Disparity and Convergence in Bipedal Archosaur Locomotion: K. T. Bates and E. R. Schachner

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J. R. Soc. Interface doi:10.1098/rsif.2011.0687 Published online
Disparity and convergence in bipedal archosaur locomotion

K. T. Bates1, * and E. R. Schachner2,3
1
Department of Musculoskeletal Biology, Institute of Aging and Chronic Disease, University of Liverpool, Sherrington Buildings, Ashton Street, Liverpool L69 3GE, UK 2 Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, UT 84112, USA 3 Marmarth Research Foundation, Marmarth, ND 58643, USA
This study aims to investigate functional disparity in the locomotor apparatus of bipedal archosaurs. We use reconstructions of hindlimb myology of extant and extinct archosaurs to generate musculoskeletal biomechanical models to test hypothesized convergence between bipedal crocodile-line archosaurs and dinosaurs. Quantitative comparison of muscle leverage supports the inference that bipedal crocodile-line archosaurs and non-avian theropods had highly convergent hindlimb myology, suggesting similar muscular mechanics and neuromuscular control of locomotion. While these groups independently evolved similar musculoskeletal solutions to the challenges of parasagittally erect bipedalism, differences also clearly exist, particularly the distinct hip and crurotarsal ankle morphology characteristic of many pseudosuchian archosaurs. Furthermore, comparative analyses of muscle design in extant archosaurs reveal that muscular parameters such as size and architecture are more highly adapted or optimized for habitual locomotion than moment arms. The importance of these aspects of muscle design, which are not directly retrievable from fossils, warns against over-extrapolating the functional signicance of anatomical convergences. Nevertheless, links identied between posture, muscle moments and neural control in archosaur locomotion suggest that functional interpretations of osteological changes in limb anatomy traditionally linked to postural evolution in Late Triassic archosaurs could be constrained through musculoskeletal modelling. Keywords: archosaur; locomotion; bipedalism; Poposaurus; convergence; modelling
1. INTRODUCTION The clade Archosauria contains a staggering level of morphological, functional and ecological diversity that includes living birds and crocodilians, in addition to an array of enigmatic extinct forms such as dinosaurs and pterosaurs [1,2]. Since Romers seminal work on limb anatomy and myology [3,4], archosaur locomotion in particular has stood as a perpetual subject of interest and debate in vertebrate palaeontology and comparative biomechanics. Romers work on extant and extinct archosaurs was built upon in a series of inuential and widely cited studies examining the relationship between osteological anatomy and limb posture in lepidosaurs, crocodilians and dinosaurs [5 7]. However, it was not until formal recognition of living birds as the direct descendants of Mesozoic theropod dinosaurs that the true magnitude of variation in archosaur limb morphology and function was fully appreciated within an evolutionary framework [8 11].
*Author for correspondence (k.t.bates@liverpool.ac.uk). Electronic supplementary material is available at http://dx.doi.org/ 10.1098/rsif.2011.0687 or via http://rsif.royalsocietypublishing.org. Received 7 October 2011 Accepted 2 November 2011
Understanding this disparity requires a unied biomechanical and evolutionary perspective and, in recent years, fossils have played a fundamental role in elucidating aspects of avian biological and functional evolution [9]. Indeed, the study of formfunction evolution in the musculoskeletal system of avian-line (ornithodiran) archosaurs has reached real maturity, with the marrying of traditional anatomical studies with sophisticated mathematicalcomputational approaches [913]. By providing an insight into the musculoskeletal mechanisms used to achieve locomotion in extinct archosaurs, these functional analyses potentially offer a means to more directly test hypotheses about the evolution of archosaur locomotion, selective pressures behind disparate and convergent morphologies, and their relationship to shifts in ecology and biodiversity through the Mesozoic [1,2,57,1417]. Work in this area has to date focused largely on form function evolution along the theropod-bird lineage [911] and on the engineering challenges of large multi-ton body size in animals such as Tyrannosaurus [12,13]. In contrast, extinct crocodile-line (pseudosuchian) archosaurs have received considerably less attention, particularly from serious biomechanical analysis. This is highly surprising, given that the fossil record documents signicant
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2 Bipedal archosaur locomotion K. T. Bates and E. R. Schachner

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Pseudosuchia Suchia Poposauroidea Shuvosauridae Paracrocodylomorpha Archosauria Loricata Dinosauriformes Rauisuchidae Crocodylomorpha Ornithosuchidae Aetosauria Poposaurus gracilis Sillosuchus longicervix Shuvosaurus inexpectatus Rauischus tiradentes Crocodylus niloticus
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Figure 1. (a) Simplied phylogeny for Archosauria modied from Nesbitt [16]. (b) Idealized diagrammatic illustration of the articulated skeleton of Poposaurus gracilis (YPM 57100) in left lateral view, redrawn and modied from Gauthier et al. [8]. (c) Diagram of the ornithodiran buttress erect hip in Tyrannosaurus rex (i), and the suchian pillar erect hip in Poposaurus (ii) in caudal view with the pubes and ischia removed; modied from Schachner et al. [18]. Fe, femur; il, ilium; sab, supra-acetabular buttress.
anatomical (and by inference functional) disparity in their locomotor apparatus, particularly during the Late Triassic, a time of major shifts in biodiversity in terrestrial vertebrate communities [1,2,14]. During this period, pseudosuchian archosaurs underwent evolutionary shifts in locomotor posture, between both quadrupedalism and bipedalism and sprawling to more erect forms, and evolved body plans strikingly similar or convergent to dinosaurs [1,2,1417]. As a result, locomotion has featured prominently in the heated debate surrounding diversication and extinction during the Late Triassic, and the rise of the dinosaurs [1,2,57,14]. However, the hypotheses of functional convergence and mechanical performance between pseudosuchians and dinosaurs (related to concepts of competition and superiority [1,2,57,14]) that underpin this controversy remain untested. Herein, we aim to investigate the evolution of functional disparity in the locomotor apparatus of bipedal archosaurs. In particular, we provide a detailed biomechanical investigation of pelvic and hindlimb muscle mechanics in a bipedal poposauroid (a sub-clade of extinct pseudosuchian archosaurs that includes many bipedal taxa), with the aim of understanding the similarities and differences between the evolution of upright bipedal posture and locomotion in non-dinosaurian archosaurs and the theropod lineage that gave rise to extant birds (gure 1). Our analysis is facilitated by the discovery of a new, largely complete and articulated specimen of Poposaurus gracilis (YPM 57100; gure 1b), which represents the most complete poposauroid skeleton known to date, and is probably the most complete bipedal basal (non-ornithodiran) archosaur yet discovered [8,18]. The exceptional preservation of this specimen has conserved the majority of the muscle attachment sites on the pelvic and hindlimb skeletal elements,
J. R. Soc. Interface
enabling a phylogenetically based reconstruction of hindlimb myology [18] (gure 2a). Investigating functional disparity in bipedal archosaur locomotion will be addressed through a number of more specic questions. Reconstruction of the musculotendinous system of a number of archosaurs in three-dimensional biomechanical models (gure 2) enables us to address our rst two research questions: (i) how disparate are hindlimb muscle moment arms in bipedal archosaurs and (ii) how different are their muscle activation patterns? This is performed by comparing three-dimensional muscle moment arms in a number of exemplar living and extinct archosaurs (gure 2b e) using our modelling approach. By providing estimates of muscle moment arms, this methodology provides valid mechanical comparisons between extinct and extant taxa, and as such, is particularly attractive in the study of fossil species for which other aspects of muscle design (e.g. muscle masses and architecture) are not available [9]. However, just how important is this unfossilized information on muscle design, and what similarities and differences between bipedal archosaurs might be missed by simply restricting analyses of fossil taxa to basic mechanical parameters such as moment arms? To address this important issue, we therefore also tackle two further questions in this study: (iii) to what extent are moment arms diagnostic of specic aspects of locomotion in archosaurs (such as habitual posture and limb kinematics)? or alternatively (iv) are other aspects of muscle design (e.g. mass, architecture, length, etc.) more diagnostic or optimized for habitual gait? In addition to modelling, we therefore also assemble quantitative muscle data from studies of extant archosaurs to investigate correlations between muscle properties
Bipedal archosaur locomotion

