Ontogenetic changes in the body plan of the sauropodomorph dinosaur Mussaurus patagonicus reveal shifts of locomotor stance during growth

Otero, Alejandro; Cuff, Andrew R.; Allen, Vivian; Sumner‐Rooney, Lauren; Pol, Diego; Hutchinson, John R.

doi:10.1038/s41598-019-44037-1

Cited by 55 publications

(54 citation statements)

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“…), and a recent study has hypothesized a shift from quadrupedalism to bipedalism during ontogeny based on change in the body plan and its centre of mass (Otero et al . ).…”

Section: Discussionmentioning

confidence: 97%

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A quantitative method for inferring locomotory shifts in amniotes during ontogeny, its application to dinosaurs and its bearing on the evolution of posture

et al. 2019

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Evolutionary transitions between quadrupedal and bipedal postures are pivotal to the diversification of amniotes on land, including in our own lineage (Hominini). Heterochrony is suggested as a macroevolutionary mechanism for postural transitions but understanding postural evolution in deep time is hindered by a lack of methods for inferring posture in extinct species. Dinosaurs are an excellent natural laboratory for understanding postural transitions because they demonstrate at least four instances of quadrupedality evolving from bipedality, and heterochronic processes have been put forward as an explanatory model for these transitions. We extend a quantitative method for reliably inferring posture in tetrapods to the study of ontogenetic postural transitions using measurements of proportional limb robusticity. We apply this to ontogenetic series of living and extinct amniotes, focusing on dinosaurs. Our method correctly predicts the general pattern of ontogenetic conservation of quadrupedal and bipedal postures in many living amniote species and infers the same pattern in some dinosaurs. Furthermore, it correctly predicts the ontogenetic postural shift from quadrupedal crawling to bipedal walking in humans. We also infer a transition from early ontogenetic quadrupedality to late‐ontogenetic bipedality in the transitional sauropodomorph dinosaur Mussaurus patagonicus and possibly in the early branching ceratopsian Psittacosaurus lujiatunensis but not in the sauropodomorph Massospondylus carinatus. The phylogenetic positions of these ontogenetic shifts suggest that heterochrony may play a role in the macroevolution of posture, at least in dinosaurs. Our method has substantial potential for testing evolutionary transitions between locomotor modes, especially in elucidating the role of evolutionary mechanisms like heterochrony.

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“…), and a recent study has hypothesized a shift from quadrupedalism to bipedalism during ontogeny based on change in the body plan and its centre of mass (Otero et al . ).…”

Section: Discussionmentioning

confidence: 97%

“…) and Mussaurus patagonicus (Otero et al . ). Dinosaur species with ontogenetic changes in posture might therefore be instructive in understanding how shifts occur in other lineages and represent an opportunity for testing process‐based models.…”

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A quantitative method for inferring locomotory shifts in amniotes during ontogeny, its application to dinosaurs and its bearing on the evolution of posture

et al. 2019

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“…Despite this, previous studies have also demonstrated that, depending on the research question, reconstruction of soft tissue volumes and (to a lesser extent) density assignment may result in large margins of uncertainty that can complicate biological inference (Allen et al 2009;Hutchinson et al 2011;Macaulay et al 2017). Sensitivity analysis of how different mass property estimates may affect downstream calculations and interpretations (e.g., Allen et al 2013;Bates et al 2016;Otero et al 2019) may therefore be warranted.…”

Section: Reconstructing Body Shape and Dimensionsmentioning

confidence: 99%

“…The intersection of dinosaur paleontology and biomechanics can be reciprocally illuminating; not only can biomechanics shed insight into how dinosaurs functioned as living animals (Alexander 1985(Alexander , 1989(Alexander , 2006aHenderson 2012), but dinosaurs have much to offer the field of biomechanics, too. As some of the most successful vertebrates in history, they included the largest terrestrial animals to ever exist, for both quadrupeds and bipeds (Colbert 1962;Hutchinson et al 2011;Campione and Evans 2012;Campione et al 2014;Bates et al 2016, Benson et al 2018; exhibited repeated evolutionary increases and decreases in body size (Sereno 1999;Carrano 2006;Turner et al 2007;Benson et al 2018) and transitions from bipedal to quadrupedal posture (Charig 1972;Carrano 2005;Barrett 2012, 2014;Maidment et al 2014c); and displayed substantial disparity in cranial and postcranial anatomy with attendant functional differences (Rayfield 2005;Hutchinson and Allen 2009;Maidment et al 2014b;Button and Zanno 2020); one lineage evolved an additional mode of locomotion, powered flight (Ostrom 1976;Gauthier and Padian 1985;Gatesy 2002;Gauthier and Gall 2002;Heers and Dial 2012); and an increasing array of taxa are suspected of having undergone substantial change in functional abilities during ontogeny (e.g., Heinrich et al 1993;Dilkes 2001;Currie 2003;Carr and Williamson 2004;Hutchinson et al 2011;Otero et al 2019). These aspects, combined with the...…”

Section: Introductionmentioning

confidence: 99%

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

Bishop

Cuff

Hutchinson³

2020

Paleobiology

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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.

