 morphobank.org 27,95 41,55 Amazona farinosa Protivin Museum / 456 morphobank.org 37,02 52,97 Amazona leucocephala Protivin Museum / 493 morphobank.org 29,40 39,70 Ara ararauna Protivin Museum / 1074 morphobank.org 49,25 67,84 Ara chloropterus Protivin Museum / 237 morphobank.org 48,07 66,83 Ara militaris Protivin Museum / 604 morphobank.org 48,02 69,49 Deroptyus accipitrinus Protivin Museum / 430 morphobank.org 33,31 52,75 Loriculus galgulus Protivin Museum / 676 morphobank.org 18,42 28,27 Melopsittacus undulatus Protivin Museum / 619 morphobank.org 16,60 27,10 Orthopsittaca manilata Protivin Museum / 773 morphobank.org 35,07 51,23 Psittacula eupatria Protivin Museum / 274 morphobank.org 33,50 46,89 Psittacula krameri Protivin Museum / 742 morphobank.org 24,74 38,12 Psittaculirostris desmarestii Protivin Museum / 1121 morphobank.org 25,61 36,53 Strigops habroptilus MHN Grenoble / MHN.Gr.Os. paleo.esrf.eu 42,09 57,10 Eudyptula minor Protivin Museum / 915 morphobank.org 30,96 39,51

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Eudyptula minor Peaugres paleo.esrf.eu 37,43 49,01 Spheniscus demersus Peaugres paleo.esrf.eu 42,18 52,86 Spheniscus humboldti Protivin Museum / 243 morphobank.org 45,40 56,71 Asio otus Protivin Museum / 446 morphobank.org 25,38 44,59 Bubo africanus Protivin Museum / 623 morphobank.org 29,48 51,52 Bubo bubo Protivin Museum / 867 morphobank.org 38,30 62,54 Bubo scandiacus Protivin Museum / 379 morphobank.org 34,84 58,09 Bubo scandiacus Peaugres paleo.esrf.eu 35,92 61,32 Otus scops Protivin Museum / 868 morphobank.org 17,74 29,75 Strix nebulosa Protivin Museum / 0 morphobank.org 31,95 68,61 Tyto alba Protivin Museum / 89 morphobank.org 24,53 46,28 Phalacrocorax capensis Protivin Museum / 764 morphobank.org 34,32 41,14 Phalacrocorax carbo ESRF collection paleo.esrf.eu 47,95 55,96

Phalacrocorax penicillatus Digimorph www.digimorph.org 43,84 51,73 Sula bassanus ESRF collection paleo.esrf.eu 46,76 60,19

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Log Type I PC Semilandmark Genus Species D C/D Scores PC Scores C/D color scale 1,00 Spathorhynchus fossorium 1,23 1,05 1,05 Diplometodon zarudnyi 0,69 1,09 1,10 Physignathus cocincinus 1,13 1,10 1,15 Anguis fragilis 0,87 1,00 1,20 Ophisaurus apodus 1,26 1,02 1,25 Chamaeleo calyptratus 1,24 1,02 1,30 Platysaurus imperatus 1,08 1,04 1,35 Coleonyx variegatus 0,81 1,03 1,40 Gecko sp. 0,69 1,02 1,45 Gecko sp. 1,30 1,05 1,50 Zonosaurus ornatus 1,01 1,04 1,55 Heloderma horridum 1,56 1,02 1,60 Heloderma suspectum 1,36 1,07 1,65 Anolis carolinensis 0,88 1,07 1,70 Crotaphytus collaris 1,09 1,10 1,75 Ctenosaura pectinata 1,34 1,01 1,80 Dipsosaurus dorsalis 1,02 1,07 1,85 Gambelia wislizenii 0,96 1,07 1,90 Iguania sp. 1,38 1,06 1,95 Sauromalus ater 1,20 1,09 2,00 Uta stansburiana 0,75 1,07 2,05 Podarcis muralis 0,88 1,06 2,10 Podarcis muralis 0,81 1,03 2,15 Podarcis muralis 0,93 1,03 2,20 Podarcis muralis 0,87 1,07 2,25 Podarcis muralis 0,69 1,04 2,30 Podarcis muralis 0,80 1,03 Podarcis muralis 0,70 1,05 Podarcis muralis 0,63 1,02 Podarcis muralis 0,74 1,06 Lanthanotus borneensis 1,04 1,01 Lanthanotus borneensis 1,08 1,02 Eumeces fasciatus 0,75 1,02 Shinisaurus crocodilurus 1,15 1,16 Tupinambis teguixin 1,43 1,02 Uranoscodon superciliosus 1,09 1,03 Varanus exanthematicus 1,34 1,05 Varanus exanthematicus 1,60 1,04 Lepidophyma flavimaculatum 1,07 1,03 Plotosaurus bennisoni 2,21 1,06 Sphenodon punctatus 1,33 1,07 Anomochilus leonardi 0,72 1,04 Boa constrictor 1,40 1,03 Calabaria reinhardtii 1,12 1,05 Eryx colibrinus 0,95 1,02 Casarea dussumieri 0,92 1,01 Lampropeltis getula 1,25 1,06 Thamnophis marcianus 1,08 1,02 Cylindrophus ruffus 1,00 1,00 Cobra sp. 1,19 1,02 Micrurus fulvius 1,07 1,01 Naja naja 1,23 1,03 Leptotyphlops dulcis 0,55 1,05 Loxocemus bicolor 1,12 1,01 Aspidites melanocephalus 1,38 1,04 Python molurus 1,48 1,00

176

Python sp. 1,62 1,00 Tropidophis haetianus 0,90 1,01 Lachesis muta 1,38 1,05 Vipera sp. 0,94 1,01 Uropeltis woodmasoni 0,61 1,02 Xenopeltis unicolor 1,18 1,05

Ebrachosuchus neukami 1,71 1,01 -0,26186 -0,20661 Parasuchus angustifrons 1,75 1,03 -0,24418 -0,21868 Desmatosuchus spurensis 1,97 1,07 -0,17679 -0,12344 Riojasuchus tenuiceps 1,96 1,07 -0,16217 -0,09274

Rhabdognathus sp. 1,88 1,02 -0,24023 -0,20256 Alligator mississipiensis 2,27 1,05 -0,22298 -0,17267 Alligator mississipiensis 1,86 1,02 -0,2662 -0,21086 Alligator mississipiensis 1,92 1,01 -0,22419 -0,20648 Alligator mississipiensis 1,64 1,05 Alligator mississipiensis 1,83 1,08 -0,19286 -0,15493 Caiman crocodylus 1,65 1,04 -0,17273 -0,15474 Caiman crocodylus 1,68 1,05 -0,15586 -0,13043 Caiman crocodylus 1,63 1,05 -0,16086 -0,13875 Caiman crocodylus 1,63 1,05 -0,16711 -0,15742 Caiman crocodylus 1,76 1,01 -0,19337 -0,17267 Caiman crocodylus 1,72 1,05 -0,16278 -0,13501 Caiman crocodylus 1,78 1,06 -0,1514 -0,12733 Caiman crocodylus 1,74 1,02 -0,20741 -0,1957 Crocodylus acutus 1,69 1,06 -0,14572 -0,1072 Crocodylus cataphractus 1,79 1,04 -0,18467 -0,15644 Crocodylus cataphractus 1,75 1,02 -0,19631 -0,16179 Crocodylus johnstoni 1,74 1,04 -0,18817 -0,15917 Crocodylus moreletti 1,88 1,03 -0,20148 -0,16061 Crocodylus niloticus 1,66 1,02 -0,20864 -0,22121 Crocodylus niloticus 1,31 1,10 -0,09089 -0,08181 Crocodylus niloticus 1,72 1,01 -0,20805 -0,20511 Crocodylus niloticus 1,57 1,06 -0,16405 -0,1593 Crocodylus niloticus 1,89 1,03 -0,18098 Crocodylus niloticus 1,34 1,10 -0,13918 -0,08787 Crocodylus niloticus 1,32 1,10 -0,11828 -0,09621 Crocodylus niloticus 1,35 1,09 -0,09165 -0,0887 Crocodylus niloticus 1,30 1,10 -0,12429 -0,10007 Crocodylus niloticus 1,37 1,06 -0,14155 -0,12108 Crocodylus niloticus 1,31 1,10 -0,13619 -0,1059 Crocodylus niloticus 1,33 1,09 -0,12797 -0,1111 Crocodylus niloticus 1,33 1,08 -0,13689 -0,11682 Crocodylus niloticus 1,37 1,08 -0,11238 -0,10386 Crocodylus niloticus 1,34 1,07 -0,13182 -0,11446 Crocodylus niloticus 1,29 1,10 -0,09104 -0,07532 Crocodylus niloticus 1,33 1,09 -0,10843 -0,09508 Crocodylus niloticus 1,34 1,08 -0,11226 -0,10925 Crocodylus niloticus 1,91 1,03 -0,228 -0,19939 Crocodylus niloticus 1,87 1,02 -0,23323 -0,22295 Crocodylus niloticus 1,92 1,01 -0,23045 -0,21394 Crocodylus niloticus 1,88 1,03 -0,20619 -0,1674

