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How to Build a Dinosaur: Musculoskeletal Modeling and Simulation of Locomotor Biomechanics in Extinct Animals

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How to Build a Dinosaur: Musculoskeletal Modeling and Simulation of Locomotor Biomechanics in Extinct Animals Paleobiology, 47(1), 2021, pp. 1–38 DOI: 10.1017/pab.2020.46 Featured Article How to build a dinosaur: Musculoskeletal modeling and simulation of locomotor biomechanics in extinct animals Peter J. Bishop* , Andrew R. Cuff , and John R. Hutchinson 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 exe- cution 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 reac- tion 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 estimat- ing 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 repro- ducibility. Although we focus on one specific taxon and question, many of the techniques and philoso- phies explored here have much generality to them, so they can be applied in biomechanical investigation of other extinct organisms. Peter J. Bishop. Structure and Motion Laboratory, Department of Comparative Biomedical Sciences, Royal Veterinary College, Hatfield, U.K.; and Geosciences Program, Queensland Museum, Brisbane, Australia. E-mail: [email protected] Andrew R. Cuff. Structure and Motion Laboratory, Department of Comparative Biomedical Sciences, Royal Veterinary College, Hatfield, U.K.; and Hull York Medical School, University of York, York, U.K. E-mail: [email protected] John R. Hutchinson. Structure and Motion Laboratory, Department of Comparative Biomedical Sciences, Royal Veterinary College, Hatfield, United Kingdom. E-mail: [email protected] Accepted: 6 September 2020 Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.73n5tb2v9 *Corresponding author. Introduction as some evidently did in the Jurassic (Foster Throughout the history of life on Earth, the 2007); there are no 10-tonne bipeds alive today vast majority of species to have ever existed (Hutchinson et al. 2011); and the list goes on. have become extinct. Among those extinct spe- Additionally, the myriad species that bridge cies and lineages is to be found a staggering the anatomical, physiological and ecological div- diversity of body forms, sizes, functions, and ide between disparate major clades today, such ecologies that have no counterpart in the mod- as “fishapods” (stem tetrapods), “mammal-like ern day. Today there are no gargantuan terres- reptiles” (nonmammalian synapsids) “proto- trial, aquatic, or aerial arthropods of the scale birds” (nonavian theropods), and “protowhales” seen in the Paleozoic (Braddy et al. 2008); extant (archaeocete artiodactyls) are absent from mod- marine reptiles present only a fraction of the ern environments (Kemp 2016). It therefore highly diverse phenotypes that existed in the comes as little surprise that research into the Mesozoic (Sues 2019); no modern habitat sus- paleobiology of these enigmatic extinct species tains the number or size of terrestrial herbivores is a long-lived and still-growing field. © The Author(s), 2020. Published by Cambridge University Press. This is an Open Access article, distributed under the Downloadedterms from of https://www.cambridge.org/core the Creative Commons Attribution. IP address: licence 170.106.34.90 (http://creativecommons.org/licenses/by/4.0/, on 25 Sep 2021 at 14:12:21, subject to the Cambridge), whichCore terms permits of unre- use, availablestricted at https://www.cambridge.org/core/terms re-use, distribution, and reproduction. https://doi.org/10.1017/pab.2020.46 in any medium, provided the original work is properly cited. 