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C. R. Palevol 5 (2006) 519–530 http://france.elsevier.com/direct/PALEVO/ The evolution of locomotion in

John R. Hutchinson

Structure and Laboratory, The Royal Veterinary College, University of London, Hatfield, AL9 7TA, UK

Received 5 April 2005; accepted after revision 6 September 2005 Available online 07 February 2006 Written on invitation of the Editorial Board

Abstract Archosaurian evolved a more erect posture and parasagittal early on. Early were the first habitual striding bipeds, a trait retained by living . Yet there is much more to locomotor evolution than these two transitions. I review our understanding of the pattern of locomotor evolution from the first archosaurs to Crocodylia and Neornithes, outlining where transitions of locomotor evolved. I evaluate current research approaches, advocating more experimental work on extant to establish rigorous form–function relationships, and more biomechanical research that is bolstered by validation and sensitivity analysis of its assumptions, methods, and results. To cite this article: J.R. Hutchinson, C. R. Palevol 5 (2006). © 2006 Académie des sciences. Published by Elsevier SAS. All rights reserved. Résumé L’évolution de la locomotion chez les archosaures. Les reptiles archosauriens ont évolué tôt vers une posture plus dressée et une démarche parasagittale. Les premiers dinosaures ont été les premiers bipèdes à marcher à grandes enjambées, caractéristique retenue par les oiseaux vivants. Cependant, il y a beaucoup plus lors de l’évolution locomotrice des archosaures que ces deux transitions. Je réexamine notre compréhension du modèle de l’évolution locomotrice à partir des premiers archosaures jusqu’aux Crocodiliens et Néornithes, en soulignant où les transitions de la fonction ont évolué. J’évalue les approches de la recherche en cours en me faisant l’avocat de davantage d’études expérimentales sur les animaux pour établir des relations rigoureuses fonction– forme et de davantage d’études biomécaniques pour étayer l’analyse et la validation des suppositions, méthodes et résultats. Pour citer cet article : J.R. Hutchinson, C. R. Palevol 5 (2006). © 2006 Académie des sciences. Published by Elsevier SAS. All rights reserved.

Keywords: Archosaur; ; ; ; ; Locomotion; Evolution

Mots clés : Archosaure ; Oiseau ; Crocodile ; Dinosaure ; Biomécanique ; Locomotion ; Évolution

1. Introduction 81]. In contrast, neornithine birds stand and move in more erect postures and stereotyped , albeit Extant crocodylians move in widely-varying ways, with variation between species [1,40,43]. Yet how this from very sprawling to somewhat erect postures [37, difference evolved is equivocal from a neontological standpoint, because of 250 Myr of extinctions between the and the present – there are no extant non- avian bipedal archosaurs available for study. Current E-mail address: [email protected] (J.R. Hutchinson). acceptance that birds evolved from theropod dinosaurs

1631-0683/$ - see front matter © 2006 Académie des sciences. Published by Elsevier SAS. All rights reserved. doi:10.1016/j.crpv.2005.09.002 520 J.R. Hutchinson / C. R. Palevol 5 (2006) 519–530

[48,70,97] has transformed this difficult question into a Pterosauria, ). This provides hope soluble one: birds now have dozens of fossil outgroup for reconstructing how living and birds came taxa among non-avian archosaurs for calibrating how to locomote so differently from each other and from avian locomotion evolved (Fig. 1). Hence data from more basal reptiles. The focus of this review is on fossils are vital for reconstructing the evolution of arch- how this reconstruction can be done and how the mod- osaur locomotion. The disparate of the fossil ern consensus on this topic became established. What relatives of crocodiles and birds support the inference have we learned in over a century of research on arch- that their locomotor repertoires often were qualitatively osaur locomotor evolution since Marey, Muybridge, somewhere between those of extant archosaurs, with and others helped initiate the scientific study of loco- marked specialization within side-branch (e.g., motion?