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Crocodylus niloticus 1,76 1,01 -0,21586 -0,20271 Crocodylus niloticus 1,81 1,01 -0,18604 -0,18219 Crocodylus niloticus 1,62 1,04 -0,15737 -0,14643 Crocodylus niloticus 1,76 1,01 -0,1992 -0,18081 Crocodylus niloticus 1,92 1,01 -0,27155 -0,23396 Crocodylus niloticus 1,88 1,03 -0,18853 -0,20722 Crocodylus niloticus 1,83 1,01 -0,20583 -0,19703 Crocodylus niloticus 2,00 1,04 -0,17782 -0,16178 Crocodylus niloticus 2,06 1,01 -0,23728 -0,21026 Crocodylus niloticus 1,93 1,02 -0,18236 -0,18093 Crocodylus niloticus 2,06 1,01 -0,20488 -0,18603 Crocodylus niloticus 1,91 1,01 -0,21956 -0,1979 Crocodylus niloticus 1,91 1,02 -0,19889 -0,18566 Crocodylus niloticus 1,69 1,05 -0,16385 -0,15025 Crocodylus niloticus 1,66 1,04 -0,13948 -0,13905 Crocodylus niloticus 1,65 1,07 -0,1112 -0,14994 Crocodylus niloticus 1,71 1,04 -0,1586 -0,14386 Crocodylus niloticus 1,97 1,01 -0,23819 -0,21595 Crocodylus niloticus 2,07 1,03 -0,20341 -0,17305 Crocodylus niloticus 1,95 1,02 -0,24251 -0,19082 Crocodylus niloticus 1,92 1,02 -0,21236 -0,198 Crocodylus niloticus 1,97 1,01 -0,28141 -0,23011 Crocodylus novaeguinae 1,74 1,02 -0,15003 -0,15467 Crocodylus porosus 1,93 1,04 -0,19933 -0,1775 Crocodylus porosus 1,80 1,02 -0,23312 -0,23182 Crocodylus porosus 1,96 1,03 -0,21876 -0,17764 Crocodylus sp. 1,90 1,01 -0,21554 -0,1972 Crocodylus sp. 1,90 1,04 -0,20228 -0,18489 Crocodylus sp. 1,90 1,03 -0,22018 -0,19336 Crocodylus sp. 1,93 1,01 -0,24254 -0,22029 Crocodylus sp. 1,96 1,04 -0,19161 -0,17484 Crocodylus sp. 1,91 1,02 -0,21994 -0,19639 Crocodylus sp. 1,89 1,01 -0,2291 -0,21525 Crocodylus sp. 2,01 1,02 -0,20293 -0,18233 Crocodylus sp. 2,00 1,02 -0,21108 -0,19925 Crocodylus sp. 1,97 1,02 -0,19683 -0,18361 Crocodylus sp. 1,99 1,05 -0,20267 -0,14745 Leidyosuchus canadensis 1,81 1,01 -0,21981 -0,20775 Melanosuchus niger 1,83 1,04 -0,1406 -0,13942 Osteolaemus tetraspis 1,62 1,06 -0,16677 -0,12426 Paleosuchus palpebrosus 1,58 1,10 -0,11865 -0,08336 Paleosuchus trigonatus 1,40 1,07 Tomistoma schlegelii 1,80 1,03 Pelagosaurus typus 1,64 1,01 -0,24429 -0,18637 Hamadasuchus rebouli 1,80 1,04 -0,21634 -0,13687 Sebecus icaeorhinus 1,92 1,08 -0,15999 -0,11346

Araripesaurus santanae 1,72 1,33 -0,03093 0,010656 Tropeognathus mesembrinus 1,49 1,34 0,017327 0,045572 Alkaruen koi 1,37 1,19 -0,14077 -0,06687 Parapsicephalus purdoni 1,42 1,13 -0,07116 Rhamphorhynchus muensteri 1,27 1,25 -0,04097 -0,04822

178

Anchiceratops ornatus 2,08 1,11 -0,31023 -0,22864 Pachyrhinosaurus lakustai 1,98 1,04 -0,24494 -0,19287 Protoceratops grangeri 1,90 1,10 -0,10017 -0,09702 Psittacosaurus lujiatnensis 1,59 1,07 -0,21727 -0,18265 Amurosaurus riabini 2,15 1,06 -0,21383 -0,13356 Corythosaurus sp. 1,95 1,30 -0,07214 -0,00321 Corythosaurus sp. 2,10 1,15 -0,20157 -0,07636 Edmontosaurus sp. 2,32 1,19 -0,13505 -0,02925 Hypacrosaurus altispinus 2,17 1,10 -0,21706 -0,13464 Kritosaurus notabilis 2,25 1,12 -0,20654 -0,11096 Lambeosaurus sp. 2,02 1,17 -0,1499 -0,05827 Parasaurolophus sp. 1,57 1,22 -0,10167 -0,07861 Tenontosaurus tilleti 1,94 1,14 -0,08167 0,011197 Heterodontosaurus tucki 1,61 1,08 -0,07443 -0,10883 Arenysaurus ardevoli 2,06 1,19 -0,12931 -0,08169 Dysalotosaurus lettowvorbecki 1,53 1,09 -0,16823 -0,11007 Dysalotosaurus lettowvorbecki 1,64 1,13 -0,18625 -0,10726 Iguanodon bernissartensis 2,06 1,13 -0,20276 -0,11179 Pachycephalosaurus grangeri 2,04 1,09 -0,2006 -0,12506 Stegoceras validus 1,63 1,22 0,019323 Euoplocephalus tutus 1,99 1,09 -0,19643 -0,1338 Kunbarrasaurus ieversi 1,85 1,06 -0,17344 -0,14736 Pawpawsaurus campbelli 1,88 1,11 -0,09534 -0,09414 Stegosaurus armatus 2,11 1,07 -0,14955 -0,12019 Stegosaurus stenops 2,03 1,09 -0,08339 -0,08852