(a) IT 1 IT 2 IT 3 (b)
K. T. Bates and E. R. Schachner
CFL FTE PIFE 3
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ADD 2 FTI ILFB FDL G PL FDL TA EDL PB EDB G FDL
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Figure 2. (a) Hindlimb myology of Poposaurus gracilis YPM 57100 (modied from Schachner et al. [18]) and the threedimensional musculoskeletal models of (b) Poposaurus, (c) Alligator, (d) Allosaurus and (e) the ostrich in left lateral view (see table 1 for abbreviations). (Online version in colour.)
(e.g. size and architecture) and overall locomotor style. Specically, we compare living taxa with diverse locomotor strategies in terms of how muscle mass is functionally distributed within their hindlimbs [1923], and use the concept of muscle function space [21] to explore structurefunction links in muscle design. Combining knowledge of these parameters in extant taxa with data from our modelling analysis addresses two fundamental questions in evolutionary biomechanics: how are animals adapted to the functions they perform and is this discernable from fossil evidence? In the current context, this study provides a preliminary dataset to begin disentangling the evolutionary sequence of musculoskeletal changes associated with the various postural shifts that occurred in extinct archosaurs.
2. MATERIAL AND METHODS 2.1. Three-dimensional muscle moment arms The moment arm, or leverage, of a muscle tendon unit can be dened as the shortest perpendicular distance from the joint centre of rotation to the muscles line of action. Moment arms provide qualitative denition of muscle function in terms of the direction of torque they impart at joints, and are fundamental to quantifying how forces generated by muscles are converted to torques at joints. Three-dimensional musculoskeletal models of Poposaurus (YPM57100; gure 2b), Alligator mississippiensis and three ornithodiran bipeds (Allosaurus fragilis, MOR693; Struthiomimus sedens, BHI1266; and an extant paleognath bird, the ostrich,
4 Bipedal archosaur locomotion K. T. Bates and E. R. Schachner Struthio camelus) were constructed in order to quantitatively compare locomotor anatomy by predicting pelvic and hindlimb muscle moment arms (gure 2). These taxa were chosen specically because they belong to theropod sub-groups (carnosaurs (largebodied tetanurans) and Ornithomimosauria) to which bipedal pseudosuchians have been directly compared by previous researchers [1,2,14 17]. The ostrich and Alligator specimens were chosen because limb segment lengths closely matched those of specimens for which muscle architecture and moment arms have been published [19 21]. Information on digitization and model construction can be found in the electronic supplementary material. Pelvic limb muscle attachments in Poposaurus were based on Schachner et al. [18] (gure 2a), and the myologies of the non-avian theropod models were derived from previous reconstructions [10,12,13] (see electronic supplementary material). In the absence of extensive soft tissue preservation in fossils, the denition of muscle paths was guided by information from homologous muscles in extant taxa and osteological correlates of muscle origin and insertion sites [10,12,13]. Muscle homologies and abbreviations are listed in table 1. Biomechanical analyses of the models were carried out in GAITSYM [13]. Effective moment arms of each muscle for joint exion extension at all major hindlimb joints, along with the abduction/adduction and longaxis rotation moment arms of muscles crossing the hip joint, were estimated. The exion extension muscle moment arms in the ostrich model closely match experimentally measured values [18] (see electronic supplementary material), and we therefore infer that predicted abduction/adduction and long-axis rotation moments are good estimates of values for this taxon. Additional data on exion extension moment arms in Tyrannosaurus and Velociraptor were extracted from the literature [12,24] to provide more complete phylogenetic coverage of bipedal ornithodirans. Rather than discuss the relationship between posture and threedimensional moments arms on a muscle-by-muscle basis (which would require comparison of over 200 individual muscles), we concentrate on muscle groups cited as key to three-dimensional control of the hip joint in archosaurs [9,10,12,24 27] and gross comparisons of muscle joint mechanics by summing muscle moments for a given function (e.g. exion, extension, etc.) at each joint angle measured. Moment arms are normalized by the relevant segment length to account for size differences. 2.2. Archosaur muscle data Moment arms allow quantitative comparison of muscle function, but gait is also determined by the size, architectural geometry and contractile properties of muscle tendon units (data not available for fossil taxa). Rather than ignore these crucial aspects of locomotor biology, we explore the disparity in hindlimb muscle parameters available in the literature for living archosaurs and lepidosaurs [1923]. First, we focus on how muscle mass is functionally distributed within the limbs of a number of taxa from these groups by
calculating the percentage of hindlimb muscle capable of inducing specic directional torque at each joint (e.g. hip extension versus exion, hip adduction versus abduction, etc.). Second, we sought to investigate how gross size and architectural properties of proximal hindlimb musculature varied between an exemplar semi-erect, quadrupedal archosaur and an obligate bipedal archosaur. For comparison, hip muscle bre lengths (FLs) from Alligator [21] and ostriches [19] were normalized to body mass0.33 and muscle physiological cross-sectional areas (PCAs) to body mass0.67. Plotting FLs against PCAs produces a muscle function space, providing a basic insight into the relative working range and forcegenerating capacity of muscles within and between taxa (see Allen et al. [21] for discussion). For example, muscles with both relatively large PCAs and FLs are expected to be designed for exerting comparatively high forces over long contraction distances. Relatively smaller PCAs are considered indicative of lower force capability and shorter FLs of reduced contraction working range or distance [21]. In a study of Alligator muscle function, Allen et al. [21] conceptualized the distribution of locomotor muscles in this function space into a number of categories, which are subsequently followed here. Specically, muscles with relatively large PCAs and FLs are considered high-power specialists, muscles with high PCAs but shorter bres are considered force specialists and muscles with low PCAs and relatively long bres are considered displacement specialists. Other factors, such as contraction velocity and moment arm, may exaggerate or mediate differences between muscles in this function space. Where appropriate we integrate moment arm data from our three-dimensional musculoskeletal models to further inform our comparison of muscle function but, for the purpose of this preliminary study, we make the simplication of assuming constant contraction velocity across muscles [21].
3. RESULTS 3.1. Muscle moment arms Muscle moment arm polarities and joint angle relationships in key hip muscle groups [10] are generally conservative despite the shifts in skeletal architecture, posture, body size and locomotor behaviour covered by our sample taxa (gure 3; see electronic supplementary material for full data). This suggests that muscle origins and insertions remained relatively stable with respect to the hip joint across Archosauria. However, a number of interesting differences and trends are present in the data. CFB abducts the femur in Poposaurus, but is an adductor in all other taxa (gure 3b). The cranial portion of the IF group has a much larger medial rotation moment arm in the ostrich (gure 3d). PIFE1 (gure 3e) and 2 extend the hip and rotate the femur laterally in the ostrich, but are hip exors and medial rotators in all other taxa. Abductionadduction and long-axis rotation moment arms are consistently low in Poposaurus, whereas adduction moment arms are generally low in the ostrich but high in Alligator (gures 3 and 4). Much of the above is reected in the summed moment arm data (gure 4). The sum of hip extensor moment
Table 1. Homologies and abbreviations of the pelvic and hindlimb muscles in select extant diapsids. There is some variation within the different groups with respect to muscle presence and morphology, so the condition listed is representative of the inferred plesiomorphic state for the group. Not all pedal muscles are included (based on earlier studies [8,15]). squamata muscles from the pelvis M. iliotibialis (IT) M. ambiens (AMB) M. femorotibialis (FT) M. iliobularis (ILFB) M. iliofemoralis (IFM) M. puboischiofemoralis internus 1 (PIFI) M. puboischiofemoralis internus 2 (PIFI) M. puboischiofemoralis internus 3 (PIFI) M. pubotibialis (PT) M. puboischiotibialis (PIT) M. exor tibialis internus 1 (FTI) M. exor tibialis internus 2 (FTI) M. exor tibialis externus (FTE) M. adductor (ADD) M. puboischiofemoralis externus (PIFE) M. ischiotrochantericus (ISTR) M. caudofemoralis brevis (CFB) M. caudofemoralis longus (CFL) muscles to the pes M. gastrocnemius lateralis (G) M. gastrocnemius medialis (G) M. tibialis anterior (TA) M. popliteus M. peroneus longus (PL) M. peroneus brevis (PB) M. extensor digitorum longus (EDL) M. extensor digitorum brevis (EDB) M. exor digitorum longus (FDL) M. exor digitorum brevis (FDB) M. extensor hallucis longus (EHL) M. exor hallucis longus (FHL) crocodylia M. iliotibialis 1 (IT 1) M. iliotibialis 2 (IT 2) M. iliotibialis 3 (IT 3) M. ambiens 1 (AMB 1) M. ambiens 2 (AMB 2) M. femorotibialis externus (FMTE) M. femorotibialis internus (FMTI) M. iliobularis (ILFB) M. iliofemoralis (IFM) M. puboischiofemoralis internus 1 (PIFI 1) M. puboischiofemoralis internus 2 (PIFI 2) M. puboischiotibialis (PIT) M. exor tibialis internus 1 (FTI) M. exor tibialis internus 2 (FTI) M. exor tibialis internus 3 (FTI) M. exor tibialis internus 4 (FTI) M. exor tibialis externus (FTE) M. adductor 1 (ADD 1) M. adductor 2 (ADD 1) M. puboischiofemoralis externus 1 (PIFE 1) M. puboischiofemoralis externus 2 (PIFE 2) M. puboischiofemoralis externus 3 (PIFE 3) M. ischiotrochantericus (ISTR) M. caudofemoralis brevis (CFB) M. caudofemoralis longus (CFL) M. gastrocnemius externus (G) M. gastrocnemius internus (G) M. tibialis anterior (TA) M. popliteus M. peroneus longus (PL) M. peroneus brevis (PB) M. extensor digitorum longus (EDL) M. extensor digitorum brevis (EDB) M. exor digitorum longus (FDL) M. exor digitorum brevis (FDB) M. extensor hallucis longus (EHL) M. exor hallucis longus (FHL) aves M. iliotibialis cranialis (IC) M. iliotibialis lateralis (IL) M. iliotibialis lateralis (IL) M. ambiens (AMB) M. femorotibialis lateralis (FMTL) M. femorotibialis intermedius (FMT) M. femorotibialis medialis (FMT) M. iliobularis (ILFB) M. iliofemoralis externus (IFM) M. iliotrochantericus caudalis (ITC) M. iliofemoralis internus (IFI) M. iliotrochantericus medialis (ITM) M. iliotrochantericus cranialis (ITCR) M. exor cruris medius (FCM) M. exor cruris lateralis pars pelvica (FCL) M. puboischiofemoralis pars medialis (PIFM) M. puboischiofemoralis pars lateralis (PIFL) M. obturatorius lateralis (OL) M. obturatorius medialis (OM) M. ischiofemoralis (ISF) M. caudofemoralis pars pelvica (CFP) M. caudofemoralis pars caudalis (CFC) M. gastrocnemius pars lateralis (G) M. gastrocnemius pars intermedia M. gastrocnemius pars medialis (G) M. tibialis cranialis (TA) M. popliteus M. bularis longus (FL) M. bularis brevis (FB) M. extensor digitorum longus (EDL) M. exor digitorum longus (FDL) M. extensor hallucis longus (EHL) M. exor hallucis longus (FHL)
arms in all taxa vary considerably with joint angle, but all peak at similar moderately exed joint angles, and decrease with hip exion and extension (gure 4a). Alligator and Poposaurus have summed exor moment arms lower than ornithodiran taxa (gure 4b). Both hip abduction (gure 4c) and adduction (gure 4d) moment arms
also show a clear taxonomic signal in their relative magnitudes. Poposaurus has the lowest summed moment arms for abduction and adduction, followed by nonavian theropods. The ostrich has extremely high values for hip abduction but values equally as low as Poposaurus for hip adduction (gure 4c,d). Alligator has similar