Fig. 1. ‘Consensus’ phylogenetic framework for Archosauria, modified from references listed in [55–57], showing major transformations of locomotor function in Archosauria. Numbers indicate the latest likely timing of locomotor shifts within indicated: 1, more erect posture; 2, less erect posture; 3, variable posture from sprawling to erect; 4, ; 5, Striding ; 6, body-size increase; 7, body-size decrease; 8, more upright pose; 9, more crouched pose; 10, shift to digitigrady/plantigrady; 11, primitive mesotarsal ; 12, crocodile-normal ankle; 13, advanced mesotarsal ankle; 14, more parasagittal gait; 15, large and fourth trochanter, predominant hip-based during stance; 16, metatarsus held low to ground; 17, near-vertical metatarsus; 18, reduced tail and fourth trochanter, increased -based propulsion during stance; 19, adductor-based postural support; 20, abductor-based postural support; 21, medial rotator-based postural support; 22, poor bipedal ability; 23, good bipedal running ability; 24, poor turning ability; 25; improved turning ability; 26, medially-offset femoral head; 27, open ; 28, bounding and galloping locomotor modes; 29, near-isometric scaling; 30, more proportions; 31, less cursorial limb proportions; 32, near-horizontal vertebral column; 33, semi-aquatic habits; 34, more terrestrial habits; 35, . Question marks indicate extremely ambiguous evidence for the timing of origin of certain traits. Not all taxa (e.g., , ornithosuchids) are included; some taxa may lie in slightly different positions than indicated but this would not affect the conclusions. Fig.1. Diagramme phylogénétique de « consensus » pour les archosauriens, modifié à partir des références listées [55–57], montrant les transformations majeures de la fonction locomotrice chez les archosauriens. Les nombres indiquent le moment vraisemblablement le plus récent des changements de locomotion dans le clade : 1, posture plus dressée ; 2, posture moins dressée ; 3, posture variable entre à terre et dressée ; 4, quadrupédie ; 5, bipédie à grands pas ; 6, augmentation de la taille du corps ; 7, diminution de la taille du corps ; 8, attitude plus verticale ; 9, attitude plus accroupie ; 10, changement vers le mode / ; 11, cheville mésotarsale primitive ; 12, cheville normale de crocodile ; 13, cheville mésotarsale avancée ; 14, démarche plus parasagittale ; 15, grande queue et quatrième trochanter, propulsion basée de façon prédominante sur la hanche pendant la posture ; 16, métatarse maintenu bas par rapport au sol ; 17, métatarse presque vertical ; 18, queue réduite et quatrième trochanter, propulsion basée sur le genou, augmentée pendant la posture ; 19, support postural basé sur l’adducteur ; 20, support postural basé sur l’abducteur ; 21, support postural basé sur le rotateur médian ; 22, faible aptitude à la course bipède ; 23, bonne aptitude à la course bipède ; 24, faible aptitude à tourner ; 25,aptitude à tourner améliorée ; 26 tête du fémur débutant médialement ; 27, acetabulum ouvert ; 28, modes locomoteurs par bond et galop ; 29, recouvrement à peu près isométrique d’écailles d’os ; 30, proportions des membres plus adaptées à la course ; 31, proportions des membres moins adaptées à la course ; 32, colonne vertébrale presque horizontale ; 33, habitudes semi-aquatiques ; 34, habitudes plus terrestres ; 35, vol ; les points d’interrogation indiquent une évidence extrêmement ambiguë sur le «timing» d’origine de certaines caractéristiques. Tous les (par exemple, Ptérosaures, Ornithosuchides) ne sont pas inclus ; certains taxons peuvent se trouver dans des positions légèrement différentes de celles qui sont indiquées, mais ceci n’affecte pas les conclusions. J.R. Hutchinson / C. R. Palevol 5 (2006) 519–530 521

First, I survey the methods and evidence used to re- sion of basal archosaurs such as ornithosuchids and construct archosaur locomotor function and evolution rauisuchians [27]. Huene’s [54] early functional work (focusing on functional morphology and scaling/biome- was not well received [86]. chanics approaches), outlining what I consider to be the Romer’s [85–87] studies are a classic and influential modern consensus. Second, I highlight the major unre- work on archosaur locomotor evolution that set the solved questions and evaluate the promise of, or chal- standard for over 50 years, revealing how pelvic mus- lenges for, particular methods that might resolve them. cles had fragmented and shifted dorsocaudally in Arch- I conclude by explaining a simple biomechanical ap- osauria, corresponding to a generally more erect posture proach for understanding what limb orientations different and parasagittal gait. However, his studies emphasized archosaurs may have used, as an example of how we can the limb myology of alligators and specialized dino- better understand archosaur locomotor mechanics and saurs (e.g., sauropods and coelurosaurs), as birds were evolution. My chief concern is detailing the ancestral not yet accepted as dinosaur descendants, and fewer mechanisms by which archosaurian clades positioned basal archosaurs were well known. Myological recon- and moved their hindlimbs, and tracing the evolution of structions and functional studies have nonetheless been these mechanisms along the crocodile and bird lines tightly linked ever since Romer’s work – osteological (sensu [41]). I summarize this information in Fig. 1. descriptions of archosaurs are replete with inferences Events within crocodylomorph or theropod side- about what soft tissues adhered to particular bony struc- branches, and within ornithischians or sauropodomorphs, tures, and these inferences are often used to support are exciting topics but are less crucial for resolving how higher-level inferences about function [101]. the terrestrial locomotor modes of extant crocodiles and A few important anatomical and functional analyses birds came to be the way they are