Camarasaurus lentus 1,65 1,18 -0,19477 -0,07398 Shunosaurus lii 2,02 1,04 -0,22858 -0,23567 Amargasaurus cazani 1,99 1,16 -0,14035 -0,13176 Diplodocus longus 1,75 1,17 -0,19078 -0,10645 Nigersaurus taquetii 1,87 1,16 -0,05388 -0,03157 Bonatitan reigni 1,80 1,09 -0,17157 -0,09521 Ampelosaurus sp. 1,87 1,07 -0,15829 -0,12382 Spinophorosaurus nigerensis 2,02 1,08 -0,28489 -0,14525 Arcovenator escotae 2,08 1,09 -0,11165 -0,10114 Aucasaurus garridoi 2,14 1,09 -0,17653 -0,08911 Majungasaurus crenatissimus 2,04 1,10 -0,21629 -0,10565 Allosaurus fragilis 2,07 1,12 -0,1748 -0,10044 Acrocanthosaurus atokensis 2,02 1,18 -0,16534 -0,05706 Carcharodontosaurus saharicus 2,21 1,12 -0,19477 -0,11209 Giganotosaurus carolinii 2,15 1,10 -0,2084 -0,12654 Ceratosaurus magnicornis 1,91 1,15 -0,15637 -0,08342 Sinosaurus triassicus 1,99 1,20 -0,07381 -0,03189 Sinraptor dongi 2,12 1,06 -0,21048 -0,15154 Alioramus altai 2,03 1,10 -0,21082 -0,13546 Gorgosaurus libratus 2,12 1,08 -0,23786 -0,12612 Nanotyrannus lancensis 2,15 1,20 -0,11586 -0,06128 Tarbosaurus bataar 2,24 1,07 -0,22595 -0,15512 Tyrannosaurus rex 2,25 1,13 -0,20579 -0,11013 Tyrannosaurus rex 2,30 1,11 -0,19387 -0,11594 Tyrannosaurus rex 2,30 1,14 -0,21711 -0,10761 Erlikosaurus andrewsii 1,89 1,09 -0,16322 -0,12509 Compsognathus longipes 1,40 1,06 0,02306 -0,15433

179

Garudimimus brevipes 1,79 1,33 -0,11071 -0,06103 Ornithomimus edmontonicus 1,91 1,25 -0,04267 6,98E-06 Struthiomimus altus 1,96 1,34 -0,01861 0,012015 Citipati osmolskae 1,83 1,25 -0,16551 -0,04056 Conchoraptor gracilis 1,83 1,39 0,007958 0,043147 Incisivosaurus gauthieri 1,61 1,35 -0,01042 0,057218 Khaan mckennai 1,79 1,15 -0,14871 -0,10166 Bambiraptor feinbergi 1,66 1,15 -0,05259 -0,02097 Deinonychus anthirropus 1,76 1,14 -0,11152 -0,07264 Zanabazar junior 1,87 1,34 -0,02409 0,018357 Halszkaraptor escuillei 1,37 1,18 0,007643 -0,00272 Archaeopteryx lithographica 1,35 1,16 -0,02183 -0,04737 Archaeopteryx lithographica 1,39 1,21 Archaeopteryx lithographica 1,35 1,18

Cerebavis cenomanica 1,18 1,54 0,086043 0,1302

Aepyornis maximus 1,83 1,25 -0,01633 -0,00325 Apteryx owenii 1,48 1,62 0,28474 0,18722 Apteryx mantelli 1,54 1,67 0,19833 0,072036 Casuarius casuarius 1,77 1,27 0,023983 0,015965 Dromaius novaehollandiae 1,75 1,33 0,08015 0,1085 Dromaius novaehollandiae 1,68 1,29 0,02803 0,03316 Dinornis giganteus 1,85 1,32 0,06082 0,060429 Dinornis sp. 1,72 1,11 -0,02146 -0,08056 Dinornis sp. 1,71 1,12 Anomalopteryx didiformis 1,69 1,24 -0,05246 -0,0051 Emeus crassus 1,67 1,12 -0,09141 -0,08394 Emeus curtus 1,61 1,24 -0,04016 -0,0312 Emeus gravis 1,73 1,14 -0,04018 -0,03519 Emeus gravis 1,70 1,17 -0,0548 -0,08629 Pachyornis australis 1,78 1,10 -0,1331 -0,12321 Pachyornis elephantopus 1,74 1,14 -0,08097 -0,09304 Lithornis plebius 1,39 1,20 -0,03475 -0,02107 Rhea americana 1,36 1,31 0,15854 0,069573 Rhea americana 1,47 1,48 0,034393 0,11449 Rhea americana 1,44 1,42 Struthio camelus 1,79 1,55 Struthio camelus 1,76 1,66 Struthio camelus 1,77 1,56 Struthio camelus 1,78 1,47 Struthio camelus 1,68 1,71 Nothoprocta ornata 1,32 1,38 0,044842 0,086621 Nothura boraquira 1,30 1,34 0,073155 0,09314 Nothura darwinii 1,25 1,38 0,09675 0,11416 Rhynchotus rufescens 1,39 1,33 0,048217 0,073542 Tinamous major 1,36 1,33 0,035918 0,062874

Accipiter gentilis 1,50 1,60 0,14924 0,15888 Accipiter nisus 1,33 1,64 0,14574 0,16854 Buteo buteo 1,50 1,62 0,16794 0,1649 Buteo lagopus 1,51 1,64 0,17115 0,15912 Circaetus gallicus 1,57 1,52 0,12008 0,13305

180

Haliaeetus leucocephalus 1,62 1,52 0,14078 0,12691 Milvus aegypticus 1,45 1,62 0,16832 0,16057 Neophron percnopterus 1,54 1,55 0,12816 0,14952 Pernis apivorius 1,51 1,52 0,16592 0,13787 Stephanoaetus coronatus 1,52 1,53 0,12452 0,1318 Gyps fulvus 1,50 1,62 0,16731 0,15861 Cathartes aura 1,56 1,45 0,13514 0,11121 Coragyps atratus 1,56 1,47 0,22164 0,099841 Sarcoramphus papa 1,76 1,36 0,12899 0,091035 Vultur gryphus 1,74 1,35 0,10517 0,097888 Sagittarius serpentarius 1,62 1,51 0,14024 0,12215 Anas clypeata 1,38 1,35 0,15426 0,094582 Anas crecca 1,34 1,41 0,15258 0,088312 Anas plathyrhynchos 1,41 1,29 Chenonetta jubata 1,42 1,29 0,1131 0,058769 Cygnus olor 1,61 1,17 0,063757 -0,04176 Nettapus auritus 1,35 1,28 0,12055 0,068178 Oxyura leucocephala 1,41 1,33 0,17935 0,077281 Tadorna tadorna 1,46 1,25 0,10714 0,036411 Callonetta leucophrys 1,38 1,31 0,16463 0,067616 Cereopsis novaehollandiae 1,51 1,29 0,10825 0,059571 Chauna chavaria 1,57 1,29 0,032068 0,028997 Anseranas semipalmata 1,53 1,22 0,10624 0,047222 Anser albifrons 1,50 1,30 0,12505 0,055292 Anser anser 1,57 1,27 0,10041 0,045371 Anser erythropus 1,49 1,32 0,11738 0,070165 Branta canadensis 1,57 1,25 0,13243 0,03058 Presbyornis sp. 1,17 1,23 Apus pallidus 1,08 1,68 0,23571 0,20299 Panyptila melanoleuca 1,08 1,84 0,23199 0,23987 Thalurania furcata 0,99 1,96 0,25756 0,29888 Aceros corrigatus 1,57 1,33 0,086077 0,044159 Aceros plicatus 1,57 1,43 0,12145 0,10168 Anthracoceros malayanius 1,52 1,41 0,074498 0,092297 Bycanistes bucinator 1,52 1,38 0,11971 0,09704 Bycanistes cylindricus 1,59 1,37 0,088153 0,079698 Bycanistes fistulator 1,57 1,32 0,086081 0,064221 Bycanistes subcylindricus 1,56 1,50 0,12065 0,1267 Buceros cassidix 1,58 1,35 0,065424 0,037924 Ceratogymna atrata 1,57 1,42 0,11559 0,098932 Ceratogymna elata 1,58 1,31 0,11015 0,05139 Rhyticeros undulatus 1,62 1,37 0,116 0,079934 Tockus deckeni 1,40 1,46 0,15495 0,1331 Tockus erythrorhynchus 1,40 1,40 0,15246 0,13037 Bucorvus abyssinicus 1,67 1,58 0,11926 0,10883 Bucorvus leadbeateri 1,68 1,51 0,14934 0,1368 Upupa epops 1,24 1,46 0,17781 0,13649 Cariama cristata 1,55 1,39 0,073917 0,060683 Alca torda 1,48 1,49 0,13117 0,12105 Alle alle 1,31 1,39 0,12849 0,12364 Fratercula arctica 1,38 1,46 0,098399 0,13285 Pinguinus impennis 1,59 1,38 0,10355 0,080354 Uria aalge 1,46 1,36 0,080269 0,059566 Haematopus ostralegus 1,38 1,65 0,18924 0,18308 Actophilornis africanus 1,27 1,26 0,066699 0,056804