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Figure 3. Predicted pelvic muscle moment arms for hip exionextension (left), abductionadduction (centre) and long-axis rotation (right) in key muscle groups (a) ADD1, (b) CFB, (c) CFL, (d ) IF, (e) PIFE1, ( f ) PIFI2 and (g) PIT over a range of hip joint exion extension angles. See table 1 for abbreviations. All data normalized by femoral length. Only exion extension data are available for Tyrannosaurus and Velociraptor from previous studies [12,24], while PIT is present only in Poposaurus and Alligator, having been lost in ornithodirans (see text for discussion). (Online version in colour.)
overall leverage for abduction as non-avian theropods (gure 4c), but has by far the highest summed adduction moment arms (gure 4d). Predictions for both medial and lateral femoral long-axis rotation produce a similar pattern; Poposaurus has the lowest moment arms, with moderately higher magnitudes for non-avian theropods and Alligator, and signicantly higher magnitudes for the ostrich.
In the rotary crurotarsal ankle joint, the astragalus is xed to the distal end of the tibia and bula. The calcaneum rotates about a peg-like, laterally directed process on the astragalus, bringing about exion and extension of the ankle. Without preservation of any soft tissues around the ankle, the range of motion possible at the joint between the calcaneum and metatarsals in Poposaurus is unclear, and so we present moment arm data

(a) extensor MA/segment length 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0 80 60 40 20 (b) flexor MA/segment length 0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8 2.0
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Figure 4. Sum of (a) hip extensor, (b) hip exor, (c) hip abduction, (d ) adduction, (e) lateral femoral rotation and ( f ) medial femoral rotation muscle moment arms normalized by segment length for Poposaurus, Alligator and ornithodiran bipeds (for further comparisons, see electronic supplementary material). All data normalized by femoral length. Only exionextension data are available for Tyrannosaurus and Velociraptor from previous studies [12,24]. (Online version in colour.)
for both the astragalo-calcaneal and calcaneo-metatarsal joints separately, and in the former case over a wide range of joint angles that likely exceeds maximum exion possible at this joint. At both joints, signicantly higher ankle extensor leverage is predicted for Poposaurus relative to ornithodiran bipeds and Alligator (gure 5) as a direct result of the enlarged calcaneal tuber, which displaces the gastrocnemius and digital exor muscles caudally with respect to the ankle joints (gure 2a). If ankle extensors are allowed to pass through the tuber in the Poposaurus digital model to articially mimic the passage of the ankle extensor tendons along the caudal surface of the astragalus as in ornithodiran taxa, then
ankle extensor moment arms are reduced to broadly similar magnitudes (gure 5). 3.2. Extant archosaur muscle distribution and function The relative contribution to total hindlimb muscle mass of muscles with predominantly hip extension and medial rotation moment arms varies considerably between sampled taxa (gure 6a). Lateral rotators are also somewhat varied, though they have a noticeably higher contribution in Alligator than in other taxa (gure 6a). However, most other categories show at least moderate

(a) extensor MA/segment length 2.1 1.8 1.5 1.2 0.9 0.6 0.3 0 40 60 80 40 20 0 20 astragalo-calcaneal joint angle (Poposaurus) calcaneo-metatarsal joint (Alligator/ornithodirans) () 0 10 20 30 40 50 60 70 calcaneo-metatarsal joint angle () 80 (b)
Alligator Poposaurus Allosaurus Struthiomimus ostrich Poposaurus_NoCalcTub
Alligator Poposaurus Allosaurus Struthiomimus ostrich Poposaurus_NoCalcTub
Figure 5. The sum of ankle extensor moment arms normalized by segment length across a range of ankle exionextension joint angles in our sample of taxa. (a) Extensor moment arms of Poposaurus about the cruscalcaneum joint versus the calcaneum metatarsal joint in other taxa and (b) extensor moment arms across the calcaneummetatarsal joint in all taxa. The enlarged calcaneal tuber of Poposaurus gives its ankle extensor muscles signicantly greater moment arms, particularly at extended joint postures. If ankle extensors are allowed to pass through the calcaneal tuber in the model, then moment arms are more similar to Alligator and the ornithodiran bipeds. All data normalized by length of the metatarsal segment. (Online version in colour.)
distinction between more basal, quadrupedal crocodilians and lepidosaurs and derived avian bipeds in our sample. Hip exors and adductors show the greatest disparity, with crocodilians and lepidosaurs having much higher proportion of muscle mass dedicated to these muscles than birds (gure 6a). Conversely, abductors tend to be relatively larger in Gallus and the ostrich than those of crocodilians and lepidosaurs. A clear distinction at distal joints is also evident (gure 6b). In more basal quadrupedal taxa, the ratio of exor to extensor muscle mass is more equal, whereas bipedal birds invest a signicantly higher proportion of distal limb muscle mass in extensors than exors (gure 6b). The normalized plot of muscle PCA against FL reveals that overall Alligator and the ostrich share closely aligned or overlapping total muscle function space, but vary somewhat in the relative distribution of muscles within this space (gure 6c). In Alligator, the most power-specialized hip muscles are large extrinsic muscles, namely CFL and PIFI2, and also FTE (gure 6c). By contrast, ILFB appears to be the only power-specialist hip muscle in the ostrich (gure 6c). Two muscles in the ostrich, IC and FCL, plot in the extreme displacement-specialist region of function space. Although with shorter bres than IC and FCL in the ostrich, Alligator has a relatively greater number of hip muscles plotting in the displacementspecialist region (IT1, FTI4, ILFB, PIT, ADD1, ADD2, FTI2; gure 6c). Neither taxon appears to have highly force-specialized hip muscles, perhaps consistent with the observation that muscles operating across distal joints, rather than proximal joints, tend to have relatively large PCAs and short bres [21]. The homologous muscles of the iliotibialis group (IT2 in Alligator, IL in the ostrich) are moderately force specialist (gure 6c). The remainder of muscles in
both taxa plot towards lower left extremity of function space and therefore range from weak displacement- to weak force-specialist (gure 6c). 4. DISCUSSION In this discussion, we address our four research questions in two separate sections. First, we evaluate the moment arm estimates from our musculoskeletal models of extinct and extant archosaurs to address the questions of disparity and convergence in muscle moment arms and neuromuscular control of the hip in bipedal archosaurs (questions (i) and (ii) mentioned earlier). In the second section, we use model data, together with muscle data from the literature, to assess whether moment arms or other aspects of muscle design (specically size and architecture) are more optimized (hence predictive) of habitual gait in living archosaurs (questions (iii) and (iv) mentioned earlier). 4.1. Moment arms and neuromuscular control of locomotion in bipedal archosaurs Predicting three-dimensional muscle moment arms in extinct taxa involves a degree of subjectivity. While many muscles have well-constrained origins and insertions in extinct taxa and conserved paths among living archosaurs, others are clearly poorly constrained by fossilized osteology (see Hutchinson et al. [12] for discussion). While these uncertainties must always be acknowledged when reconstructing soft tissues in extinct taxa, homologous muscles in this study were reconstructed with a consistent set of osteological correlates [10,12,13,18] (table 1) and identical geometrical constraints in each model (e.g. position and number of via points dening muscle paths), and each model was