today. The latter ques- such as Schaeffer [88] on ankle function and Colbert tion in my opinion is the most profound one in the evo- [27] on saurischian evolution followed Romer’s work, lution of in archosaurs. Arboreality but Charig’s [20] classic work on the transition between in any taxa, or the origins of flight in pterosaurs [72] and sprawling and erect postural grades had the broadest birds [21,31,70,73] are reviewed elsewhere. Some basal impact. Some of Charig’s ideas were heavily criticized archosaurs may have been semi-aquatic (it is well ac- – for example, he made many errors and oversimplifi- cepted that non-avian dinosaurs were habitually terres- cations in his inferences about muscle reconstructions, trial), and many lineages within Archosauria indepen- function, and mechanics. His ‘femur-knocking-on-the- dently returned to the , but this too cannot be pubis’ problem (i.e., that the femur would be overly covered here in detail. Following Gatesy [37,39], I try adducted by femoral protractors arising from the pubis to emphasize a continuum of limb positions, and use during hip flexion) over-emphasized the role of pubic ‘posture’ only to refer to more/less abducted poses (more muscles in femoral protraction [62,91,96]. Yet Charig’s sprawling to more erect), and ‘limb orientation’ or sim- basic conclusions remain generally accepted: (1) arch- ply ‘pose’ to refer to the degree of limb extension osauromorphs transitioned from more to less-sprawling (i.e., straightening; more crouched to more upright). (more erect) postures, reflected in osteological and myological features detailed by Charig and many others 2. Functional morphology (e.g., inturned femoral head and fenestrated acetabu- lum), (2) quadrupedalism was ancestral for Archosaur- As Archosauria came to be recognized as a major ia, not bipedalism as some previous authors had argued, group within Reptilia that gave rise to crocodiles, birds, and (3) digitigrady is correlated with an erect posture, and many extinct taxa, it was clear they had evolved although with exceptions [76,77]. novel ways of standing and moving, atypical of more Later studies elucidated that archosauromorphs ple- basal reptiles [13,20,27,29,30,74,76,77,85–87]. Initi- siomorphically had a ‘primitive mesotarsal’ ankle, ally, the main source of information about archosaur which was elaborated into functional complexes such locomotion was trackway evidence but this was not as the complex ‘crocodile-normal’ (on the crocodile well-integrated with the anatomical record, as the track- line), bizarre ‘crocodile-reversed’ (ornithosuchids), and makers typically were ambiguous [74,94]. Likewise, hingelike ‘advanced mesotarsal’ (on the bird line) an- much anatomical/functional information was not yet kles [29,30,43,89,90]. An excellent experimental study synthesized into a widely-accepted phylogenetic per- of crocodilian limb function [13] determined that cro- spective [43,70] – even dinosaurs were not accepted codiles differed from the ancestral condition in as monophyletic for many years, at least to the exclu- maintaining a cranially-oriented tarsus and metatarsus 522 J.R. Hutchinson / C. R. Palevol 5 (2006) 519–530

(i.e., a more parasagittal gait) during the first half of opods [19,70], rhinoceroses and ceratopsians [3,4,80],or stance phase, then rotated this unit laterally during plan- and large theropods [3,4] were deficient be- tarflexion later in stance. Dinosaurs presumably lost the cause in many cases form-function relationships were calcaneal tuber intrinsic to the ‘crocodile-normal’ ankle poorly demonstrated for extant animals ([14] is a good as they adopted a more erect posture and parasagittal exception), and anatomical/functional differences tended gait, reducing distal limb rotation. Parrish [76,77] com- to be de-emphasized in favour of similarities. One can plemented this work with a detailed analysis of inferred find many similarities between extinct theropods and ex- form-function relationships in archosaur and tant taxa (some homologous), but one can also find many overall limb structure. He inferred that the evolution differences – that is the problem. If extinct and extant of a more erect posture occurred at least twice in arch- archosaurs were not so different in some aspects, there osaurs: once on the crocodile line (most importantly, would be fewer problems in reconstructing their locomo- that crocodiles were secondarily less erect and more tor function and evolution, and the questions involved aquatic than their crocodylomorph forebears), and once might even be less exciting. on the bird line. Additionally he emphasized that there The integrative work of Gatesy [36,39] was a para- was much parallelism between archosaur lineages, digm shift for studies of archosaur locomotor evolution, especially in secondarily more sprawling aquatic forms. because it combined methods that previously were not Since then, studies have emphasized a continuum of well-integrated: osteology and myology, form-function postures [37,81,90], admitting that it is difficult to pi- relationships based on rigorous experimental studies of geon-hole taxa into Charig’s grades of sprawling, semi- extant animals, and an explicit phylogenetic context. erect, and erect. This exemplifies the benefits of avoiding vague analo- Walker [96] provided some well-considered refine- gical comparisons, instead focusing on homologous ments of Romer’s studies [see,18,55,56]. Tarsitano [91] form-function complexes. In doing so, old approaches also came to some different conclusions from Romer, emphasizing crocodylian [85–87,91] or avian [75,78] but many of these later were contradicted by stronger were shown to be misleading; both ancestral and de- arguments [68,75,78] (but see [39]). The multitude of rived mechanisms could be inferred in non-avian ther- dinosaur myological studies was nicely reviewed