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Chroicocephalus ridibundus 1,39 1,40 0,083155 0,075754 Larus argentatus 1,46 1,41 0,088998 0,067515 Larus marinus 1,49 1,43 0,11364 0,097379 Larus michaellis 1,50 1,36 0,085807 0,062076 Gallinago gallinago 1,25 1,57 0,2466 0,18943 Scolopax minor 1,26 1,78 0,14843 0,20823 Scolopax rusticola 1,34 1,63 0,15472 0,15644 Ciconia ciconia 1,58 1,49 0,088794 0,11634 Ephippiorhynchus senegalensis 1,64 1,41 0,077709 0,084906 Leptoptylos crumeniferus 1,67 1,44 0,1056 0,095197 Mycteria ibis 1,56 1,60 0,15399 0,15146 Columba oenas 1,30 1,46 0,089072 0,11557 Gallicolumba luzonica 1,26 1,39 0,1126 0,091276 Ocyphaps lophotes 1,27 1,48 0,17287 0,13486 Phaps chalcoptera 1,31 1,36 0,15722 0,089372 Streptopelia tranquebarica 1,28 1,44 0,17118 0,12109 Otidiphaps nobilis 1,33 1,48 0,14413 0,12924 Raphus cucullatus 1,63 1,20 -0,03826 -0,0232 Pezophaps solitaria 1,61 1,19 -0,03958 0,002572 Ceryle rudis 1,25 1,54 0,15606 0,13445 Merops apiaster 1,12 1,92 0,19769 0,22181 Merops viridis 1,10 2,02 0,20238 0,22751 Geococcyx californianus 1,37 1,42 0,10759 0,076482 Guira guira 1,30 1,41 0,12376 0,098217 Opisthocomus hoazin 1,44 1,41 0,094783 0,091753 Falco cherrug 1,47 1,76 0,18197 0,199 Falco subbuteo 1,34 1,72 0,19424 0,20154 Falco tinnunculus 1,38 1,59 0,17824 0,17257 Crax mitu 1,56 1,29 0,070947 0,040371 Acryllium vulturinum 1,45 1,31 0,063691 0,048951 Numida meleagris 1,43 1,32 0,060277 0,065597 Callipepla squamata 1,21 1,48 0,19716 0,14093 Crossoptilon auritum 1,51 1,30 0,04165 0,034955 Gallus gallus 1,46 1,17 -0,026 -0,05716 Lagopus mutus 1,39 1,35 0,063247 0,065661 Pavo cristatus 1,51 1,29 0,043648 0,041575 Perdix perdix 1,31 1,31 0,061145 0,064744 Phasianus colchicus 1,44 1,30 0,036344 0,047869 Rollulus rouloul 1,30 1,34 0,102 0,052713 Tetrao tetryx 1,42 1,31 0,033635 0,058974 Tetrao urogallus 1,48 1,20 -0,03017 -0,04234 Balearica regulorum 1,62 1,27 0,040927 0,029998 Grus grus 1,67 1,30 0,074737 0,022257 Grus canadensis 1,58 1,46 Coloeus monedula 1,39 1,56 0,18088 0,12908 Corvus albicollis 1,53 1,58 0,22164 0,16305 Corvus corone 1,46 1,58 0,19255 0,14404 Corvus corax 1,55 1,58 0,23785 0,17117 Pica pica 1,40 1,61 0,23907 0,19681 Emberiza citrinella 1,14 1,46 0,17477 0,13287 Erythrura trichroa 1,05 1,57 0,2302 0,17727 Lonchura punctulata 1,06 1,57 0,24335 0,17478 Taeniopygia guttata 1,03 1,55 0,21663 0,18935 Fringilla coelebs 1,12 1,51 0,19508 0,13811 Loxia curvirostra 1,28 1,44 0,20827 0,12783

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Garrulax chinensis 1,31 1,40 0,1787 0,11504 Liocichla omeiensis 1,05 1,59 0,2226 0,15987 Ficedula albicollis 1,03 1,72 0,19454 0,21001 Phoenicurus phoenicurus 1,10 1,47 0,16586 0,14024 Panurus biarmicus 1,08 1,46 0,19533 0,1414 Cyanistes caeruleus 1,07 1,78 Parus major 1,10 1,72 0,27628 0,2292 Passer domesticus 0,89 1,41 0,095109 0,114 Passer domesticus 1,10 1,50 0,2185 0,17511 Passer domesticus 1,04 1,49 0,26222 0,18212 Gracula religiosa 1,42 1,35 0,14727 0,094132 Leucopsar rothschildii 1,29 1,49 0,19632 0,12206 Scissirostrum dubium 1,21 1,54 0,21535 0,1759 Sturnus vulgaris 1,29 1,47 0,21783 0,13963 Turdus philomelos 1,25 1,46 0,14328 0,1244 Zoothera citrina 1,23 1,48 0,18238 0,1574 Ardea cinerea 1,52 1,51 0,012501 -0,01162 Bubulcus ibis 1,40 1,29 0,053669 0,046346 Nycticorax nycticorax 1,54 1,08 -0,08453 -0,10822 Pelecanus crispus 1,64 1,32 0,093488 0,055923 Geronticus eremita 1,51 1,55 0,20251 0,15634 Platalea alba 1,54 1,57 0,19933 0,16646 Plegadis falcinellus 1,44 1,45 0,21353 0,12873 Threskiornis aethiopicus 1,52 1,53 0,21766 0,13542 Threskiornis aethiopicus 1,55 1,47 Phoeniconaias minor 1,55 1,27 0,085112 0,047633 Phoenicopterus roseus 1,59 1,29 0,094695 0,047934 Megalaima sp. 1,15 1,51 0,16846 0,11293 Dryocopus martius 1,45 1,69 0,25796 0,21041 Picus viridis 1,39 1,59 0,23429 0,16763 Pteroglossus aracari 1,39 1,39 0,12847 0,086287 Pteroglossus viridis 1,31 1,28 0,082342 0,04679 Rhamphastos vitellinus 1,44 1,40 0,10636 0,063383 Podilymbus cristatus 1,29 1,17 Tachybaptus ruficollis 1,29 1,16 0,04201 -0,02446 Thalassarche melenophris 1,64 1,43 0,076906 0,094399 Fulmarus glacialis 1,47 1,44 0,088039 0,090676 Caccatua moluccensis 1,65 1,34 0,12374 0,1021 Eolophus rosecapillus 1,48 1,50 0,19641 0,14653 Agapornis personatus 1,30 1,56 0,24262 0,16647 Alisterus scapularis 1,45 1,49 0,21375 0,14236 Amazona farinosa 1,57 1,43 0,2117 0,12448 Amazona leucocephala 1,47 1,35 0,17287 0,11366 Ara ararauna 1,69 1,38 0,16844 0,091862 Ara chloropterus 1,68 1,39 0,16847 0,090275 Ara militaris 1,68 1,45 0,19517 0,11784 Deroptyus accipitrinus 1,52 1,58 0,24753 0,1704 Loriculus galgulus 1,27 1,53 0,28314 0,16615 Melopsittacus undulatus 1,22 1,63 0,28648 0,20084 Orthopsittaca manilata 1,54 1,46 0,22571 0,12596 Psittacula eupatria 1,53 1,40 0,20021 0,11216 Psittacula krameri 1,39 1,54 0,23224 0,12919 Psittaculirostris desmarestii 1,41 1,43 0,23307 0,12655 Strigops habroptilus 1,62 1,36 0,17725 0,11099 Eudyptula minor 1,49 1,28 0,040749 0,041107