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IL
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PIFI1 PIFI1 ADD1 FTI2 FTI3 CFC PIFL&M ILFB PIT IT1 FTI4 FTI1 ADD2
FCL
IC
0.01
0.02
0.03
0.04 FL/Mbody0.33
0.05
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Figure 6. Muscle mass and architecture in extant lepidosaurs and archosaurs [19,21 23]. (a) Percentage of hindlimb muscle mass capable of exerting torque in specic directions at the hip, specically exion versus extension, abduction versus adduction and medial versus lateral long-axis rotation. (b) Percentage of hindlimb muscle mass capable of extension versus exion at the knee and ankle joints. (c) Muscle function space plot (normalized PCA against normalized fascicle length) for hip muscles of Alligator (lled diamonds) and the ostrich (open squares). See table 1 for abbreviations. (Online version in colour.)
generated with the same methodology. When differences in osteology support clear differences in muscle moment arms, then genuine functional differences in muscular joint control can be safely inferred [10,12,13]. Given these caveats, what are the implications for (i) disparity in hindlimb muscle moments and (ii) neuromuscular control of the hip in bipedal archosaurs? Many Late Triassic pseudosuchians, such as Poposaurus and Postosuchus kirkpatricki, were previously erroneously identied as ancestral dinosaurs or even as basal members of the Dinosauria [14]. This has led to categorization of these basal archosaurs as carnosaur-like (e.g. Postosuchus) [17] and ornithomimidlike (e.g. Efgia) [15,16] and the suggestion that these forms were exploiting similar ecological niches [1,14]. Whether erect posture evolved once at the base of Archosauria or independently in dinosaurs and
basal pseuoduchians is currently unclear. However, bipedal pseudosuchians developed a ventrally projecting acetabulum, or pillar erect hip, in contrast to the laterally projecting acetabulum, or buttress erect hip morphology of ornithodiran bipeds (gure 1). The three-dimensional model quantitatively demonstrates that the acetabular osteology of Poposaurus, and by inference that of other pillar-erect pseudosuchians, is clearly synchronized with a conguration of muscle leverage signicantly geared towards limb protraction retraction rather than either abductionadduction or long-axis rotation (gures 3 and 4). This contrasts sharply with Alligator (and by inference other sprawling to semierect quadrupedal archosauromorphs) in which high adduction and rotational moment arms aid in producing large arcs of non-parasagittal motion in abducted, rotary gaits (see later text). Bipedal poposauroids possess a
os
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ar
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K. T. Bates and E. R. Schachner ornithodiran archosaurs [12], which would likely have been a major contributor to hip extension and limb retraction during stance, as in living Alligator [26] (see later text). Understanding the functional signicance of lower leverage for non-sagittal rotation and differences in individual muscles is not straightforward (see below), but clearly these differences suggest some limit to the functional convergence of basal tetanuran theropods and bipedal pseudosuchians. Nevertheless, obligate pseudosuchian bipeds still faced the same fundamental constraints on stability as ornithodirans, namely the need to balance a net adduction moment at the hip during limb support. During the support phase, bipedal animals typically place the foot beneath the body medial to the hip, incurring an adduction moment at the hip joint. In basal theropods, Hutchinson & Gatesy [10] proposed that stance phase hip stability was achieved through a counteractive abduction moment created by activation of the IF muscles placed dorsal to the hip joint (gure 2). In extant birds, the IF group has shifted its origin cranially, increasing its moment arm for medial rotation (gure 3d). Stance phase activation of the IF group is retained, but medial rotation of the femora is employed to counter the adduction moment of the ground reaction force (GRF). Pubic retroversion in birds also shifts the origins of the PIFE group caudal to the hip joint, switching its function from hip exion and medial rotation to extension and lateral rotation (gure 3e). Hutchinson & Gatesy [10] inferred a stepwise evolution from the abductor-based mode of limb support in basal bipedal Dinosauriformes to the long-axis rotational mechanism in crown-group birds. Although our phylogenetic coverage across Theropoda is not sufcient to detail the timing and specic nature of this transition, it is clear that muscle leverage for both medial and lateral femoral long-axis rotation is much higher in the ostrich relative to basal tetanurans, Poposaurus and Alligator (gures 3e,f and 4e,f ). Our models, therefore, support Hutchinson & Gatesys [10] hypothesis that rotational moment arms increased along the line to birds, and further suggest that this occurred in groups more derived than basal tetanurans (e.g. Maniraptora). Adduction moment arms are also greatly reduced in the ostrich (gure 4d), resulting largely from pubic and ischial retroversion and caudolateral expansion of the pelvis, which moved muscle origins close, and in some postures lateral, to the hip joint (switching their function to hip abduction and lateral rotation). Together with the cranial expansion of the preacetabular ilium, this explains the maintenance of relatively high abduction moment arms in the ostrich (gure 4c). While noting differences in the magnitude of muscle leverage (gures 3 and 4), we infer that stance phase lateral limb stability in bipedal suchians was achieved in the same manner as inferred for basal theropods, specically a support phase abduction moment generated by the IF group (gure 7), represented by IFM in Poposaurus [18]. Given the triradiate arrangement of the pelvis, and the likely more upright posture and caudofemoralis-driven limb retraction, it is likely that femoral abduction predominantly countered the adduction GRF moment in Poposaurus, rather than medial rotation as in extant
deep, perforate ventrally facing acetabulum as well as vertically orientated ilia, and lacks an offset femoral head (gures 1 and 2). Furthermore, in poposauroids the femoral head forms a rounded bulge with only slight deviation from the proximal shaft and lacks the signicant medial offset achieved by the distinct neck present in dinosaurs [25,28]. The femoral head inserts tightly and ventrally into the acetabulum, and abductionadduction and long-axis rotation are tightly constrained by the prominent supra-acetabular crest in this pillar erect conguration (gure 1c). As a result, muscle insertions on the femora are situated close to both their pelvic origins and the hip joint in the mediolateral plane, producing relatively low moment arms for hip abduction adduction and long-axis rotation (gures 3cf and 4cf ). This conguration has a slightly lesser effect on hip adduction moment arms in Poposaurus (gures 3d and 4d) owing to the more distal insertions of adductor muscles (distal femoral and tibial insertions) and the fact that the femoral shaft is somewhat laterally inclined when articulated properly with the acetabulum. In tetanuran theropods, the enlarged barrel-like femoral head and neck laterally offset the proximal femur (gure 1c) and its associated muscle insertions from the mediolateral plane of the hip joint and pelvic muscle origins, thereby relatively enhancing their abduction and long-axis rotation moment arms (gures 3c,e,f and 4c,e,f ). The dorsoventrally taller ilia and enlarged and laterally situated femoral trochanters of tetanuran theropods further increase the moment arms of proximal muscles for abduction and long-axis rotation [25] relative to poposauroids. When three-dimensional hip moments are considered, Poposaurus differs from both Alligator and non-avian theropods. Indeed, in most aspects of muscle leverage ( particularly abductionadduction and long-axis rotation moment arms), large-bodied tetanurans (carnosaurs [17]) and ornithomimids are shown to be more similar to each other than either is to Poposaurus (gures 3 and 4). Furthermore, differences in specic muscles are also evident in Poposaurus, notably the adductor group (ADD1 and 2) and CFB. A raised process midway down the caudal aspect of the femoral shaft and a vertically oriented ridge that extends distally from this process are reconstructed as the insertion sites of ADD1 and 2 in Poposaurus [18]. These insertion sites of the adductor complex in Poposaurus are signicantly larger than those in any other archosaur, extinct or extant (see electronic supplementary material). Also, Nesbitt [2] and Brusatte et al. [1] note that the large ventrally directed fossa present on the posteroventral surface of the ilium of poposauroids (e.g. Poposaurus, Efgia and Shuvosaurus) is likely analogous to the brevis fossa present in dinosaurs and subsequently reconstruct CFB origins on this surface, as we do in our models [18]. However, this example of convergent osteology is not matched in functional predictions for the associated CFB. In nonavian theropods, this muscle passes posteroventrally to the hip joint centre, producing a weak adduction moment arm, while in Poposaurus CFB originates and passes dorsolateral to the joint centre, yielding a weak abduction moment arm (gure 3b). Poposaurus also retains PIT, a muscle hypothesized to have been lost in