else- opods [39]. Gatesy [36] showed that the hip extensor where [32]. A chief problem with most of these is the M. caudofemoralis longus is crucial for retracting the choice of extant animals for soft data – too often femur during the stance phase of locomotion in extant single taxa (alligators, birds, or ) were used as saurian reptiles. In contrast, he also demonstrated that models rather than all of these animals (and fossil out/ extant birds have de-emphasized femoral retraction dur- ingroups) in an explicit phylogenetic context as is now ing and correspondingly reduced their homo- favoured [18,32,101]. Furthermore, many studies used logue of M. caudofemoralis longus. Flexion/extension myological data to infer ranges of joint motion and limb of the knee joint concurrently became a more crucial orientation, but these usually had inaccurate assump- component of avian locomotion. Gatesy then recon- tions about how muscles control or produce movement structed how the tail and the fourth trochanter on the in living animals. For example, a priori assumptions femur, which are osteological correlates of caudofemor- about how long hip flexor/extensor muscle fibres were, al muscle attachments, gradually reduced in size from or how much they could shorten, were employed to basal archosaurs to crown-group birds. This supported infer how extinct archosaurs moved [20,79,91], but the inference that as these structures were reduced in generally ignored the complex architecture of muscle- theropod dinosaurs, tetanurans (especially coelurosaurs) units [35,102], treating muscles as simple lines. transitioned from the ancestral saurian mechanism of Analogies with extant animals (or optimal design cri- ‘hip-driven’ locomotion toward the more ‘knee-driven’ teria; [76]) are often a mainstay of this functional mor- one typical of walking birds. Furthermore, Gatesy in- phology approach [53]. Form-function relationships are ferred that as the tail shortened, the centre of of typically inferred from an intuitive consideration of these theropod bodies [3] was shifted further craniad, requir- links in extant animals, rather than demonstrated, and ing a more crouched limb orientation. Hence basal di- then transferred to similar anatomies in extinct animals. nosaurs probably stood and moved with more upright This approach will always be a useful foundation for lo- limbs than later non-avian theropods or birds did, and comotor research, but is severely limited, often raising or this transition was probably gradual across the bird line. obscuring more questions than it conclusively answers. These conclusions contradicted some earlier studies For example, analogies between bipedal lizards and ther- [75,78] that emphasized extremely ‘bird-like’ stance J.R. Hutchinson / C. R. Palevol 5 (2006) 519–530 523 and gait even in basal theropods. Gatesy’s [36] conclu- comotor biology, by estimating speeds for fossil - sions have become the consensus, supported and elabo- prints (also [92–94]) using the assumption of dynamic rated on by additional studies [14–17,25,38–46]. similarity. Coombs [28] applied a different quantitative Importantly, this consensus is consilient with the approach to dinosaur locomotion, categorizing dinosaur fossil trackway record, which shows little change in limb proportions and structure into ‘graviportal’, ‘cur- foot placement along the bird line [75] – an erect pos- sorial’, and other functional groups. These classic stu- ture and parasagittal gait were maintained. Until re- dies have had a major impact on the study of archosaur cently, archosaur trackways suffered from the problem locomotion, inspiring more detailed biomechanical stu- that they did not reveal much about how proximal limb dies. Yet it is important to be wary of speed estimates moved during locomotion, beyond general pos- from trackways as these can often be very inaccurate tural clues [39]. Previous trackway studies had diffi- [5], and simple categories of locomotor function can culty integrating track data into whole-limb and phylo- be misleading [15,37]. Furthermore, the importance of genetic perspectives because of the latter problem and limb dimensions for locomotor performance is complex because the identities of trackmakers were unknown and not necessarily related mainly to running speed, so beyond a general taxonomic level. In another major ad- there is no simple test – even with direct data from vance for the field, Gatesy et al. [47] integrated fossil tracks or – for how fast an extinct archosaur trackway data, functional , computer anima- could move. tion, and experimental studies of track-making by birds, The 1970s also saw a burgeoning of studies applying illustrating how deep footprints of basal theropods re- scaling principles of biomechanical relevance to vealed that, early in the stance phase of locomotion, the locomotion [7,66,67]. These methods were later applied metatarsus was held closer to the ground (compared to dinosaur bones [3,14,17,22,23,25,38], convincingly with its more vertical position in birds). Because limb showing from direct osteological evidence that dino- joint angulations are interdependent (see below), this saurs generally changed bone shape with size in ways supported the contention that basal theropods moved similar to most [14,17,23,24]. So far, no with more vertical femora and less bent than ex- clades of non-avian dinosaurs demonstrate limb bone tant birds of similar size [36,43]. This and similar inte- scaling that is stunningly different from isometry or grative studies [100] demonstrate how trackway data slight positive allometry – few scaling patterns match can yield specific information about how archosaur lo- the most extreme scaling in large mammals [8], bovid comotion evolved. artiodactyls [7,67], or even running birds [66]; dino- Hutchinson and Gatesy [61] synthesized anatomical saurian limb design is