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Eudyptula minor 1,57 1,31 0,076951 0,066679 Spheniscus demersus 1,63 1,25 0,098071 0,053117 Spheniscus humboldti 1,66 1,25 0,048023 0,022482 Asio otus 1,40 1,76 0,21869 0,22324 Bubo africanus 1,47 1,75 0,21244 0,19783 Bubo bubo 1,58 1,63 0,15166 0,15535 Bubo scandiacus 1,54 1,67 0,20405 0,18629 Bubo scandiacus 1,56 1,71 0,19504 0,1937 Otus scops 1,25 1,68 0,23595 0,20082 Strix nebulosa 1,50 2,15 0,25947 0,27409 Tyto alba 1,39 1,89 0,2274 0,22861 Phalacrocorax capensis 1,54 1,20 -0,04425 -0,02658 Phalacrocorax carbo 1,68 1,17 -0,04767 -0,04541 Phalacrocorax penicillatus 1,64 1,18 Sula bassanus 1,67 1,78 0,025429 0,032224 Developmental Class Order Family Genus Species Data Origin stage

Crocodilomorpha Neosuchia Eusuchia Alligator mississipiensis 5 Juvenile Crocodilomorpha Neosuchia Eusuchia Alligator mississipiensis 5 Juvenile Crocodilomorpha Neosuchia Eusuchia Alligator mississipiensis 5 Juvenile Crocodilomorpha Neosuchia Eusuchia Alligator mississipiensis 5 Juvenile

Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 18 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 20 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 22 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 22 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 23 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 24 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 25 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 28 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 29 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 33 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 39 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 41 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 45 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 45 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 47 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 48 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 49 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 50 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 51 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 55 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 55 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 56 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 57 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 58 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 60 days

184

Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 61 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 62 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 63 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 63 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 64 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 67 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 68 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 68 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 70 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 70 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 71 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 72 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 74 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 74 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 75 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 78 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 79 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 79 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 79 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 79 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 79 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 79 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 80 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 81 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 82 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 83 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 83 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 87 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 87 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 87 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 87 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 93 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 93 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 93 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 93 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Embryo 93 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Hatchling Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Hatchling 13 days Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF 1 year Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF 3 years Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Juvenile Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Juvenile Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Juvenile Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Juvenile Crocodilomorpha Neosuchia Eusuchia Crocodylus niloticus ESRF Juvenile

185

Dinosauria Ornithopoda Hadrosauridae Corythosaurus sp. 12 Juvenile Dinosauria Ornithopoda Hadrosauridae Corythosaurus sp. 12 Subadult

Dinosauria Ornithopoda Iguanodontidae Dysalotosaurus lettowvorbecki 17 Juvenile Dinosauria Ornithopoda Iguanodontidae Dysalotosaurus lettowvorbecki 17 Subadult

Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Embryo 5,5 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Embryo 6,5 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Embryo 12 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Embryo 13 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Embryo 14 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Embryo 15 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Embryo 16 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Embryo 17 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Embryo 18 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Embryo 19 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Juvenile 21 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Juvenile 45 days Neognathae Galliformes Phasianidae Gallus gallus ESRF collection Adult

Neognathae Galliformes Phasianidae Phasianus colchicus ESRF collection Embryo Neognathae Galliformes Phasianidae Phasianus colchicus ESRF collection Hatchling Neognathae Galliformes Phasianidae Phasianus colchicus ESRF collection Adult

Neognathae Passeriformes Muscicapidae Ficedula albicollis ESRF collection Embryo Neognathae Passeriformes Muscicapidae Ficedula albicollis ESRF collection Hatchling Neognathae Passeriformes Muscicapidae Ficedula albicollis ESRF collection Juvenile Neognathae Passeriformes Muscicapidae Ficedula albicollis ESRF collection Adult

Paleognathae Rheiformes Rheidae Rhea americana 49 Hatchling Paleognathae Rheiformes Rheidae Rhea americana 49 Juvenile Paleognathae Rheiformes Rheidae Rhea americana 49 Adult Protivin Paleognathae Rheiformes Rheidae Rhea americana Museum Adult

186

Paleognathae Rheiformes Rheidae Rhea americana Digimorph Adult

Paleognathae Struthioniformes Struthionidae Struthio camelus 52 Embryo 39 days Paleognathae Struthioniformes Struthionidae Struthio camelus 52 Embryo 40 days Paleognathae Struthioniformes Struthionidae Struthio camelus 52 Hatchling 14 days Juvenile 2 Paleognathae Struthioniformes Struthionidae Struthio camelus 52 months Juvenile 4 Paleognathae Struthioniformes Struthionidae Struthio camelus 52 months Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF collection Juvenile Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF collection Juvenile Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF collection Adult Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF collection Adult Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF collection Adult Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF collection Adult Paleognathae Struthioniformes Struthionidae Struthio camelus ESRF collection Adult Inventory Number / Log Repository Data Log Absolute Absolute Genus Species institution Availability D C D C/D Age Age C/D color scale 1,00 Alligator mississipiensis OUVC 10117 12,97 14,85 1,11 1,14 1,05 Alligator mississipiensis OUVC 46,1 36,41 41,12 1,56 1,13 1,10 Alligator mississipiensis OUVC 10391 50,62 52,34 1,70 1,03 1,15 Alligator mississipiensis OUVC 9761 173,79 181,38 2,24 1,04 1,20 1,25 Crocodylus niloticus ENS paleo.esrf.eu 5,61 11,95 0,75 2,13 18 1,255 0,194 1,30 Crocodylus niloticus ENS paleo.esrf.eu 7,43 14,23 0,87 1,91 20 1,301 0,215 1,35 Crocodylus niloticus ENS paleo.esrf.eu 9,34 16,35 0,97 1,75 22 1,342 0,237 1,40 Crocodylus niloticus ENS paleo.esrf.eu 9,00 17,00 0,95 1,89 22 1,342 0,237 1,45 Crocodylus niloticus ENS paleo.esrf.eu 8,27 16,34 0,92 1,98 23 1,362 0,247 1,50 Crocodylus niloticus ENS paleo.esrf.eu 9,48 16,23 0,98 1,71 24 1,38 0,258 1,55 Crocodylus niloticus ENS paleo.esrf.eu 8,71 14,18 0,94 1,63 25 1,398 0,269 1,60 Crocodylus niloticus ENS paleo.esrf.eu 10,84 17,33 1,03 1,60 28 1,447 0,301 1,65 Crocodylus niloticus ENS paleo.esrf.eu 9,96 13,86 1,00 1,39 29 1,462 0,312 1,70 Crocodylus niloticus LFAC paleo.esrf.eu 11,62 18,59 1,07 1,60 33 1,519 0,355 1,75 Crocodylus niloticus LFAC paleo.esrf.eu 13,81 21,94 1,14 1,59 39 1,591 0,419 1,80 Crocodylus niloticus LFAC paleo.esrf.eu 14,05 19,49 1,15 1,39 41 1,613 0,441 1,85 Crocodylus niloticus LFAC paleo.esrf.eu 15,10 22,67 1,18 1,50 45 1,653 0,484 1,90 Crocodylus niloticus LFAC paleo.esrf.eu 14,56 21,04 1,16 1,45 45 1,653 0,484 1,95 Crocodylus niloticus LFAC paleo.esrf.eu 15,63 21,11 1,19 1,35 47 1,672 0,505 2,00 Crocodylus niloticus LFAC paleo.esrf.eu 15,91 21,43 1,20 1,35 48 1,681 0,516 2,05 Crocodylus niloticus LFAC paleo.esrf.eu 17,14 23,26 1,23 1,36 49 1,69 0,527 2,10 Crocodylus niloticus LFAC paleo.esrf.eu 17,39 23,63 1,24 1,36 50 1,699 0,538 2,15 Crocodylus niloticus LFAC paleo.esrf.eu 17,51 23,97 1,24 1,37 51 1,708 0,548 2,20 Crocodylus niloticus LFAC paleo.esrf.eu 16,52 23,76 1,22 1,44 55 1,74 0,591 2,25 Crocodylus niloticus LFAC paleo.esrf.eu 20,70 25,85 1,32 1,25 55 1,74 0,591 2,30