(a) PIFI12 PIFE1 (b)
11
CFB IFM ADD1 ADD2 CFL
PIFE2 PIT
Figure 7. Hindlimb muscles hypothesized to be active during the (a) swing and (b) stance phase of locomotion in Poposaurus. See table 1 for abbreviations. (Online version in colour.)
birds [10], which is greatly aided by enhanced muscle leverage for this action (gures 3 and 4). In Poposaurus, the IF group maintains higher moment arms for abduction and a position dorsal to the hip joint, consistent with the morphology and hip abduction mode of lateral limb support proposed for non-avian theropods [10] (gures 3d and 4). The long slender femur of bipedal suchians is poorly suited to resisting bending and torsional stresses incurred under a exed avian-like posture and a rotational-based system of muscular support [25]. Thus we infer the same shift in neural control of the IF group from swing phase abduction and protraction (in basal quadrupedal archosaurs and Alligator) to stance phase abduction as hypothesized by Hutchinson & Gatesy [10] for basal Dinosauriformes (gure 6). If these hypotheses of multiple independent shifts in motor control of the IF group are correct, then this functional and neurological adaptation may be ubiquitously associated with the evolution of bipedalism in archosaurs. Gatesy [26] showed that femoral protraction was achieved through swing phase activation of the PIFI group and PIFE1 and 2 in Alligator, while the CFL retracts the femur during stance, helping in controlling abduction of the lower limb (gure 3c) [26]. ADD1 and 2 and PIT also activate during early stance to prevent collapse by resisting femoral abduction (gure 3a) [26]. Major femoral protractor (e.g. PIFI1 and 2, PIFE1 and 2) moment arms in Poposaurus are similar to Alligator, and it is likely that swing phase activation of the PIFI group and PIFE1 and 2 was present in Poposaurus (gure 7a), as in extant archosaurs [10]. Thus, the plesiomorphic archosaurian stance phase activation of these muscles was likely maintained in bipedal pseudosuchians, as in quadrupedal Alligator, despite their change in posture (gure 7b). 4.2. Muscle design and locomotion in living archosaurs: how redundant is fossil evidence? By integrating moment arm predictions from threedimensional musculoskeletal reconstructions with muscle activation patterns measured in living taxa, it is possible to constrain aspects of limb control and habitual locomotion in extinct bipeds such as
Poposaurus and non-avian theropods. On the basis of this data, an abductor-based mode of stance phase limb support mediated by the IF group is supported for bipedal pseudosuchians, as previously suggested for non-avian theropods [10], and it is likely that both groups used a predominantly hip-based system of limb retraction, in contrast to exed postures and predominantly knee-based limb retraction observed in extant birds [10,25,27]. Musculoskeletal models also produce trends that appear to reect differences in limb control and habitual locomotion in living archosaurs, notably the high leverage for hip adduction in Alligator important for large arcs of femoral rotation and resisting lateral limb collapse during stance in abducted postures [26]. The ostrich also has relatively high values for femoral long-axis rotation but very low hip adduction moment arms, consistent with relatively adducted posture and a rotational-based system of lateral limb support [10] (gure 4c,d ). Our rst three research questions asked how disparate are muscle moment arms in archosaurs and to what extent do they appear optimized for habitual locomotion? Qualitative and quantitative disparity in muscle moment arms estimates do appear to differentiate major functional categories in terms of locomotor mechanics, specically animals with quadrupedal rotator gaits from parasagittal bipeds, and bipeds with abductor-based versus rotation-based mechanisms of lateral limb support. However, it is clear that beyond these broad functional dichotomies, muscle moment arms alone are unable to provide clear insight into aspects of locomotion such as habitual kinematics and maximal performance. For example, hip extensor moment arms in Alligator are extremely similar (quantitatively and qualitatively; gures 3 and 4a) to the ostrich despite signicant differences in the habitual limb motion and locomotor ability (e.g. running ability) of these taxa (see below). Indeed, summed leverage for hip extension is both similar in magnitude and its angular dependency in extinct and extant taxa modelled here (gure 4). This has been observed despite numerous anatomical and functional changes, such as the retention of PIT and ve exor cruris muscles in pseudosuchians (FTI12 and 4 are lost in neornithine birds) [10], and pubic
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K. T. Bates and E. R. Schachner Homologous single-joint hip extensors in Alligator and the ostrich are generally consistent with their relative locomotor styles and the magnitude of hip joint excursions. Muscles of the adductor femoris group (ADD1 and 2 in Alligator and PIFM and PIFL in the ostrich) are noticeably more displacement specialist in Alligator, while the caudofemoralis of the ostrich is signicantly reduced in terms of both force (PCA) and working range (FL). Pubic retroversion means that OM and OL in the ostrich (homologues of PIFE1 and 2 in Alligator) are single-joint hip extensors, and OM plots in force-specialized function space, though OL is moderately displacement specialized (gure 6c). Single-joint hip exors (IFI, ITCR) in the ostrich also show reduced FLs and PCA compared with Alligator (PIFI1 2) again reecting lesser joint excursion at the hip in birds (gure 6c). Consistent with conceptualization of their locomotion as hip-based and knee-based, the relative magnitude of joint excursion at the hip is reversed at the knee; Alligator exhibits less than 208 exion extension at the knee [30] versus 50 558 in the ostrich [29]. Knee extensors in the ostrich are spread across a wide range of function space, including those capable of generating force over larger working ranges (notably IC and IL; gure 6c) and large PCA, short-bred force-specialist muscles (e.g. femorotibial group muscles; gure 6c). By contrast, two-joint (gure 6c) and one-joint knee extensors [21] in Alligator are predominantly forcespecialist (e.g. IT2) or weakly specialized for force or displacement (i.e. more generalist; IT3, IT1, AMB), and therefore less well suited to generating force over a large working range. The architecture of knee exors is best understood in terms of their role in three-dimensional control of the hindlimb. In Alligator, members of the exor cruris group are responsible for adducting the limb during late swing and into the stance phase [26], and indeed many knee exors plot close to other limb adductors (e.g. ADD1 and 2) in moderately displacement-specialist function space (gure 6c). Hamstring muscles with moderately longer bres may therefore reect the use of relatively large adduction arcs in Alligator (approx. 35408 at the hip [30]). FTE is active in stance in Alligator [26] and it is possible that this moderately power-specialist muscle (gure 6c) principally assists with hip extension and anti-gravity support. Ostriches habitually rotate their femora through much smaller arcs of abductionadduction (approx. 108 [29]), and during stance they exert a medial rotation moment at the hip to resist limb collapse through adduction (rather abduction as in Alligator). PIT, FTI1 2 and FTI4 were lost during avian evolution [10] and it is noteworthy that birds retain exor cruris muscles with the largest moment arms for hip extension (also important during stance) [31] and that the adduction leverage of these muscles (and others; gure 4) is reduced owing to lateral expansion of the pelvis, at least in our ostrich model, relative to Alligator (gures 3 and 4; electronic supplementary material). This comparative analysis of Alligator and the ostrich emphasizes that muscular parameters such as size and architecture (gure 6) are highly adapted to
retroversion in birds switching the function of PIFE1 and 2 from exion to extension (gure 3 and also see electronic supplementary material). Furthermore, where disparity in moment arms exists, it is important to remember that this may be balanced by compensatory differences in muscle mass or architecture. For example, Alligator is predicted to have relatively low overall leverage for hip exion, but muscle data suggest that this may be compensated for by the relatively high mass of hip exor muscles (gure 6a). Analyses of muscle size and architecture in living archosaurs (addressing our fourth research question) strongly suggest that these unfossilized traits are more indicative or optimized for habitual gait (gure 6). Even in slow running gaits (approx. 3.3 m s21), ostriches have been shown to maintain a relatively exed hip between 2488 and 608 [29], whereas in fast walking (approx. 0.62 m s21), Alligator retracts the femur from around 2408 hip exion to approximately 608 hip extension [30]. This is a considerable difference in joint excursion and one that cannot be diagnosed from moment arms alone (gures 3 and 4). Experimental studies have shown CFL and PIFI2 to be the prime retractors (CFL) and protractors (PIFI2) of the limb in Alligator [26,27]. Our results suggest that CFL and PIFI2 do not have the highest exion extension moment arms in Alligator, nor are their moment arms substantially larger in Alligator than the ostrich (gure 3c,f ). CFL inserts on the proximal femur and tibia and is active during stance to retract the entire limb, generating much of the power required for acceleration and gravitational support [26,27,30]. PIFI2 originates in front of hip and is active during swing to protract the limb. As noted by Allen et al. [21], CFL and PIFI2 are the largest muscles in the Alligator hindlimb, both of these extrinsic muscles plotting in the power-specialized region of muscle function space (gure 6c). The long FLs and high PCAs (especially CFL) of these muscles make them ideally suited for generating high forces across the large working range habitually used by Alligator in terrestrial locomotion [26,30]. In the ostrich, the most powerful hip extensor is ILFB (gure 6c), a two-joint muscle that also exerts a exor moment at the knee. The hip extension moment arm for ILFB is considerably higher in the ostrich than Alligator (electronic supplementary material, gure S4i), consistent with the idea that synchronous hip extensor and knee exor moments may be important during late swing and early stance in birds while the GRF passes cranial to the knee joint (see Gatesy [31] and below for discussion). Thus, differences in both architectural design and the moment arm of ILFB appear consistent with the contrasting limb segment movements in Alligator and the ostrich. In the ostrich, a larger PCA and extensor moment arm enable signicant contribution to early stance antigravity support at the hip, while relatively long bres allow force to be generated for knee exion over a wider working range (gure 6c). In Alligator, ILFB is active near the stance swing transition, contributing to knee exion and femoral abduction [26], which may require less force over a shorter range of joint angles relative to the ostrich.
Bipedal archosaur locomotion their usage and loading during habitual locomotion. This has a number of important implications for evolutionary biomechanics. In itself, it is an important form function nding that muscles appear to be optimized more in terms of size and architecture rather than moment arms. These data suggest that locomotor adaptations in archosaurs have been largely achieved by selection of these traits rather than by alteration of moment arms. By emphasizing the importance of aspects of muscle design that are not directly retrievable from fossil animals, this analysis illustrates the difculty of discerning detailed measures of gait and performance in extinct taxa. Sophisticated computational simulations are now commonly used to study detailed muscle dynamics and locomotion in living animals, and recently some of these approaches have been used to explore aspects of gait and performance in fossil species [3234]. The challenge facing palaeobiologists and biomechanicists attempting to construct these models for extinct archosaurs clearly lies in dening muscle properties (inputs into biomechanical models) in a meaningful and objective way. It is highly unlikely that either living crocodilians or birds provide good analogues for muscle properties in nonavian dinosaurs and bipedal pseudosuchians. It may therefore be more appropriate to employ a wider functional bracket approach [33] to quantitative muscle reconstruction in extinct archosaurs. For example, muscle FLs in Alligator and the ostrich appear to correlate well with habitual joint excursions, perhaps suggesting FLs might be more precisely constrained or estimated as a proportion of length change over the likely range of joint motion in extinct taxa. Where attempts have been made to simulate locomotion in extinct archosaurs, redundancies in muscle input values have been addressed using sensitivity analyses; plausible ranges for input values, rather than single values, are tested resulting in a spectrum of gait predictions [33,34]. Where fossilized osteology is similar, along with estimatable parameters such as muscle moment arms, as we have shown to be the case with bipedal pseudosuchians and non-avian theropods (gures 3 and 4), then more detailed tests of functional disparity and convergence may be extremely difcult owing to large (hence overlapping) error bars on predictions [9,34]. However, where gross anatomy differs more considerably, then functional disparity may be more robustly established. We illustrate this using a simple analysis of muscle moments at the ankle joint in our sample of archosaurs. 4.3. Archosaur ankle mechanics Our analysis of muscle moment arms and mass distribution within the hindlimbs of extant lepidosaurs and archosaurs reveals a dichotomy in the ratio of muscle mass devoted to joint extensors versus exors (gure 6a,b). Bipedality naturally requires greater limb joint extension capacity because only two limbs are supporting the body against gravity (versus four in quadupedality). This represents a greater constraint during locomotion, and particularly running with an aerial phase when a single limb must support the body, versus multiple limbs in a quadruped. In
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archosaurs, functional disparity appears to be the greatest at the ankle joint, where skeletal morphology and moment arms also differ signicantly. Pseudosuchians (and particularly Poposaurus; gure 5) have relatively higher ankle extensor moment arms, while crown-group birds have a much higher proportion of hindlimb muscle mass (and body mass) as ankle extensor musculature than more basal quadrupedal taxa (gure 6b). The latter is particularly true of extant ratites such as the ostrich, a trait that underpins its ability to generate high muscle torques at the ankle [19,20]. Unless basal taxa were very poor runners, these data strongly suggest that the evolution of bipedalism in ornithodirans was likely coupled with a notable increase in ankle extensor muscle mass relative to basal, quadrupedal archosaurs, possibly reaching masses proportionally similar to those in extant terrestrial birds. This phylogenetic and functional pattern clearly emphasizes the crucial role of the calcaneal tuber in bipedal pseudosuchian locomotion. By increasing ankle extensor moment arms, retention of the calcaneal tuber (plesiomorphic for Archosauria) may have eliminated the need for higher ankle extensor muscle masses hypothesized for ornithodiran bipeds. Ankle extensors in the ostrich are noticeably more power-specialized (i.e. higher PCA, longer FL) than those of Alligator, suggesting a higher capacity to contribute to limb acceleration and support [1921]. These different strategies for ankle joint control may have had further consequences elsewhere in the hindlimb, particularly as most large ankle extensors also cross the knee joint in archosaurs (gure 2). Stance phase activation of ankle extensors would have synchronously imparted a exor moment at the knee, which was probably undesirable given knee extension was likely required to contribute to straightening the limb during the second half of stance. By increasing ankle extensor moment arms in bipedal pseudosuchians, the enlarged calcaneal tuber may have produced larger muscle torques distally in the limb, without major impacts at the knee that might be incurred purely from an increased ankle extensor muscle mass. The potential for disparity in relative ankle extensor muscle masses, moment arms and lengths in pseudosuchians versus ornithodirans (gures 5 and 6) highlights this joint as a key area for future biomechanical studies of disparity in archosaur locomotor evolution.
