Disparity and convergence in bipedal archosaur locomotion

Abstract

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 significance of anatomical convergences. Nevertheless, links identified 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.

Figure 1.

(a) Simplified phylogeny for Archosauria modified from Nesbitt [16]. (b) Idealized diagrammatic illustration of the articulated skeleton of Poposaurus gracilis (YPM 57100) in left lateral view, redrawn and modified 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; modified from Schachner et al. [18]. Fe, femur; il, ilium; sab, supra-acetabular buttress.

Figure 2.

(a) Hindlimb myology of Poposaurus gracilis YPM 57100 (modified from Schachner et al. [18]) and the three-dimensional 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.)

Figure 3.

Predicted pelvic muscle moment arms for hip flexion–extension (left), abduction–adduction (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 flexion–extension angles. See table 1 for abbreviations. All data normalized by femoral length. Only flexion–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.)

Figure 4.

Sum of (a) hip extensor, (b) hip flexor, (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 flexion–extension data are available for Tyrannosaurus and Velociraptor from previous studies [12,24]. (Online version in colour.)

Figure 5.

The sum of ankle extensor moment arms normalized by segment length across a range of ankle flexion–extension joint angles in our sample of taxa. (a) Extensor moment arms of Poposaurus about the crus–calcaneum joint versus the calcaneum–metatarsal joint in other taxa and (b) extensor moment arms across the calcaneum–metatarsal joint in all taxa. The enlarged calcaneal tuber of Poposaurus gives its ankle extensor muscles significantly 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.)

Figure 6.

Muscle mass and architecture in extant lepidosaurs and archosaurs [,–23]. (a) Percentage of hindlimb muscle mass capable of exerting torque in specific directions at the hip, specifically flexion versus extension, abduction versus adduction and medial versus lateral long-axis rotation. (b) Percentage of hindlimb muscle mass capable of extension versus flexion at the knee and ankle joints. (c) Muscle function space plot (normalized PCA against normalized fascicle length) for hip muscles of Alligator (filled diamonds) and the ostrich (open squares). See table 1 for abbreviations. (Online version in colour.)

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.)