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Crocodylus niloticus LFAC paleo.esrf.eu 17,31 23,45 1,24 1,35 56 1,748 0,602 Crocodylus niloticus LFAC paleo.esrf.eu 16,64 22,84 1,22 1,37 57 1,756 0,613 Crocodylus niloticus LFAC paleo.esrf.eu 16,76 22,34 1,22 1,33 58 1,763 0,624 Crocodylus niloticus LFAC paleo.esrf.eu 15,90 21,08 1,20 1,33 60 1,778 0,645 Crocodylus niloticus LFAC paleo.esrf.eu 17,78 23,46 1,25 1,32 61 1,785 0,656 Crocodylus niloticus LFAC paleo.esrf.eu 15,56 21,27 1,19 1,37 62 1,792 0,667 Crocodylus niloticus LFAC paleo.esrf.eu 16,68 22,07 1,22 1,32 63 1,799 0,677 Crocodylus niloticus LFAC paleo.esrf.eu 17,40 22,84 1,24 1,31 63 1,799 0,677 Crocodylus niloticus LFAC paleo.esrf.eu 17,21 20,16 1,24 1,17 64 1,806 0,688 Crocodylus niloticus LFAC paleo.esrf.eu 18,56 21,32 1,27 1,15 67 1,826 0,72 Crocodylus niloticus LFAC paleo.esrf.eu 20,59 22,51 1,31 1,09 68 1,833 0,731 Crocodylus niloticus LFAC paleo.esrf.eu 18,22 20,97 1,26 1,15 68 1,833 0,731 Crocodylus niloticus LFAC paleo.esrf.eu 20,19 22,90 1,31 1,13 70 1,845 0,753 Crocodylus niloticus LFAC paleo.esrf.eu 18,71 21,21 1,27 1,13 70 1,845 0,753 Crocodylus niloticus LFAC paleo.esrf.eu 18,54 20,73 1,27 1,12 71 1,851 0,763 Crocodylus niloticus LFAC paleo.esrf.eu 18,11 19,74 1,26 1,09 72 1,857 0,774 Crocodylus niloticus LFAC paleo.esrf.eu 16,66 19,72 1,22 1,18 74 1,869 0,796 Crocodylus niloticus LFAC paleo.esrf.eu 18,22 20,69 1,26 1,14 74 1,869 0,796 Crocodylus niloticus LFAC paleo.esrf.eu 18,97 20,77 1,28 1,10 75 1,875 0,806 Crocodylus niloticus LFAC paleo.esrf.eu 19,29 21,35 1,29 1,11 78 1,892 0,839 Crocodylus niloticus LFAC paleo.esrf.eu 18,29 20,88 1,26 1,14 79 1,898 0,849 Crocodylus niloticus LFAC paleo.esrf.eu 19,36 21,52 1,29 1,11 79 1,898 0,849 Crocodylus niloticus LFAC paleo.esrf.eu 19,79 22,48 1,30 1,14 79 1,898 0,849 Crocodylus niloticus LFAC paleo.esrf.eu 19,98 22,35 1,30 1,12 79 1,898 0,849 Crocodylus niloticus LFAC paleo.esrf.eu 19,52 22,39 1,29 1,15 79 1,898 0,849 Crocodylus niloticus LFAC paleo.esrf.eu 17,94 19,60 1,25 1,09 79 1,898 0,849 Crocodylus niloticus LFAC paleo.esrf.eu 19,51 21,72 1,29 1,11 80 1,903 0,86 Crocodylus niloticus LFAC paleo.esrf.eu 19,58 21,88 1,29 1,12 81 1,908 0,871 Crocodylus niloticus LFAC paleo.esrf.eu 17,84 20,02 1,25 1,12 82 1,914 0,882 Crocodylus niloticus LFAC paleo.esrf.eu 21,08 23,03 1,32 1,09 83 1,919 0,892 Crocodylus niloticus LFAC paleo.esrf.eu 19,93 21,95 1,30 1,10 83 1,919 0,892 Crocodylus niloticus LFAC paleo.esrf.eu 20,42 22,73 1,31 1,11 87 1,94 0,935 Crocodylus niloticus LFAC paleo.esrf.eu 19,70 21,67 1,29 1,10 87 1,94 0,935 Crocodylus niloticus LFAC paleo.esrf.eu 20,02 21,85 1,30 1,09 87 1,94 0,935 Crocodylus niloticus LFAC paleo.esrf.eu 19,52 21,61 1,29 1,11 87 1,94 0,935 Crocodylus niloticus LFAC paleo.esrf.eu 20,33 22,20 1,31 1,09 93 1,968 1 Crocodylus niloticus LFAC paleo.esrf.eu 20,41 22,85 1,31 1,12 93 1,968 1 Crocodylus niloticus LFAC paleo.esrf.eu 20,16 22,02 1,30 1,09 93 1,968 1 Crocodylus niloticus LFAC paleo.esrf.eu 21,04 23,44 1,32 1,11 93 1,968 1 Crocodylus niloticus LFAC paleo.esrf.eu 18,93 21,86 1,28 1,16 93 1,968 1 Crocodylus niloticus LFAC paleo.esrf.eu 22,17 24,16 1,35 1,09 94 1,973 1,025 Crocodylus niloticus LFAC paleo.esrf.eu 22,02 23,97 1,34 1,09 107 2,029 1,029 Crocodylus niloticus LFAC paleo.esrf.eu 23,56 25,08 1,37 1,06 459 2,662 1,123 Crocodylus niloticus LFAC paleo.esrf.eu 35,62 37,07 1,55 1,04 1189 3,075 1,318 Crocodylus niloticus ENS 01 paleo.esrf.eu 28,59 29,41 1,46 1,03

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Crocodylus niloticus ENS 02 paleo.esrf.eu 28,49 29,97 1,45 1,05 Crocodylus niloticus ENS 03 paleo.esrf.eu 18,33 20,22 1,26 1,10 Crocodylus niloticus ENS 04 paleo.esrf.eu 29,42 31,31 1,47 1,06 Crocodylus niloticus ENS 05 paleo.esrf.eu 28,33 30,37 1,45 1,07 Crocodylus niloticus LFAC paleo.esrf.eu 76,39 78,62 1,88 1,03 3744 3,573 2 Crocodylus niloticus LFAC paleo.esrf.eu 67,13 67,89 1,83 1,01 3744 3,573 2 Crocodylus niloticus LFAC paleo.esrf.eu 101,04 104,64 2,00 1,04 3744 3,573 2 Crocodylus niloticus LFAC paleo.esrf.eu 113,92 115,16 2,06 1,01 3744 3,573 2 Crocodylus niloticus LFAC paleo.esrf.eu 85,44 87,01 1,93 1,02 3744 3,573 2 Crocodylus niloticus LFAC paleo.esrf.eu 114,57 115,15 2,06 1,01 3744 3,573 2

Corythosaurus sp. ROM 759 89,80 116,87 1,95 1,30 Corythosaurus sp. CMN 34825 124,86 144,00 2,10 1,15

BSPG AS I Dysalotosaurus lettowvorbecki 834 33,70 36,70 1,53 1,09 Dysalotosaurus lettowvorbecki MB.R.137x 44,11 49,95 1,64 1,13