5. CONCLUSIONS This quantitative analysis supports inferences that bipedal suchians were generally similar to large-bodied basal tetanurans (carnosaurs) [7,17] and ornithomimids [15,16] in their basic hindlimb muscular mechanics and neuromuscular control of locomotion. These groups independently evolved similar musculoskeletal solutions to the challenges of parasagittally erect bipedalism. Homologous muscles responsible for femoral protraction and retraction retained plesiomorphic activation patterns. However, the IF musculature, responsible for swing phase abduction in basal quadrupedal archosaurs and Alligator, retained its moment arm but switched to stance phase activation to provide lateral limb stability in an adducted bipedal
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W. Joyce and T. Lyson for access to specimens at the Yale Peabody Museum, and L. Bryant, S. Foss and A. Titus (Bureau of Land Management); R. Whilhite, D. Connor (http://reptileadventures.net), J. Atterholt, National Geographic, and NHNZ for archosaur specimens; P. Dodson and B. Grandstaff for dissection assistance; C. Farmer and K. Sanders for access to CT data on A. mississippiensis; and S. Gilbert and B. Pinder for laboratory space at Swarthmore College. This work was partially supported under a National Science Foundation grant to S. Gilbert (RUI-0740508). Funding was also provided by the SVP Student Member Travel Grant, Palaeontological Association Sylvester-Bradley Award, Paleontological Society Stephen J. Gould Student Research Grant, the University of Pennsylvania Summer Stipend in Paleontology and the Teece Dissertation Research Fellowship. For information on E.R.S.s illustrations, see www.theropoda.com. Comments and suggestions from S. Brusatte, C. Sullivan, C. Sarrazin, S. Maidment and an anonymous reviewer greatly improved the manuscript.
posture in both bipedal pseudosuchians and non-avian theropods. Musculoskeletal models also produce moment arm estimates that appear to reect some general differences in hindlimb control and habitual locomotion in living archosaurs. Notably, the high leverage for hip adduction in Alligator appears consistent with the need to adduct the limb and counteract abduction moments in rotary gaits, while high values for femoral long-axis rotation moment arms in the ostrich help facilitate the rotation-based mode of lateral stance phase support present in birds [10]. These ndings support a link between posture, muscle moment arms and neural control in archosaur locomotion, and perhaps suggest that interpretations of osteological changes in pelvic and hindlimb morphology and links to postural evolution in Late Triassic pseudosuchians [1,2,5 7,14 17] could be appropriately constrained through the quantitative reconstruction of muscle moment arms, as we have carried out here. While analyses such as these provide a quantitative measure of the convergence and disparity in musculoskeletal bauplans and their relationships to postural evolution, it is important to emphasize that they do not test directly for similarities or differences in gait. Muscles function to convert metabolic energy to mechanical work, and it is the rate of contraction and the amount of work performed in a single contractionextension cycle that is the crucial muscular determinant of gait and performance. Muscle dynamics are dictated primarily by their mass, architecture and contractile properties [35], and a more sophisticated analysis is required to test for disparity and convergence beyond the resolution of the broadest functional categories (e.g. quadrupedal rotator gaits versus parasagittal gaits, bipeds with abductor-based versus rotation-based mechanisms of lateral limb support). This clearly limits our ability to even qualitatively assess how the walking and running gaits of bipedal pseudosuchians and ornithodirans may have differed dynamically in biomechanical terms. We therefore urge that our conclusions regarding comparative musculoskeletal anatomy are not over-extrapolated to make biomechanical speculations about similarities in locomotor performance in extinct taxa, and subsequently to support or reject macroevolutionary hypotheses regarding, for example, pseudosuchian and dinosaur diversity during the Late Triassic [1,2,5 7,1417]. Analysing functional convergence and mechanical performance (related to concepts of competition and superiority [57,14]) from purely osteological characterswhether that be through structurefunction analogies [57,17] or statistical measures of disparity [14] as previously attemptedignores many important causative factors underlying formfunction relationships and at best provides an abstract picture of animal locomotion. Musculoskeletal models, and their insights into functional anatomy, provide a rm foundation for further biomechanical studies to test notions of functional convergence and dominance more directly.
The authors thank W. Sellers for support with GAITSYM; P. Manning for laboratory space at the University of Manchester; J. Gauthier, C. Norris, M. Fox, D. Brinkman,
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13 Bates, K. T., Benson, R. B. J. & Falkingham, P. L. In press. A computational analysis of muscle leverage and body size in Allosauroidea (Dinoauria:Theropoda). Paleobiology. 14 Brusatte, S. L., Benton, M. J., Ruta, M. & Lloyd, G. T. 2008 Superiority, competition and opportunism in the evolutionary radiation of dinosaurs. Science 321, 14851488. (doi:10.1126/science.1161833) 15 Nesbitt, S. J. & Norell, M. A. 2006 Extreme convergence in the body plans of an early suchian (Archosauria) and ornithomimid dinosaurs (Theropoda). Proc. R. Soc. B 273, 1045 1048. (doi:10.1098/rspb.2005.3426) 16 Nesbitt, S. J. 2007 The anatomy of Efgia okeeffeae (Archosauria, Suchia), theropod-like convergence, and the distribution of related taxa. Bull. Am. Mus. Nat. Hist. 302, 184. (doi:10.1206/0003-0090(2007)302[1: TAOEOA]2.0.CO;2) 17 Chatterjee, S. 1985 Postosuchas, a new thecodontian reptile from the Triassic of Texas and the origin of Tyrannosaurs. Phil. Trans. R. Soc. Lond. B 309, 395460. (doi:10.1098/rstb.1985.0092) 18 Schachner, E. R., Manning, P. L. & Dodson, P. 2011 Pelvic and hindlimb myology of the basal archosaur Poposaurus gracilis (Archosauria: Poposauridaea). J. Morph. 272, 1464 1491. (doi:10.1002/jmor.10997) 19 Smith, N. C., Wilson, A. M., Jespers, K. J. & Payne, R. C. 2006 Muscle architecture and functional anatomy of the pelvic limb of the ostrich (Struthio camelus). J. Anat. 209, 765 779. (doi:10.1111/j.1469-7580.2006.00658.x) 20 Smith, N. C., Payne, R. C., Jespers, K. J. & Wilson, A. M. 2007 Muscle moment arms of pelvic limb muscles of the ostrich (Struthio camelus). J. Anat. 211, 313324. (doi:10.1111/j.1469-7580.2007.00762.x) 21 Allen, V., Ellsey, R., Jones, N., Wright, J. & Hutchinson, J. R. 2010 Functional specialisation and ontogenetic scaling of limb anatomy in Alligator mississippiensis. J. Anat. 216, 423 445. (doi:10.1111/j.1469-7580.2009.01202.x) 22 Verstappen, M., Aerts, P. & De Vree, F. 1998 Functional morphology of the hindlimb musculature of the blackbilled magpie, Pica pica (Aves, Corvidae). Zoomorphology 118, 207 223. (doi:10.1007/s004350050070) 23 Zaaf, A., Herrel, A., Aerts, P. & De Vree, F. 1999 Morphology and morphometrics of the appendicular musculature in geckoes with different locomotor habits (Lepidosauria). Zoomorphology 119, 922. (doi:10.1007/s004350050077)
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24 Hutchinson, J. R., Miller, C. E., Fritsch, G. & Hildebrandt, T. 2008 The anatomical foundation for multidisciplinary studies of animal limb function: examples from dinosaur and elephant limb imaging studies. In Anatomical imaging techniques: towards a new morphology (eds R. Frey & H. Endo), pp. 2338. Berlin, Germany: Springer. 25 Carrano, M. T. 2000 Homoplasy and the evolution of dinosaur locomotion. Paleobiology 26, 489512. (doi:10.1666/ 0094-8373(2000)026,0489:HATEOD.2.0.CO;2) 26 Gatesy, S. M. 1997 An electromyographical analysis of hindlimb function in Alligator during terrestrial locomotion. J. Morph. 234, 197212. (doi:10.1002/(SICI)10974687(199711)234:2,197::AID-JMOR6.3.0.CO;2-9) 27 Gatesy, S. M. 1990 Caudofemoralis musculature and the evolution of theropod locomotion. Paleobiology 16, 170186. 28 Parrish, M. J. 1987 The origin of crocodilian locomotion. Paleobiology 13, 396 414. 29 Rubenson, J., Lloyd, D. G., Besier, T. F., Heliams, D. B. & Fournier, P. A. 2007 Running in ostriches (Struthio camelus): three dimensional joint axes alignment and joint kinematics. J. Exp. Biol. 210, 25482562. (doi:10.1242/ jeb.02792) 30 Blob, R. W. & Biewener, A. A. 2001 Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis). J. Exp. Biol. 204, 10991122. 31 Gatesy, S. M. 1999 Guineafowl hind limb function. II. Electromyographic analysis of motor pattern evolution. J. Morph. 240, 127 142. (doi:10.1002/(SICI)10974687(199905)240:2,127::AID-JMOR4.3.0.CO;2-Q) 32 Sellers, W. I., Cain, G. M., Wang, W. & Crompton, R. H. 2005 Stride lengths, speed and energy costs in walking of Australopithecus afarensis: using evolutionary robotics to predict locomotion of early human ancestors. J. R. Soc. Interface 5, 431441. (doi:10.1098/rsif.2005.0060) 33 Sellers, W. I. & Manning, P. L. 2007 Estimating dinosaur running speeds using evolutionary robotics. Proc. R. Soc. B 274, 27112716. (doi:10.1098/rspb.2007.0846) 34 Bates, K. T., Manning, P. L., Margetts, L. & Sellers, W. I. 2010 Sensitivity analysis in evolutionary robotic simulation of bipedal dinosaur running. J. Vert. Paleontol. 30, 458466. (doi:10.1080/02724630903409329) 35 Alexander, R. M. 2003 Principles of animal locomotion. Princeton, NJ: Princeton University Press.
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Electronic Supplementary Material
Disparity and convergence in bipedal archosaur locomotion
Bates, K.T. & Schachner, E.R.
Institutional Abbreviations used in main text and supplementary data: BHI, Black Hills Institute of Geological Research, Hill City, South Dakota, USA; MOR, Museum of the Rockies, Montana State University, Bozeman, Montana, USA; YMP, Yale Peabody Museum of Natural History, New Haven, Connecticut, USA.
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2. MATERIAL AND METHODS (a) Musculoskeletal model construction Full description of model construction methods can be found in Bates et al. (in press), but are repeated here for completeness. For comparison to the 3D model of Poposaurus gracilis (YMP 57100), the specimens of Allosaurus fragilis (MOR 693) and Struthiomimus sedens (BHI 1266) were chosen because they represent the most complete and well preserved pelvic and hindlimb osteologies within their respective theropod sub-clades. These taxa were chosen specifically because they belong to theropod sub-groups (carnosaurs [large bodied tetanurans] and Ornithomimosauria) to which bipedal pseudosuchians have been directly compared by previous researchers (e.g., Bonaparte 1984; Chatterjee 1985; Nesbitt 2007; Nesbitt and Norell 2006). The ostrich specimen (BB.3462) mounted at the Manchester Museum (UK) was chosen because mass
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data was available from a previous study (Bates et al. 2009a) and limb segment lengths closely matched those of specimens for which muscle architecture and moment arms have been published (Smith et al. 2006, 2007). A Polhemus FastSCAN cobra laser scanner (www. polhemus.com) was used to acquire high resolution scans of bone surface geometry of the femur, tibia, fibula, metatarsals and pes of each of the specimens and these were combined with LiDAR (Light Detection And Range) scans of pelvic bones from previous studies (Bates et al. 2009a&b). The resolution of the Polhemus scan depends on wand-object range, and is typically 0.5mm at 200mm range. The scanner is useable up to a range of 0.75m, with an accuracy of approximately 1mm at 200mm range. The scanner operates in real-time and instantly acquires a three dimensional surface image as the handheld scanning wand is swept over an object. The device works by projecting a fan of laser light onto the object while the camera views the laser to record cross sectional depth profiles. The real-time visual feedback on the laptop screen makes controlling the scan wand straightforward and enables monitoring and a high level of quality control on data capture. In order to scan the full 3D surfaces the casts of each limb bone were placed on flat surfaces scanned and then turned over and scanned again, with effort made to scan as much area as possible to ensure maximum amount of overlap in two different scans. Two separate scans of the each bone were then aligned automatically using PolyWorks (www.innovmetric.com) on basis of overlapping areas (see Bates et al. 2008 for more information). Point clouds were then surfaced using a trial version of Silverlining (www.farfieldtechnology.com) which generates smooth meshes through point-cloud data or incomplete mesh data, producing well-formed water tight meshes for computer graphics and rapid prototyping. The Computer-Aided Design (CAD) package Maya (www.autodesk/maya) was used to digitally rearticulate hindlimb bones and reconstruct 3D muscle-tendon units and joint centre positions. As far as possible the femora were re-orientated so that lateral surfaces of the greater and lesser
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trochanters faced laterally and the anterior surface of the shaft faced cranially and the axis of the femoral head was orientated at 90 degrees to the vertical. The hip joint centre was then specified as the centre of curved medial articular surface of the femoral head sitting within the acetabulum. The shank segment (tibia and fibula) was then re-orientated beneath the femur so that the medial side of the tibial crest lay in the same longitudinal plane as the medial femoral condyle and so that the femoral condyles were centred craniocaudally on top of the tibia, in accordance with Hutchinson et al. (2005, 2008). Again following Hutchinson et al. (2005, 2008), limb bones were displaced at joints to account for the thickness of unpreserved joint tissues. Specifically an additional 7.5% was added to femoral length, 5% to tibiotarsus length and 10% to metatarsal length (Hutchinson et al. 2005). The rigid pelvic segments (combined ilium, ischium and pubis) remained in the articulated positions of the skeletal mounts, but were rotated together so that the pelvis was pitched horizontally. Hip joints were modelled as 3D ball-and-socket joints and all distal joints (knee, ankle, metartarsopharngeal etc.) were treated as simple hinges with one degree of freedom (i.e. flexion/extension). All joints were considered orthogonal and the flexion and extension axes were defined as planar and perpendicular to the cranial-caudal axis of the body (the x-axis in the global co-ordinate system of the models). Rubenson et al. (2007) demonstrated that ostriches do not have orthogonal or uniformly aligned limb joint axes and it is likely that the same applied to the extinct taxa in this study. However, reconstructing joint axes is in extinct taxa is not possible due to the absence of joint tissues and the redundancy in joint articulations and movements (Gatesy et al. 2009). We therefore used the simpler, standardized approach to defining joint axes in all models, including the ostrich, to maintain comparative value. In the case of the ostrich this also allowed comparison of predicted moment arms with the experimental data of Smith et al. (2007), which also assumed simple planar orthogonal joint axes. For broad comparison with published data on theropods (Gatesy et al. 2009; Smith et al. 2006, 2007) and for subsequent modelling we estimated total Range Of Motion (ROM) at major hindlimb joints in