rather conservative [14,17].Itis [20,55–57,85–87], functional, and phylogenetic data to my impression that bone scaling studies have largely reconstruct how archosaur locomotion evolved (see mined the data to near-exhaustion, for extinct dinosaurs also [41]). We considered four major hindlimb muscle at least, so additional such studies will offer quickly- groups with methods similar to [36], and inferred that diminishing revelations. I do not argue that archosaur locomotor evolution on the line to birds was stepwise, locomotor scaling studies have covered all important involving a plesiomorphic adductor-based postural sup- areas though — osteological data have been empha- port mechanism that transformed into an abductor- sized but little is well known about soft tissue scaling based one in bipedal dinosauriforms, followed by a in many extant taxa, a line of evidence which generally long-axis rotational mechanism in neornithine birds needs more integration with bone scaling [58,59]. and some extinct relatives. These transformations ulti- Alexander [3,4] provided another advancement by mately reduced the adductor/abductor motions and applying static mechanics to interpret dinosaur locomo- muscles associated with the more sprawling posture of tion. He found that body centres of mass tended to lie basal archosaurs. We concluded that these modifica- closer to the hindlimbs (i.e., the hindlimbs may have tions involved alterations not only of anatomy but also supported more weight, perhaps assisting in attaining motor control, although in some cases limb function bipedalism). Also, ‘strength indicators’ for the long evolved without changes of motor control. bones of large dinosaurs were generally comparable to large mammals; for some taxa this supported the infer- 3. Scaling and biomechanical studies ence that they were not very fast runners. Blob [11; also 12] conducted similar bone geometry studies with basal Alexander [2] was the first study to convincingly reptiles and , consistent with the hypotheses transfer knowledge from biomechanics to dinosaur lo- that: (1) many intermediate taxa used a wide variety 524 J.R. Hutchinson / C. R. Palevol 5 (2006) 519–530 of postures from sprawling to erect (as crocodilians do in order to turn [63], which relates more to mass, velo- today; [37,81]), and (2) bone bending stresses increased city, and ground-reaction force production than . in more erect taxa, although a decreased body size or The medially-offset femoral head that evolved at least parasagittal gait would keep stresses lower. Unlike in three times in dinosaurs [16] increased long-axis rota- the origin of mammals and their closest relatives, few tional muscle moment [61], so it may have im- archosaurs experienced a size decrease with a more proved turning ability over the ancestral condition in erect posture, except in dinosaurian ancestors. these lineages. Yet size changes also probably played Recently, an inverse dynamics approach, in which a major role in the evolution of turning capacity, much the forces and moments incurred in a particular limb like straight-line running ability. orientation are estimated and related to the function of Biomechanical research may seem to be a departure muscle-tendon units in locomotion [10,26,84], was ap- from classical anatomically-based work in palaeontol- plied to a variety of bipedal taxa, including birds and ogy, but it can also be seen as a distillation of anatomi- – other theropods [58 60,62]. We have shown that the cal information into its most pertinent components, de- size of ankle extensor muscles is an important limiting scribed in quantitative, physical terms using factor for bipedal running ability, and that this limita- biomechanical methods. Where anatomy is important, tion (along with hip extensor muscle size) reinforces it can be considered in as much detail as needed – with- why larger theropods probably did not run very fast. in the bounds of technological capacity, which has Conversely, smaller bipedal archosaurs probably had a caught up to the level of scientific questioning. Indeed, relatively broader range of running abilities, which con- biomechanics often reveals that the complexity of mor- stricted as they evolved larger body size. Lineages that phology cannot be adequately captured in some tradi- evolved very large body size probably reduced or even tional functional morphology approaches, as multiple lost running ability [28,15,59], although this is contro- levels of interaction (e.g., body segment dynamics, versial for large theropods [33,68,78,79]. Fossil foot- muscle , and motor control) lie between ana- prints have revealed that some dinosaurs of small to tomical structure and animal movement [64,65]. This is medium size ran quickly, whereas so far large dinosaurs my rationale for advocating biomechanical approaches (5,000+ kg) lack known running trackways [33,79,92– in current archosaur locomotor research. However such 94]. The locomotor abilities of early archosaurs are un- methods are no faultless panacea – there are two impor- certain, but early dinosaurs probably were adept run- tant caveats, as follows. ners. Tetanuran dinosaurs evolved a moderately large body size, which was secondarily reduced in coeluro- First, computerized biomechanical simulations of di- saurs, including birds, so running ability probably chan- nosaur locomotion in particular are (and should be) ged repeatedly on the bird line. Likewise, as size in- popular approaches, but these too depend on empirical – ‘ ’ creased/decreased, limb orientation likely became knowledge making a dinosaur move convincingly is more/less upright [38,23,59,62]. a trustworthy conclusion only if it is based on a valid Modern biomechanical approaches have adopted so- method. I urge, and have tried to practice [59], that phisticated computer technologies to analyze complex scientific reconstructions of dinosaur locomotion aspects of dinosaur locomotor biomechanics. 