Gallus gallus paleo.esrf.eu 6,73 14,26 0,83 2,12 5,50 0,74 0,028 Gallus gallus paleo.esrf.eu 7,33 16,94 0,87 2,31 6,50 0,813 0,033 Gallus gallus paleo.esrf.eu 12,87 19,40 1,11 1,51 12,00 1,079 0,06 Gallus gallus paleo.esrf.eu 13,41 20,98 1,13 1,56 13,00 1,114 0,065 Gallus gallus paleo.esrf.eu 13,15 18,89 1,12 1,44 14,00 1,146 0,07 Gallus gallus paleo.esrf.eu 14,57 24,33 1,16 1,67 15,00 1,176 0,075 Gallus gallus paleo.esrf.eu 14,36 21,75 1,16 1,51 16,00 1,204 0,08 Gallus gallus paleo.esrf.eu 14,89 22,38 1,17 1,50 17,00 1,23 0,085 Gallus gallus paleo.esrf.eu 16,02 21,25 1,20 1,33 18,00 1,255 0,09 Gallus gallus paleo.esrf.eu 15,34 23,62 1,19 1,54 19,00 1,279 0,095 Gallus gallus paleo.esrf.eu 22,17 29,86 1,35 1,35 40,00 1,602 1,201 Gallus gallus paleo.esrf.eu 23,55 28,50 1,37 1,21 64,00 1,806 1,322 Gallus gallus paleo.esrf.eu 28,58 33,56 1,46 1,17 199,00 2,299 2

Phasianus colchicus paleo.esrf.eu 12,75 17,73 1,11 1,39 13,00 1,114 0,481 Phasianus colchicus paleo.esrf.eu 15,58 21,52 1,19 1,38 27,00 1,431 1 Phasianus colchicus paleo.esrf.eu 27,71 36,06 1,44 1,30 757,00 2,879 2

Ficedula albicollis paleo.esrf.eu 6,08 8,55 0,78 1,41 6,00 0,778 0,462 Ficedula albicollis paleo.esrf.eu 7,79 11,79 0,89 1,51 13,00 1,114 1 Ficedula albicollis paleo.esrf.eu 9,80 16,55 0,99 1,69 27,00 1,431 1,071 Ficedula albicollis paleo.esrf.eu 10,70 18,36 1,03 1,72 378,00 2,577 2

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Rhea americana 17,88 24,92 1,25 1,39 Rhea americana 21,46 27,86 1,33 1,30 Rhea americana 23,01 30,26 1,36 1,31

Rhea americana 29,76 44,14 1,47 1,48 Rhea americana 27,85 39,61 1,44 1,42

Struthio camelus paleo.esrf.eu 26,15 44,02 1,42 1,68 39,00 1,591 0,975

Struthio camelus paleo.esrf.eu 30,21 46,38 1,48 1,54 40,00 1,602 1 Struthio camelus paleo.esrf.eu 26,89 44,01 1,43 1,64 54,00 1,732 1,07 Struthio camelus paleo.esrf.eu 39,21 65,64 1,59 1,67 101,00 2,004 1,131 Struthio camelus paleo.esrf.eu 43,76 67,26 1,64 1,54 161,00 2,207 1,209 Struthio camelus paleo.esrf.eu 57,17 91,33 1,76 1,60 Struthio camelus paleo.esrf.eu 39,85 63,10 1,60 1,58 Struthio camelus paleo.esrf.eu 61,40 95,02 1,79 1,55 771,00 2,887 2 Struthio camelus paleo.esrf.eu 57,39 95,03 1,76 1,66 771,00 2,887 2 Struthio camelus paleo.esrf.eu 58,36 90,78 1,77 1,56 771,00 2,887 2 Struthio camelus paleo.esrf.eu 60,60 88,87 1,78 1,47 771,00 2,887 2 Struthio camelus paleo.esrf.eu 47,62 81,22 1,68 1,71 771,00 2,887 2

Abbreviations: CT: Characterised using conventional X-ray Computed Tomography; ESRF: Characterised using synchrotron radiation based computed tomography; ESRF collection: Curated at the European Synchrotron Radiation Facility; LFAC: La Ferme aux Crocodiles, Pierrelattes, France; TL: Thierry Loeb, Echirolles, France; ENS: Ecole Normale Supérieure, Lyon, France; MHN Grenoble: Curated at Museum d’Histoire Naturelle, Grenoble, France; MNHN: Curated at Museum National d’Histoire Naturelle, Paris, France; CCEC: Centre de Conservation et d’Etude des Collections, Lyon, France; Peaugres: Safari de Peaugres, Peaugres, France.

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Chapter VII Progenetic scenario within Archosauria

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Embryological development in Crocodylus niloticus involves the transition from a strongly coiled to an elongated brain shape (C/D from 2.13 to 1.04). Juveniles attain adult brain coiling ratios early on, yet braincase filling remains high during the first stages of post-hatchling development. Cranial filling rapidly decreases in juveniles because the braincase grows quicker than the brain itself (Jirák and Janáček 2017). Internal braincase surface structures remain undefined in non-maniraptoriform dinosaurs, which present a slightly more coiled endocast than crocodilians (Average C/D=1,12, range 1,04-1,30; equivalent to an 82-day-old crocodile embryo), even in small species such as the primitive ornithischian Heterodontosaurus. It accounts for the first progenetic stage (Table IV-10). This indicates that brain coiling and endocast filling remained independent of body size at this evolutionary level.

Compsognathus longipes, representing the closest outgroup to Maniraptoriformes, shows detectible intervals of the interhemispheric suture and the ridge between the olfactory tracts, indicating that elevated levels of endocast filling in small forms must be ancestral for

Maniraptoriformes. It has to be noticed nevertheless that it was probably a relatively young individual.

Adult Maniraptoriformes (Maniraptora and Ornithomimosauria) exhibit a more coiled endocast

(average C/D=1.22; equivalent to a 63-day-old crocodile embryo) and medium braincase infilling than other non-avian dinosaurs. This represents the second stage in the progressive progenetic evolutionary pathway (Table IV-10). Even though Halszkaraptorinae and their ancestors were clearly non-volant (Cau et al. 2017, Chapter 5), Halszkaraptor unites a body size within the range of flying birds with degrees of endocast coiling and inferred braincase filling shared with some modern birds. Poor cranial preservation prevents reliable detection of vascularization, yet the boundaries between brain structures, such as those between the optic tectum and the telencephalon, are clearly recognizable. This illustrates the comparatively high level of endocast filling by the brain already reported for Maniraptora (Osmólska 2004). In Maniraptoriformes, small taxa generally present a better-filled braincase than large-bodied relatives, as cerebral

197

structures are discernible in small-bodied species but mostly indistinguishable in larger members

of the group. Body size correlates with braincase infilling but not with coiling.

Archaeopteryx shows endocast coiling within the range of Maniraptoriformes (London specimen:

C/D=1.16; Munich specimen: C/D=1.17). Archaeopteryx exhibits clear cerebral segregation and

well-defined vascular surface expression on the cerebral hemisphere, which indicate snug cerebral

infilling of the endocranial cavity. Irrespective of volancy capacities, Archaeopteryx appears to

be similar to small Maniraptoriformes in particular to Halszkaraptor.

Notably, pterosaurian brain coiling corresponds to the same crocodilian developmental stage as

maniraptoriforms (CD range=1.13-1.34, average C/D=1.25; 62-day-old crocodile embryo).

Strong endocast coiling was already present during their early evolutionary history, as

exemplified by Rhamphorhynchus muensteri and Parasicephalus purdoni (C/D=1.24 and 1.14

respectively). All pterosaurs exhibit high braincase filling level independent from body size.