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Poposaurus using the computer model and through manual manipulation of the fossil bones. Our intention was not an extensive comparison of articular morphology and joint ROM but rather to broadly delimit the maximum plausible 3D movement given the fossilized osteology available. Pelvic and femoral musculature in nonavian theropods was reconstructed on the basis of osteological correlates of homologous muscle-tendon origins and insertions in extant archosaurs (Hutchinson 2001a&b, 2002; Carrano and Hutchinson 2002; Bates et al. in press; Fig S1). A total of
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Fig. S1. Reconstruction of pelvic and femoral muscle origins and insertion in A, Allosaurus, and B, Tyrannosaurus on the basis of archosaurian muscle homologies and the EPB of extant crocodilians and birds (image modified from Bates et al. in press, with B redrawn from Carrano and Hutchinson (2002) by E.R.S). 31 muscles were placed in each limb of the three nonavian theropod models and these are listed in Table 1 in the main text, along with their abbreviations. Muscle origin and insertions in Poposaurus were based on Schachner et al (in press). This reconstruction is based upon the direct examination of the osteology and myology of phylogenetically relevant extant taxa in conjunction with osteological correlates from the skeleton of Poposaurus. This data set includes a series of inferences (presence/absence of a structure, number of components, and origin/insertion sites)
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regarding 26 individual muscle or muscle groups, three pelvic ligaments, and two connective tissue structures in the pelvis, hindlimb, and pes of Poposaurus. The origin and insertion sites of muscles are listed in Table S1 and shown in Fig. S2. A combination of via points and cylindrical wrapping surfaces were used to guide 3D muscle paths from origin to insertion points (see Sellers et al. 2003). In the absence of extensive soft tissue preservation in fossils, the precise choice of locations for via points is inevitably arbitrary but can be appropriately guided by information from homologous muscles in extant taxa and skeletal architecture. As far as possible, the 3D paths reconstructed by Hutchinson et al. (2005) for Tyrannosaurus were qualitatively followed here, as these were inferred on the basis of homologous muscle layering observed in extant archosaurs and conform to observations by the authors in dissections (Bates et al. in press; Schachner et al. press). Care was taken to ensure the relative position of via points in homologous muscles were consistent across the models, except where variation was necessitated by skeletal differences and/or to preserve muscle layering. All models in this study were constructed by the same author to minimize individual variation.
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Table S1. Origin and insertion of pelvic and hindlimb muscles inferred in Poposaurus.
MUSCLE IT 1, 2+3 AMB FT ILFB IFM PIFI 1 ORIGIN Dorsal margin of the ilium (I) Depression on the lateral surface of the proximal pubis (I) Majority of the femoral shaft (I) Crest on the lateral postacetabular ilium (I) Supraacetabular crest and lateral preacetabular ilium (I) Cranial margin of the ilium, dorsal to the pubic process (II) Ventral aspect of the preacetabular process (II) Craniolateral surface of the ischium (II) Caudolateral surface of the postacetabular ilium (I) INSERTION Tibial cnemial crest (I) Tibial cnemial crest (I) Tibial cnemial crest (I) Fibular tubercle (I) Lateral surface of the proximal femur (I) Proximolateral surface of the femur (I) Proximolateral surface of the femur (I) Proximal tibia (II) Proximal tibia (I)
PIFI 2 PIT FTI
FTE ADD 1 ADD 2 PIFE 1 PIFE 2 PIFE 3 ISTR CFB CFL G (lateral head) G (medial head) TA POP PL PB EDL EDB FDL FDB EHL FHL
Caudolateral surface of the postacetabular ilium (I) Cranioventral ischial shaft (I) Caudodorsal ischial shaft (II) Ventral surface of the pubic apron (II) Lateral surface of the pubic boot (II) Lateral surface of the ischial boot (II) Medial surface of the ischium (II) Iliac brevis fossa (II) Caudal vertebral centra (I) Caudolateral femur just distal to the insertion of ADD2 (I) Proximal medial tibia (I) Cranial surface of the proximal tibia (I) Proximal medial fibular shaft (I) Lateral fibula (I) Lateral fibula (I) Lateral femoral condyle (I) Craniomedial surface of the tarsals (II) Caudal femur, distal to GL (I) Plantar aponeurosis (II) Cranial surface of the distal fibula (II) Caudolateral aspect of the femur (I)
Proximal tibia (I) Flange on the caudal surface of the femoral shaft (I or II?) Caudal surface of the distal femoral shaft (I or II?) Caudal surface of the proximal femur (I) Caudal surface of the proximal femur (I) Caudal surface of the proximal femur (I) Lateral surface of the proximal femur (I) Medial surface of the femur (I) Medial surface of the femur (I) Plantar surface of metatarsals IIV with medial head (II) Plantar surface of metatarsals IIV with lateral head (II) Proximodorsal surface of metatarsals I-III (IV?) (I) Distal lateral tibial shaft (I) Calcaneal tuber (II) Caudolateral surface of metatarsal V (I) Distal end of the dorsal shaft of metatarsals I-IV (II) Dorsal surface of the phalanges (II) Ventral surface of phalanges and unguals (I) Ventral surface of the phalanges (II) Dorsal surface of metatarsal I Ventral surface of the distal phalanx and ungula of digit I (I)
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Fig S2. Reconstruction of the origins and insertions of pelvic limb musculature of Popsoaurus in left lateral view (modified from Schachner et al. In press). Abbreviations: Abbreviations: ADD 1-2, M.
adductor 1-2; AMB, M. ambiens; CFB, M. caudofemoralis brevis; CFL, M. caudofemoralis longus; FT, M. femorotibialis; FTE, M. flexor tibialis externus; FTI, M. flexor tibialis internus; EDB, M. extensor digitorum brevis; EDL, M. extensor digitorum longus; FDL, M. flexor digitorum longus; G, M. gastrocnemius; GL, M. gastrocnemius lateralis; IFM, M. iliofemoralis; ILFB, M. iliofibularis; ISTR, M. ischiotrochantericus; IT 1-3, M. iliotibialis 1-3; PB, M. peroneus brevis; PIFE 2-3, M. puboischiofemoralis externus 2-3; PIFI 1-2, M. puboischiofemoralis internus 1-2; PIT, M. puboischiotibialis; PL, M. peroneus longus; TA, M. tibialis anterior.
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Ostrich model
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The origins, insertions and 3D paths of 29 pelvic limb muscles were mapped on to the 3D model of the ostrich, using observations from cadaveric dissections and aided by published myological
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descriptions (Gangl et al. 2004; Smith et al. 2006). To measure the accuracy of the reconstructed muscle moment arms of the 3D model its predictions were compared with those derived experimentally from manipulation of cadaveric specimens using the tendon travel method (Smith et al. 2007). The results are shown in Figure S3. Overall the model predictions show an extremely close match to the experimental data, particularly given the level of intra-specific variation present in muscle moment arms for ostriches (Smith et al. 2007). However, a number of consistent differences are present between the model and experimental data. Notably hip extensor moment arms decrease in magnitude to much a greater extent with increasing hip flexion in the experimental data than in the 3D model. The range of motion used in the tendon travel experiments of was largely defined by the movement permitted by the tissues in the cadaveric limbs (Smith et al. 2007; Smith personal communication 2010), hence extensor moment arms are restricted to angles of 5-35 degrees hip joint flexion (versus 0-85 degrees in the 3D model). Ostriches have been shown to reach 60 degrees hip joint flexion during slow running (Rubenson et al. 2007), which would necessitate activation of muscles with extensor moment arms to support the limb at the hip. Extrapolation of the slopes of the experimental hip extensor muscle moment arms beyond 35 degrees flexion results in the prediction that all measured hip extensors, with the exception of FCM and ILFB, switch to being hip flexors by 45 degrees hip joint flexion, with ILFB switching at roughly 65 degrees. Under such circumstance the animal would be unable to counter the net flexor moment at the hip during stance at limb angle recorded in kinematic studies (Rubenson et al. 2007). By contrast, all hip anti-gravity muscles retain extensor moment arms across the entire range of joint motion (i.e. up to 85 degrees hip flexion) in the 3D model, consistent with the mechanics of ostrich running and walking gaits (Rubenson et al. 2004, 2007) and with the geometric relationship between these muscles and the hip joint in this taxon. Hip extensor muscles in the ostrich originate from the pelvis a considerable distance caudoventrally and caudodorsally to the hip joint. Insertion on the femur from this relative direction means that
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Fig S3. Comparison of the flexion-extension moment arms of (a-e) hip, (f-g) knee and (h-i) ankle muscles in the 3D model of the ostrich (BB.3462) to the experimental results of Smith et al. (2007).
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hip extensors are only likely to switch to flexor moment arms when the hip is in hyper-extension, not simply greater degrees of flexion. Thus we are unable to explain the pronounced decline in extensor muscle arms with increasing hip flexion in the experimental data of Smith et al. (2007) and conclude that the 3D model provides a more plausible approximation of moment arms for these muscles in the ostrich. The knee joint moment arms of ILFB and FTM (FMT in Smith et al. 2007) in the 3D model also show relatively poor agreement with the experimental measurements. Smith et al. (2007) found that ILFB retained a relatively large flexor moment arm about the knee joint across their full range of measured angles. Although ILFB has similar flexor moment arm magnitudes at extended knee postures (<45 degrees) in the 3D model (Fig. S3f), this muscle quickly switches to being an extensor at flexed joint angles. This represents a limitation in the 3D model. Currently the 3D path of a muscle can be controlled by either via points or wrapping cylinders in GaitSym, but both features cannot be used in the same muscle. Via points were used to produce a realistic hip extensor moment arm for ILFB, but were not sufficient to provide realistic muscle geometry for this muscle around the back of the knee at highly flexed angles. Addition of a wrapping surface for ILFB behind the knee joint would solve this problem, but such a feature cannot be combined with via points in the current version of GaitSym. In the 3D model FTM is consistent with all other knee extensors in that its magnitude is highest at extended joint angles and decreases linearly with increasing knee flexion (Fig. S3f-g). This pattern was true for all knee extensor muscles in the other models in this study and indeed all other knee extensors in the cadaveric experiments (Fig. S3f-g; Smith et al. 2006). This discrepancy likely results how the muscle path around the craniolateral side of the knee was controlled in the tendon travel experiments of Smith et al. (2007) relative to our model. However, given the skeletal and muscle geometry we would expect the extensor moment of the FTM to decrease with increasing joint flexion, as in all other knee extensors, and thus we are confident in the predictions of our model.
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RESULTS
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data
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Figure S4. Predicted muscle moment arms for hip flexion-extension (left), abduction-adduction (centre) and long axis rotation (right) in Poposaurus, Alligator and ornithodiran bipeds over a range of hip joint flexion-extension angles. (a) ADD1, (b) ADD2, (c) AMB, (d) CFB, (e) CFL, (f) FTE, (g) FTI1, (h) FTI3, (i) IFB, (j) IFMa, (k) IFMp, (l) ISTR, (m) IT1, (n) IT3, (o) PIFE1, (p) PIFE2, (q) PIFE3, (r) PIFI1, (s) PIFI2, and (t) PIT. Abbreviations: ADD, M. adductor; AMB, M. ambiens; CFB, M. caudofemoralis brevis; CFL, M. caudofemoralis longus; FTE, M. flexor tibialis externus; FTI1, M. flexor tibialis 1; FTI3, M. flexor tibialis 3; IFB, M. iliofibularis; IFMa, M. iliofemoralis of Poposaurus against ITC of ornithodirans; IFMp, M. iliofemoralis of Poposaurus against IFE of ornithodirans p; ISTR, M. ischiotrochantericus; IT1 & 3, M. iliotibialis 1 & 3; PIFE 2-3, M. puboischiofemoralis 1-3; PIFI1-2, M. puboischiofemoralis 1-2; PIT, M. puboischiotibialis.
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(b)Adductor femoris muscle insertions in Poposaurus In the main text we state that a raised process midway down the caudal aspect of the femoral shaft and a vertically oriented ridge that extends distally from this process are reconstructed as the insertion sites of ADD1 and 2 in Poposaurus (Schachner et al. in press). These insertion sites of the adductor complex in Poposaurus are significantly larger than those in any other archosaurs,
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extinct or extant. Figure S5 shows the insertion sites of ADD1&2 inferred for Poposaurus gracilis YMP57000 (Schachner et al. In press) compare with those of Tyrannosaurus rex (FMNH PR2081) based on personal observations and the reconstructions of Carrano and Hutchinson (2002; their Fig. 6).
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Figure S5. Insertions of the adductor femoris muscles (ADD1&2) on the caudal surface of the left femur in (a-b) Tyrannosaurus rex (FMNH PR2081) and (c-d) Poposaurus gracilis (YMP5700). Abbreviations: ADD 1-2, M. adductor 1-2.
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REFERENCES Bates, K. T., Benson, R. B. J. & Falkingham, P. L. In press. A computational analysis of muscle leverage and body evolution in Allosauroidea (Dinosauria: Theropoda) with implications for locomotion. Paleobiology.
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Bates, K.T., Manning, P.L., Hodgetts, D. & Sellers, W.I. 2009a Estimating mass properties of dinosaurs using laser imaging and computer modelling. PLoS ONE 4(2), e4532 doi:10.1371. Bates, K.T., Falkingham, P.L., Breithaupt, B.H., Hodgetts, D., Sellers, W.I. & Manning, P.L. 2009b How Big Was Big Al? Quantifying the effect of soft tissue and osteological unknowns on mass predictions for Allosaurus (Dinosauria:Theropoda). Palaeo. Electron. 12(3), 14A, 33p. Bates, K.T., Rarity, F., Manning, P.L., Hodgetts, D., Vila, B., Oms, O, Galobart, A. & Gawthorpe, R.L. 2008 High-resolution LiDAR and photogrammetric survey of the Fumanya dinosaur tracksites (Catalonia): implications for the conservation and interpretation of geological heritage sites. J. Geol. Soc. Lond. 165, 115-127. Bonaparte, J.F. 1984 Locomotion in rauisuchid thecodonts. J. Vert. Paleo. 3, 210-218. Carrano, M.T. & Hutchinson, J.R. 2002 Pelvic and Hindlimb Musculature of Tyrannosaurus rex (Dinosauria: Theropoda). J. Morph 253, 207-228. Chatterjee, S. 1985 Postosuchas, a new thecodontian reptile from the Triassic of Texas and the origin of Tyrannosaurs. Phil. Trans. R. Soc. B 309, 395-460. Gangl,D., G. E., Weissengruber, M. Egerbacher & G. Forstenpointner. 2004 Anatomical Description of the Muscles of the Pelvic Limb in the Ostrich (Struthio camelus). Anat. Hist. Embry. 33 (2), 100-114. DOI: 10.1111/j.1439-0264.2003.00522.x Gatesy, S.M., Baeker, M. & Hutchinson, J.R. 2009 Constraint-based exclusion of limb poses for reconstructing theropod dinosaur locomotion. J. Vert. Paleo. 29, 535-544. Hutchinson, J.R. 2001a The evolution of pelvic osteology and soft tissues on the line to extant birds (Neornithes). Zool. J. Linn. Soc. 131, 123-168.
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Disparity and Convergence in Bipedal Archosaur Locomotion: K. T. Bates and E. R. Schachner