3D com- (whether simple or complex) should be produced using puter renderings of various archosaur bodies have been methods that are shown to work well on extant as well used to estimate body masses, centres of mass, and as extinct animals. This validation step not only builds mass moments of inertia [49–51]. Such models were confidence in the methods and illuminates where they used to estimate turning biomechanics [52], supporting might be weakest, but can also shed light on how extant the hypothesis that turning ability (about a vertical axis) animals work [58], increasing the value of such re- in many bipedal archosaurs was limited by high rota- search. tional inertia [19]. Yet scaling of rotational inertia in Second, many quantitative studies of dinosaurs focus theropods improved turning capacity relative to other on obtaining a single number (or maybe two) as their archosaurs [52], and features such as smaller body size result; e.g., speeds [2,28]. The great degree of potential and shortened further improved rotational inertia error in all methods for reconstructing archosaur loco- along the bird line [19]. Important unaddressed non-in- motion obliges us to emphasize a range of potential ertial components of turning ability include muscular results, using sensitivity analysis to address how much capacity to rotate the trunk about the hip and the capa- what we do not know about extinct taxa (assumptions city to deflect the velocity vector of the centre of mass about missing data) or locomotor dynamics (simplifica- J.R. Hutchinson / C. R. Palevol 5 (2006) 519–530 525 tions of methods) matters for the conclusions drawn of limb function among many taxa, except between ex- about them [58,59]. treme edges of the morphospace, divergent body sizes, Approaches mindful of these two caveats can sub- or anatomical novelties that have major biomechanical stantially advance biomechanical studies beyond the significance. Theropod locomotion evolved gradually trailblazing work of Alexander [2–4], progress that I [36] so there might only be slight differences among argue is an important goal for future studies. many taxa, especially across narrow phylogenetic and functional spectra. This should hold for other archo- 4. Crucial questions and challenges saurs as well. Despite much progress in reconstructing archosaur The inference of function from form is a challenging locomotor evolution (Fig. 1), important details remain enterprise [64,65], but biomechanical and experimental unresolved. How much the locomotion of the common studies offer great promise to tease apart this complex ancestor of the crocodile and bird lines differed from relationship and address fundamental questions about that of extant crocodilians is ambiguous – anatomical how archosaurs stood and moved. We cannot study and trackway data suggest few major differences [61, the locomotion of extinct archosaurs with the experi- 74]. Yet which aspects of crocodilian locomotion are mental methods that Marey and others pioneered, yet apomorphic or parallel acquisitions – and at what level palaeobiological ‘detective work’ and strong inferences within Archosauria – remain vexing mysteries. Bound- can tell us much about this major transition. Such re- ing and galloping locomotor modes are ancestral for search not only depends on form-function principles Crocodylia [83,103], but did any archosaurs share this learned from living animals, but also is a powerful test derived trait or convergently evolve it? [77,89]. of the utility and validity of those principles, as their Whether bipedalism was present in any members of implicit goal is to have broad application and explana- the crocodile line, or if it had anything to do with the tory power [4,6,9]. If we are able to reconstruct in detail origin of crocodilian locomotion, is also uncertain. how archosaur locomotion evolved, this should by re- Moreover, how locomotion evolved from early saurians ciprocal illumination demonstrate how well we under- to Archosauria is largely ambiguous, but surely some stand some locomotor biomechanical principles. Hence important functional changes evolved on this line. I see a fertile synergy where others might see a divisive Many of these questions depend on the establish- dichotomy between neontology and palaeontology, or ment of a stable phylogeny of , between functional morphology and biomechanics. especially for basal archosaurs. Yet an improved bio- Individual extinct archosaurs such as Edmonto- mechanical understanding of structure-function rela- saurus, , and are fascinating tionships in extant crocodilians is just as important as creatures, but studies of locomotion in single extinct phylogenetic resolution. Following crucial earlier ex- archosaur taxa typically provide few revelations unless periments [13,37], recent studies of alligators deter- they are shown to be important components of a broad mined that tail-dragging may increase locomotor ener- question [41]. It is through integrating such studies into getic costs [99], and that whereas hindlimb extensor the broad framework of archosaur locomotor evolution muscles act as expected and increase activity in more that they can become quite informative, especially out- erect postures, muscles other than the ‘adductor’ mus- group taxa on the bird line. Most large dinosaurs, such cles of alligators concurrently increase femoral adduc- as Tyrannosaurus, have negligible importance for un- tion [82]. These experimental findings illuminate what derstanding avian locomotor evolution, but they help changes (reduced tail-dragging, increased hindlimb ad- answer historical questions about how different large ductor and extensor muscle activation) might have ac- land animals support their weight [3,4,58–60,62,68,79, companied more erect postures in