Finally, modern birds exhibit average coiling values correlating with an even earlier crocodilian

ontogenetic stage (42-day-old crocodilian embryo; average C/D=1.44), but span a much larger

brain shape range than all other groups (C/D ranges between 1.08 and 2.15). In birds, as in

pterosaurs, braincase filling is always highly independent from body size.

equivalent log (D) Strong filling of C/D standard Heterochronic C/D average crocodile average the brain cavity deviation stage embryonic age

Lepidosauria 1,08 1,04 no 0,03 adult 0 Crocodilomorphs 1,75 1,04 no 0,03 adult 0 non-maniraptoriforms dinosaurs 1,98 1,12 no 0,06 82 1 in small forms maniraptoriforms 1,68 1,24 only 0,09 63 2 Pterosaurs 1,46 1,25 yes 0,09 62 3 birds 1,45 1,44 yes 0,18 42 3

size coiling increase endocast diversification Development process decrease increase infilling in birds stages

Table IV-10. Overview of identified heterochronic stages with specified developments in

selected sauropsids and their representative associated crocodilian embryonic ages.

198

Relative to the primitive archosaurian pattern exhibited by adult crocodiles and lepidosaurs (stage

0), stage 1, represented by non-maniraptoriforms dinosaurs, involves a slightly more coiled endocast without detectable body size effects on braincase infilling. Stage 2 coincides with the origin of Maniraptoriformes and associates an overall reduction in body size with a more coiled endocast. Body size determines cranial filling, as the smallest members of the group, such as

Halszkaraptor and Archaeopteryx, exhibit high levels of braincase filling. Stage 3 is defined through a high level of brain coiling and a high degree of braincase filling that persists independent of body size, and is observed in true birds, including secondarily flightless paleognaths. The Cretaceous ornithurine Cerebavis cenomanica, interpreted as a capable flyer, already shows a coiling ratio of 1.54 and a well-filled braincase (Walsh et al. 2016). Stage 3 was also independently reached in pterosaurs, which associates stage 3 exclusively with archosaurs that achieved volancy (Table IV-10).

Considering the general progenetic trend associated with size reduction early in the evolutionary histories of birds and pterosaurs, we infer that a certain evolutionary threshold was negotiated in small-bodied ornithodirans that enabled the evolution of volancy, partially through exaptation of brain capacity. After sufficient cerebral performance to enable basic flight was unlocked, the evolutionary radiations of pterosaurs and birds both saw a complete decoupling of endocast filling and body size. Within Pterosauria, some of these progenetic developments appear to have occurred in more advanced pterosaurs and not necessarily during the earliest stages of pterosaurian evolution, as pontine flexure and cerebral enlargement are recorded in pterosaurs that already flew (Alonso et al. 2004).

The origins of increased brain coiling and braincase infilling in birds and their ancestors were not intrinsically associated with volancy but rather permitted enhanced cerebral processing for increasingly complex behaviour (Bottjer 1997, Burish et al. 2004). Nevertheless, these cerebral developments and the simultaneous body size reduction were subsequently exapted and

199 contributed to enabling archosaurian flight. Although recent results propose that even

Archaeopteryx may already have been capable of flight (Chatterjee and Templin 2003, Voeten et al. 2018), its brain was probably not yet capable of controlling the complex volancy seen in most modern birds.

200

Co-authors affilitation

Rinchen Barsbold: Palaeontological Center, Mongolian Academy of Sciences, Ulaanbaatar 201-351, Mongolia

Stanislav Bureš : Department of Zoology and Laboratory of Ornithology, Palacký University, 17. listopadu. 50, 77146 Olomouc, Czech Republic

Andrea Cau: Geological and Palaeontological Museum ‘Giovanni Capellini’, Via Zamboni, 63, I-40126 Bologna, Italy

Philip J. Currie: Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada.

Vincent Fernandez: European Synchrotron Radiation Facility, 71 Avenue des Martyrs, CS-40220, 38043 Grenoble

Pascal Godefroit : Directorate Earth & History of Life, Royal Belgian Institute of Natural Sciences, rue Jenner 13 B-1000 Brussels, Belgium.

Jiří Janáček : Department pf Biomathematics, Institute of Physiology, Czech Academy of Sciences, Vídeňská 1083, 142 20, Prague 4, Czech Republic

Daniel Jirak : MR Unit, Department of Diagnostic and Interventional Radiology, Institute for Clinical and Experimental Medicine, Vídeňská 1958/9,, 142 21, Prague 4, Czech Republic

Institute of Biophysics and Informatics, 1st Faculty of Medicine, Charles University, Salmovská 1, 120 00, Prague 2, Czech Republic

Oliver Rauhut :

201

Department for Earth and Environmental Sciences and geoBioCenter, SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, Ludwig-Maximilian-University Munich, Richard- Wagner-Straße 10, 80333, Munich, Germany

Koen Stein : Earth System Science – AMGC Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels, Belgium

Paul Tafforeau : European Synchrotron Radiation Facility, 71 Avenue des Martyrs, CS-40220, 38043 Grenoble

Khishigjav Tsogtbataar : Institute of Palaeontology and Geology, Mongolian Academy of Sciences, Ulaanbaatar 210-351, Mongolia

Dennis Voeten : Department of Zoology and Laboratory of Ornithology, Palacký University, 17. listopadu. 50, 77146 Olomouc, Czech Republic European Synchrotron Radiation Facility, 71 Avenue des Martyrs, CS-40220, 38043 Grenoble

202

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Acknowledgements

First of all, I want to acknowledge Paul Tafforeau and Prof. Stanislav Bureš for their supervision effort during this PhD. Due to their effort, I improved my knowledge of the scientific environment, had stimulating discussion which helped me in the realisation of this study and I had the luck to access some of the most interesting fossils ever. Prof. Bureš I would like to thank you more particularly for your warm welcoming in Olomouc and helping me for arranging every thing when I arrived (and sorry that it added you too much office work which I know you like a lot).

Paul, Thanks a lot for allowing me to play with the beamlines, helping me during the experiments even when I was calling late at night/early in the morning (during experiments I do not know how quickly time is running), funny jokes, candies scanning parties.

I would also like to thank Jiří Janáček and Daniel Jirák for the very useful discussion and stays in Prague, the scans of part of the bird dataset and their welcoming in Czech Republic. Jiří thank you more particularly for arranging everything in Prague, for allowing me to use your office every time I was coming to visit you. Daniel for showing me some experiments at the IKEM and for giving me to have my best teaching experience in Liberec.

I also need to thank the Laboratory of Ornithology of Palácký University in Olomouc and the European Synchrotron Radiation Facility, for allowing my access to the office and the scanning facility.

I want to thank my colleagues from ID19 for their support. Special mention to

Vincent Fernandez (funny discussion about dinosaurs and allowing me to play with his

Heterodontosaurus pet), Camille Berruyer (for the Shnappi party), Pierre-Jean Gouttenoire (yeah, we have the same bad jokes which made life funnier), Marie Ondarsuhu (and again I am admitting you were supporting me but I know you will do an horrible photoshop montage to try to prove it).

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Thank also to Elodie Boller, Alexander Rack, Margie Olbinado and all the people that are and were members of ID19, for their support at every step of this project.

I also want to thank Dennis Voeten, for long discussions on flight evolution around a beer(s) late at night and for helping me in writing (my writing skills in English are still suboptimal but I will try to not bother you too much with this in the future).

Thank you to my slave team, Adam, Eva and Yannick, who helped me for segmentation of specimens, it saved me a lot of time allowing me to move forward in some other things.

Thank you to my parents. I know it sounded crazy for a 4-year-old child to want to be a palaeontologist, but they believed in me and supported me all the way long. Buying this first dinosaur book was finally a good idea.

Thank you to Jérôme, you were not directly involved in this PhD, but if I am here today, it’s because of you, your advices, the people I met because of you, the fact that even in less optimistic you kicked me and forced me to move forward.

My friends out of work in Olomouc, Tristan, Plejada Music Team, Tereza, Douglas, Maylis,

Marine, Anna, Ilona, François, allowing me to decrease the pressure after long and hard working days around a beer (or a song).

Lilie, Zoé, and Molly, thank you, it would not have been possible without your support during all this time, during good and bad moments, my never giving up mood was due to you.

Archaeopteryx, Compsognathus and Halszkaraptor which had the good idea to die in appropriate environment and to be exquisitely preserved, which helped a lot for making observations on them. Thanks dudes!

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