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“…These include: ( i ) the volumetric‐density (VD) approach, which incorporates the greatest amount of information about a skeleton; and ( ii ) the extant‐scaling (ES) approach, which integrates empirical knowledge of the relationship between bone dimensions and body mass in extant analogues. Within the last two decades, VD and ES approaches have been extensively applied to investigate a suite of biological properties in non‐avian dinosaurs, including metabolism (Seebacher, 2003; Gillooly et al ., 2006; Pontzer et al ., 2009; Grady et al ., 2014), growth patterns and rates (Erickson et al ., 2001; Hutchinson et al ., 2011; Myhrvold, 2013; Otero et al ., 2019), locomotion (Alexander, 1985; Christiansen, 1997; Hutchinson et al ., 2011; Sellers et al ., 2013), estimation and implications of the centre of mass (Henderson, 1999, 2006; Allen et al ., 2013; Maidment, Henderson & Barrett, 2014), aquatic abilities (Henderson, 2004, 2014, 2018), defence capabilities (Mallison, 2011 a ), relative sizes of muscles/organs (Gunga et al ., 1995; Franz et al ., 2009), macroevolutionary dynamics (Allen et al ., 2013; Dececchi & Larsson, 2013; Benson et al ., 2014, 2018), and both palaeoecology and taphonomy (O'Gorman & Hone, 2012; Codron et al ., 2012 b ; Brown et al ., 2013).…”

Section: Introductionmentioning

confidence: 99%

The accuracy and precision of body mass estimation in non‐avian dinosaurs

Campione

Evans

2020

Biological Reviews

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Inferring the body mass of fossil taxa, such as non‐avian dinosaurs, provides a powerful tool for interpreting physiological and ecological properties, as well as the ability to study these traits through deep time and within a macroevolutionary context. As a result, over the past 100 years a number of studies advanced methods for estimating mass in dinosaurs and other extinct taxa. These methods can be categorized into two major approaches: volumetric‐density (VD) and extant‐scaling (ES). The former receives the most attention in non‐avian dinosaurs and advanced appreciably over the last century: from initial physical scale models to three‐dimensional (3D) virtual techniques that utilize scanned data obtained from entire skeletons. The ES approach is most commonly applied to extinct members of crown clades but some equations are proposed and utilized in non‐avian dinosaurs. Because both approaches share a common goal, they are often viewed in opposition to one another. However, current palaeobiological research problems are often approach specific and, therefore, the decision to utilize a VD or ES approach is largely question dependent. In general, biomechanical and physiological studies benefit from the full‐body reconstruction provided through a VD approach, whereas large‐scale evolutionary and ecological studies require the extensive data sets afforded by an ES approach. This study summarizes both approaches to body mass estimation in stem‐group taxa, specifically non‐avian dinosaurs, and provides a comparative quantitative framework to reciprocally illuminate and corroborate VD and ES approaches. The results indicate that mass estimates are largely consistent between approaches: 73% of VD reconstructions occur within the expected 95% prediction intervals of the ES relationship. However, almost three quarters of outliers occur below the lower 95% prediction interval, indicating that VD mass estimates are, on average, lower than would be expected given their stylopodial circumferences. Inconsistencies (high residual and per cent prediction deviation values) are recovered to a varying degree among all major dinosaurian clades along with an overall tendency for larger deviations between approaches among small‐bodied taxa. Nonetheless, our results indicate a strong corroboration between recent iterations of the VD approach based on 3D specimen scans suggesting that our current understanding of size in dinosaurs, and hence its biological correlates, has improved over time. We advance that VD and ES approaches have fundamentally (metrically) different advantages and, hence, the comparative framework used and advocated here combines the accuracy afforded by ES with the precision provided by VD and permits the rapid identification of discrepancies with the potential to open new areas of discussion.

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Ontogenetic changes in the body plan of the sauropodomorph dinosaur Mussaurus patagonicus reveal shifts of locomotor stance during growth

Cited by 55 publications

References 44 publications

A quantitative method for inferring locomotory shifts in amniotes during ontogeny, its application to dinosaurs and its bearing on the evolution of posture

A quantitative method for inferring locomotory shifts in amniotes during ontogeny, its application to dinosaurs and its bearing on the evolution of posture

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

The accuracy and precision of body mass estimation in non‐avian dinosaurs

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