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Disparity and Convergence in Bipedal Archosaur Locomotion: K. T. Bates and E. R. Schachner

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J. R. Soc. Interface doi:10.1098/rsif.2011.0687 Published online

Disparity and convergence in bipedal archosaur locomotion

This journal is q 2011 The Royal Society

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2 Bipedal archosaur locomotion K. T. Bates and E. R. Schachner

Pterosauromorpha Ornithodira Ornithischia Sauropodomorpha

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Bipedal archosaur locomotion

K. T. Bates and E. R. Schachner

CFL FTE PIFE 3

ADD 2 FTI ILFB FDL G PL FDL TA EDL PB EDB G FDL

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Bipedal archosaur locomotion

K. T. Bates and E. R. Schachner

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6 Bipedal archosaur locomotion K. T. Bates and E. R. Schachner

hip joint angle ()

hip joint angle ()

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Bipedal archosaur locomotion

K. T. Bates and E. R. Schachner

40 (d) adduction MA/segment length (f)

(c) abduction MA/segment length 0 0.5 1.0 1.5 2.0 2.5

medial rotation MA/segment length

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8 Bipedal archosaur locomotion K. T. Bates and E. R. Schachner

Alligator Poposaurus Allosaurus Struthiomimus ostrich Poposaurus_NoCalcTub

Alligator Poposaurus Allosaurus Struthiomimus ostrich Poposaurus_NoCalcTub

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Bipedal archosaur locomotion

K. T. Bates and E. R. Schachner

%knee extensor %knee flexor %ankle extensor %ankle flexor

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Bipedal archosaur locomotion

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Bipedal archosaur locomotion

K. T. Bates and E. R. Schachner

CFB IFM ADD1 ADD2 CFL

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Bipedal archosaur locomotion

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K. T. Bates and E. R. Schachner

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Bipedal archosaur locomotion

K. T. Bates and E. R. Schachner

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Bipedal archosaur locomotion

K. T. Bates and E. R. Schachner

Electronic Supplementary Material

Disparity and convergence in bipedal archosaur locomotion

Bates, K.T. & Schachner, E.R.

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PIFI 2 PIT FTI

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178 (a) Complete hip muscle moment arm 179

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