archosaurs, lending 80]. Justification of such single-taxa studies however empirical weight to evolutionary speculations. They remains an important consideration – how useful would also reveal how function sometimes does not easily fol- it be to reconstruct how each species of the clade Car- low from structure or meet a priori expectations – with- nosauria moved, for example? This is particularly im- out such tests of form-function relationships, studies of portant in cases in which little evidence for appreciable archosaur locomotor evolution would have little ground functional disparity exists. The morphospace occupied to stand on [81]. by non-avian theropod hindlimbs is quite narrow [14, Locomotor evolution on the bird line also has many 46]. If this anatomical disparity is correlated with func- open questions. Bipedalism among pterosaurs remains tional disparity, then we should expect little difference contentious [72,91,95,98] and depends somewhat on 526 J.R. Hutchinson / C. R. Palevol 5 (2006) 519–530 the phylogenetic position of pterosaurs. This contro- for understanding the evolution of stance and gait in versy also renders inconclusive how many times biped- dinosaurs and other archosaurs, and below I provide a alism evolved in archosaurs, and when habitual striding simple example of how it could be clarified. bipedalism first evolved on the bird line, although some Available evidence supports the hypothesis that bipedal ability was present in the first dinosauriforms. some coelurosaurs stood and moved in more crouched Our increasing understanding of the most basal dino- ‘bird-like’ poses, but still not in the same way as extant saurs and the phylogeny of basal ornithischians, sauro- birds do, and it is expected that this would even apply podomorphs, and theropods [97] is improving resolu- to basal birds like Archaeopteryx. Yet the timing, tem- tion of locomotor evolution in the Triassic, which sets po, and sequence of these changes during theropod evo- the ancestral conditions for the dinosaur radiation. Di- lution are ambiguous. It is widely agreed (reviewed nosaurs evolved quadrupedalism several times [14–17]. above) that the ancestor of crown-group birds and a What specific biomechanical and musculoskeletal fac- few outgroups (Ornithurae) stood and moved much like tors were involved in these transformations are open living birds do, but how much locomotion changed be- questions, although outwardly little else might seem to fore this clade is an interesting question. As heavy, have changed [14,17]. muscular theropod tails turned into ‘dynamic stabili- There has been much discussion on the orientation zers’ and thence into the fronds and finally fans of of the vertebral column in dinosaurs [19,20,34,59,69, feathered flyers [42,44], with the grasping arms follow- 70,75,91] but little resolution. The modern consensus ing suit as they transformed into , what happened seems to be that, like other archosaurs, dinosaur trunks to hindlimb function, the third ‘locomotor module’ were oriented near-horizontally, but likely with much [45]? Did the hindlimbs have much to do with the ori- phylogenetic/behavioural variation [40,78]. Trackway gin of flight [31,71,73] or were they mainly ‘along for evidence supports this conclusion; the early notion that the ride’? The quickening pace of fossil discoveries, the dinosaurs routinely dragged their tails has long been validation and application of biomechanical tools, and dismissed by these data and tail functional anatomy better insight into how living archosaurs work are to- [3,34]. Similarly, various studies have interpreted the gether refining phylogenetic inferences about archosaur relationship between limb joint anatomy and orientation locomotor evolution. Therefore we can expect robust in archosaurs, particularly dinosaurs, quite differently – answers to many of these questions. some contended that similar femoral condyle morphol- ogy indicates very flexed knees in small and large ther- 5. Principles of limb orientation: one way forward opods alike [75,78,79] (but see [23]), whereas others inferred that these flexed articulations were only used I provide here a simple example of how a biomecha- in extreme joint positions, favouring a more straigh- nical perspective could reveal details about how arch- tened limb in large theropods [69]. I have argued else- osaurs stood and moved. A concept implicit in most where [59] that this qualitative evidence is inconclu- previous studies of archosaur locomotion is that, parti- sive, as possible limb orientations in most non-avian cularly in bipeds, for a given orientation of one limb theropods span a wide range from fairly vertical to joint, there is a fairly narrow range of orientations of strongly flexed [33]. the other limb joints that would be functional for stand- The controversies about vertebral column and limb ing and moving. Hence if the hip joint of a bipedal orientation benefit much from a biomechanical perspec- archosaur was fairly flexed, the knee joint must have tive, as this elucidates the relative benefits and tradeoffs been so as well, and this ‘zigzag’ arrangement should of specific poses [59,62]. Although the consensus (re- have continued down the limb. Conversely, a more ex- viewed above; Fig. 1) is that the femur was held in a tended hip joint (i.e. near-vertical femur) would require more vertical position (during standing and slow move- a straighter knee. ment at least) in non-avian theropods compared with In Fig. 2, I use a simple 2D model of a representa- birds, this neither means that it was completely vertical tive bipedal archosaur [59,60] to examine how nar- nor only trivially less flexed than the poses used by rowly limb joint angles can be proscribed in certain extant birds – it likely was positioned somewhere be- conditions, with the assumption that (as during standing tween these extremes. This