How to build a dinosaur: Musculoskeletal modeling and simulation of locomotor biomechanics in extinct animals

Abstract

The intersection of paleontology and biomechanics can be reciprocally illuminating, helping to improve paleobiological knowledge of extinct species and furthering our understanding of the generality of biomechanical principles derived from study of extant species. However, working with data gleaned primarily from the fossil record has its challenges. Building on decades of prior research, we outline and critically discuss a complete workflow for biomechanical analysis of extinct species, using locomotor biomechanics in the Triassic theropod dinosaur Coelophysis as a case study. We progress from the digital capture of fossil bone morphology to creating rigged skeletal models, to reconstructing musculature and soft tissue volumes, to the development of computational musculoskeletal models, and finally to the execution of biomechanical simulations. Using a three-dimensional musculoskeletal model comprising 33 muscles, a static inverse simulation of the mid-stance of running shows that Coelophysis probably used more upright (extended) hindlimb postures and was likely capable of withstanding a vertical ground reaction force of magnitude more than 2.5 times body weight. We identify muscle force-generating capacity as a key source of uncertainty in the simulations, highlighting the need for more refined methods of estimating intrinsic muscle parameters such as fiber length. Our approach emphasizes the explicit application of quantitative techniques and physics-based principles, which helps maximize results robustness and reproducibility. Although we focus on one specific taxon and question, many of the techniques and philosophies explored here have much generality to them, so they can be applied in biomechanical investigation of other extinct organisms.

The evolution of pelvic limb muscle moment arms in bird-line archosaurs

“…Both increased IT1 and IT2 hip flexor leverage (nodes Dinosauria onward; especially early theropods) and reduction in CFL and CFB hip extensor leverage (past nodes Averostra and Avetheropoda) therefore predated reduction in the relative size of the caudofemoral muscles [from Coelurosauria onward, as indicated by tail anatomy; ( 4 , 11 , 12 )] by several phylogenetic nodes. Large muscles with low leverage [as expected for IT1, IT2, and other hip flexors even in early theropods; e.g., ( 16 )] can produce fast, powerful “high-geared” motions ( 29 ). Thus, we infer that the ability of the hindlimb to be protracted during swing phase phylogenetically “led” the overall reduction of capacity to retract it during stance phase because larger hip flexor muscles with lower leverage preceded the evolution of smaller hip extensors with lower leverage.…”

“…Toward the middle of the support phase (“midstance”), the ground-reaction force (GRF) vector of a steady-state striding bipedal tetrapod is more or less vertically oriented between the center of pressure in the foot and the CoM ( 13 ). The position of the CoM constrains femoral posture (at least around midstance), as the knee joint tends to be placed cranial to the CoM in order for the knee extensor muscles to provide support forces to counter the GRF [( 14 , 15 ), but see ( 16 )].…”

“…However, as stated, much of the inferences from muscle function rest on qualitative assessments of muscle moment arms (leverage) based on simple observations. Muscle sizes are also important, and their evolution has been qualitatively gauged from bone dimensions [e.g., ( 5 , 16 , 23 )] or even quantitatively estimated ( 12 ). All other factors being equal, larger moment arms tend to increase joint moments but decrease joint rotational velocity or mobility.…”

A new role for joint mobility in reconstructing vertebrate locomotor evolution

“…The resulting locomotor hypotheses can then be tested using other parameters such as bone strain, energy expenditure, balance, and/or similarity of ground reaction forces to those of extant species (following refs. 1 , 13 , and 14 ), ultimately improving our understanding of the locomotion of individual extinct archosaurs and reshaping analyses of archosaurian locomotor evolution (e.g., ref. 12 ).…”

“…These charismatic “ruling reptiles” have undergone repeated transformations in locomotor posture and mode ( 12 ) and are by far the most frequent subjects of locomotor reconstructions (e.g., refs. 3 , 13 , and 14 ). Here we carried out a marker-based X-ray reconstruction of moving morphology (XROMM) ( 15 ) analysis of unprecedented magnitude to measure nearly 600,000 in and ex vivo poses from the hindlimb joints of two living archosaurs—the Helmeted Guineafowl and American alligator—that represent an extant phylogenetic bracket for the archosaurian ancestor and its pseudosuchian (crocodilian line) and ornithodiran (bird line) descendants.…”