0094-8373/21 2 PETER J. BISHOP ET AL. Underpinning many aspects of paleobio- Heinrich et al. 1993; Dilkes 2001; Currie 2003; logical research is the concept of uniformitar- Carr and Williamson 2004; Hutchinson et al. ianism (Hutton 1788), that certain principles 2011; Otero et al. 2019). These aspects, com- and phenomena observed in the modern day bined with the dinosaurs’ long evolutionary have always been in action across time and history (>160 million years) and rich fossil space. The laws of the physical world are one record, mean that dinosaurs can be viewed as such set of principles, which lend to the inves- a “natural laboratory” for testing the generality tigation of biological aspects that are influenced of biomechanical principles derived from stud- and constrained by physics, that is, biomechan- ies of extant species (Biewener 1989; Alexander ics. The investigation of biomechanical phe- 2006b). Indeed, careful study of the extremes in nomena in paleobiological enquiry has a long body form and function in dinosaurs could history, and at least some aspect of biomechan- well lead to extensions to current biomechan- ics has been explored in every extinct vertebrate ical principles based on extant species. Framed and many invertebrate groups (Thompson in a comparative context, dinosaur paleon- 1917; Alexander 1989; Thomason 1995). How- tology can therefore add a novel dimension to ever, one group in particular has received pro- biomechanical enquiry—that of “deep time” longed and intensive attention in this field of (Hutton 1788), one which is beyond the familiar study: the dinosaurs, which indeed continue temporal scales of most biomechanists, and yet to lead the charge in the development and one which is intricately linked to the anatomical application of new biomechanical approaches system in question through the process of evo- to the fossil record. lution (Darwin 1859; Taylor and Thomas 2014). The intersection of dinosaur paleontology Nevertheless, this great opportunity comes and biomechanics can be reciprocally illumin- with a variety of challenges, which ultimately ating; not only can biomechanics shed insight stem from the fact that almost all dinosaurs into how dinosaurs functioned as living ani- (along with all other extinct species) are mals (Alexander 1985, 1989, 2006a; Henderson known only from static and often incomplete 2012), but dinosaurs have much to offer the fossilized remains. In this paper, we outline an field of biomechanics, too. As some of the approach that we, as paleontologists, biomecha- most successful vertebrates in history, they nists, and evolutionary biologists, have refined included the largest terrestrial animals to ever over many years to surmount one aspect of exist, for both quadrupeds and bipeds (Colbert the challenge of integrating dinosaur paleon- 1962; Hutchinson et al. 2011; Campione and tology and biomechanics: that of reconstructing Evans 2012; Campione et al. 2014; Bates et al. locomotor biomechanics. A wide variety of 2016, Benson et al. 2018); exhibited repeated methods have been employed in the past for evolutionary increases and decreases in body inferring how a given dinosaur locomoted, size (Sereno 1999; Carrano 2006; Turner et al. including those grounded in comparison to 2007; Benson et al. 2018) and transitions from extant terrestrial vertebrates (Bakker 1971; Alex- bipedal to quadrupedal posture (Charig 1972; ander 1976, 1985, 1989; Coombs 1978; Paul Carrano 2005; Maidment and Barrett 2012, 1988; Gatesy and Middleton 1997; Carrano 2014; Maidment et al. 2014c); and displayed 2001; Moreno et al. 2007), and vary across the substantial disparity in cranial and postcranial continuum from purely qualitative through to anatomy with attendant functional differences extensively quantitative. We do not review (Rayfield 2005; Hutchinson and Allen 2009; them here, and direct the reader to Hutchinson Maidment et al. 2014b; Button and Zanno and Gatesy (2006) and Henderson (2012) for 2020); one lineage evolved an additional useful introductions to the topic, as well as mode of locomotion, powered flight (Ostrom Hutchinson (2012) and Anderson et al. (2012) 1976; Gauthier and Padian 1985; Gatesy 2002; for more general introductions to the integra- Gauthier and Gall 2002; Heers and Dial 2012); tion of biomechanical models in paleontology. and an increasing array of taxa are suspected Rather, we aim here to use dinosaurs as a of having undergone substantial change in vehicle for demonstrating how a careful, struc- functional abilities during ontogeny (e.g., tured, and quantitative approach can maximize Downloaded from https://www.cambridge.org/core. IP address: 170.106.34.90, on 25 Sep 2021 at 14:12:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2020.46 MUSCULOSKELETAL MODELING IN EXTINCT ANIMALS 3 the rigor of the entire process
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