ambiguity is not trivial or moving in a striding biped) the centre of mass (CM) either – slight differences in limb orientation could have must be positioned over the foot to maintain stability. massive effects on limb mechanics (see below; also The hip angle is arbitrarily fixed at 50° (quite flexed), [58–60,62]). Hence this mystery is an important one the metatarsophalangeal joint varies its angle accord- J.R. Hutchinson / C. R. Palevol 5 (2006) 519–530 527 ingly to keep the vertebral column horizontal at all joint might be very unstable and difficult to control, as the angles of the distal limb, and the pes remains flat on the joint moment would likely oscillate unpredictably be- ground. A ‘static stability space’ exists for those com- tween flexor and extensor moments. Alternatively, binations of joint angles that satisfy the conditions. The keeping the CM cranial to the knee (Fig. 3C) would result is that if the orientation of some joints can be require knee flexor muscle activity to stabilize the knee. established (or bounded) for an extinct archosaur, the At first this might seem useful, as many knee flexors overall limb orientation could be inferred within about also extend the hip and hence could balance moments a15–20° envelope for each joint. about two joints at once. Yet a biped using such a strat- This would still not be ideal, as for a given hip joint egy would need to rapidly switch from using its knee angle, a range of potential knee and ankle angles exists flexors to stabilize the knee to using its knee extensors (Fig. 2). A refinement of this simple approach could in order to propel itself forward, which might be diffi- narrow the envelope of static stability space. For exam- cult to control or energetically expensive. More convin- ple, extant bipeds normally keep their CM just behind cingly, extinct theropods had large knee extensor mus- the knee joint during standing or at mid-stance of loco- cles with fairly high mechanical advantage about the motion [10,26,58,84], maintaining a flexor joint mo- knee joint [57,59,62,77,87], much as extant birds and ment about the knee that requires a knee extensor mus- do [10,58]. Presumably they habitually used cle moment to balance it statically (Fig. 3A). these muscles to balance knee flexor moments during Two alternative strategies have problems that may standing and moving, as extant bipeds do. In other explain why they are not typically observed in habi- words, the mechanism of using knee extensor muscles tually-striding bipeds. Keeping the CM directly above to balance a GRF (or CM) that is behind the knee is the knee (Fig. 3B; i.e., a knee joint moment of zero) most reasonably assumed to be homologous for bipedal dinosaurs, including birds. Hence reconstructions of bi- pedal archosaurs standing or walking with their CM far in front of their knees at mid-stance are less plausible than the mechanism outlined here, and demand strong justification. Certainly during running a more dynamic mechan- ism of stabilization might be important, and during phases of the stride before/after mid-stance the CM is often in front of the knee (e.g., [26]). Regardless, within

Fig. 3. Right hindlimbs of generalized bipeds in three different poses, showing three strategies for positioning the centre of mass (CM; dot) Fig. 2. Ranges of statically stable joint angles for a bipedal archosaur and ground reaction force (GRF; assumed to pass through the CM) (Tyrannosaurus). See text for explanation. The hatched areas relative to the knee joint during standing or mid-stance of locomotion represent regions where the CM is not over the foot and hence static (modified from [58]): A, CM behind the knee as in extant striding stability would be impossible. Stick figures in each corner and the bipeds; B, CM in line with the knee joint centre, resulting in a near-centre of static stability space show the limb orientations for negligible knee joint moment; C, CM in front of the knee, requiring those regions. choice does not matter; the same qualitative active knee flexor muscles to balance. conclusions would hold for any bipedal archosaur. Fig. 3. Membres arrière droits de tous les bipèdes dans trois Fig. 2. Intervalles des angles d’articulation statiquement stables pour différentes postures, montrant trois stratégies de positionnement du un archosaure bipède (Tyrannosaurus). Voir le texte pour les centre de gravité (CM: point) et force de pesanteur (GRF supposée explications. Les zones hachurées représentent les régions où le CM passer au travers du centre de gravité) pour l’articulation du genou, n’est pas au-dessus du pied et où, par conséquent la stabilité statique pendant la locomotion en station debout ou à moitié (modifié d’après serait impossible. Les repères, à chaque coin et proches du centre de [58]):A, centre de gravité en arrière du genou, comme les bipèdes l’espace de stabilité statique, montrent l’orientation des membres pour actuels marchant à larges enjambées ; B, centre de gravité en ligne ces régions. Le choix du taxon n’importe pas ; les mêmes conclusions avec l’articulation du genou ; C, centre de gravité en avant du genou, vaudraient pour tout archosaure bipède. requérant des muscles de flexion du genou actifs pour équilibrer. 528 J.R. Hutchinson / C. R. Palevol 5 (2006) 519–530 the range of limb orientations that could keep the CM [12] R.W. Blob, A.A. Biewener, In vivo locomotor strain in the over the foot at mid-stance, only some of these orienta- hindlimb bones of Alligator mississippiensis and igua- tions would satisfy other biomechanical criteria. Addi- na: implications for the evolution of long bone safety factor and non-sprawling limb posture, J. Exp. Biol. 202 (1999) tional information about position of the GRF (probably 1023–1046. close to midway along the foot), muscle fibre strain or [13] D. 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