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Phylogenetic tree showing archosaurs used in case studies presented in this paper. Columns show skulls presented in this study in (L to R) left lateral, left oblique and ventral views.
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Comparing patterns of performance and kinematics across behavior, development and phylogeny is crucial to understand the evolution of complex musculoskeletal systems such as the feeding apparatus. However, conveying 3D spatial data of muscle orientation throughout a feeding cycle, ontogenetic pathway or phylogenetic lineage is essential to understa...
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... 1974;Dumont and Herrel, 2003) during a feeding bout. We demonstrate how ternary plots enable researchers to visualize the changes in orientations through one open-to-close phase of a feeding cycle in Alligator mississippiensis. Second, archosaurs have a wide diversity of cranial morphologies and feeding ecologies that change during ontogeny (see Fig. 1; Erickson et al., 2003;Yanega and Rubega, 2004;Grigg and Kirshner, 2015). Here, we show that ternary plots are able to track the trajectory of muscle orientation change through ontogeny in alligators. Third, comparisons across geological time reveal broad patterns among Archosauria including repeated evolution of large body size ...
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... temporal muscles are relatively weaker than mPTd and mAMP (see Figs 5 and 6), and these two muscles possess extensive rostrocaudal and dorsoventral components, respectively. The force of mPTd and mAMP together constitute approximately 35% of the total bite force produced by A. mississippiensis (Sellers et al., 2017). T. rex and P. erithacus also both exhibit very few mediolateral muscle components except in mPTd (Fig. 7B,E). ...
Citations
... adductor mandibulae externus group (see Holliday and Witmer, 2007;Holliday, 2009). This and our other inferences of muscle attachments are modelled after those of other theropod dinosaurs, which, in turn, were inferred based on phylogenetic bracketing of birds and crocodilians (Witmer, 1995;Holliday and Witmer, 2007;Holliday, 2009;Cost et al., 2022). The insertion of the m. ...
Although originally described almost three decades ago, the holotype of Irritator challengeri from the Lower Cretaceous Romualdo Formation of Brazil still represents the most complete spinosaurid skull known to science. Here, we present a detailed description of the skull of Irritator based on digital reconstructions from medical and micro computed tomography (μCT) data. Segmentation reveals the near-complete palatal complex and braincase, an unusual morphology of the retroarticular process, a large, ventrally inclined surangular shelf and the tooth replacement pattern. The digitally reconstructed skull anatomy indicates a robust dentition, a field of binocular vision in front of the skull with an inclined snout orientation, a relatively weak but fast bite, as well as laterally spreading and rotating lower jaw rami during jaw opening. We modified an existing phylogenetic matrix of Tetanurae to account for new observations on the morphology of Irritator and analysed this using parsimony and Bayesian methods. Results support Spinosauridae as members of Megalosauroidea and recover a monophyletic Carnosauria (Megalosauroidea + Allosauroidea). Parsimony analysis recovers Monolophosaurus nested within Megalosauroidea as sister taxon to spinosaurids, but this is not supported by the Bayesian analysis. Bayesian time-calibration and evolutionary rate analysis indicate that spinosaurid evolution happened fast, despite a long ghost lineage of at least 35 million years. High evolutionary rates over a prolonged time can explain the highly derived skull morphology of spinosaurids. This study provides an in-depth look into the evolution of spinosaurid skull anatomy and refines our understanding of these specialized Mesozoic predators.
... Here, we used simple and complex polyhedrons to estimate volumes of the jaw muscles in two different ways. Sellers used Strand7 (G1D Computing Pty Ltd, Sydney, Australia) to map surface areas of muscles reflecting their bony attachments (sensu Grosse et al., 2007;Davis et al., 2010;Sellers et al., 2017Cost et al., 2022;Sellers et al., 2022) and then the centroids and surface areas of the origins and insertions were used to calculate the volume of a frustum (Sellers et al., 2017), a relatively simply shape. Meanwhile, Lautenschlager employed their outline & fill (O&F) method, where, using Avizo (Thermo Fisher Scientific), the estimated boundaries of muscle attachments were marked and connected by a series of narrow cylinders (Lautenschlager 2013). ...
... These data enable further exploration into muscle mechanics by combining estimates of muscle attachments, muscle volumes and even muscle architecture (Figures 7, 8). We have previously shown that 3D muscle resultants can be accurately derived from 3D muscle attachment mapping and frustum-based volume estimates to estimate bite forces in Alligator mississippiensis (Sellers et al., 2017) and that these muscle resultants can be used to track changes in cranial performance among sauropsids (e.g., Cost et al., 2019;Wilken et al., 2019;Wilken et al., 2020;Cost et al., 2022) and during suchian evolution . ...
New imaging and biomechanical approaches have heralded a renaissance in our understanding of crocodylian anatomy. Here, we review a series of approaches in the preparation, imaging, and functional analysis of the jaw muscles of crocodylians. Iodine‐contrast microCT approaches are enabling new insights into the anatomy of muscles, nerves, and other soft tissues of embryonic as well as adult specimens of alligators. These imaging data and other muscle modeling methods offer increased accuracy of muscle sizes and attachments without destructive methods like dissection. 3D modeling approaches and imaging data together now enable us to see and reconstruct 3D muscle architecture which then allows us to estimate 3D muscle resultants, but also measurements of pennation in ways not seen before. These methods have already revealed new information on the ontogeny, diversity, and function of jaw muscles and the heads of alligators and other crocodylians. Such approaches will lead to enhanced and accurate analyses of form, function, and evolution of crocodylians, their fossil ancestors and vertebrates in general.
... Although the focus of this study was a comparison among taxa, smaller extant crocodylians had more dorsoventrally oriented muscles. This matches findings from an ontogenetic sample of A. mississippiensis (Cost et al., 2022). Heterochronic shifts are a common source of evolutionary shape change, and have been suggested to underlie other aspects of crocodylian skull shape and functional evolution ( ...
Jaw muscles are key features of the vertebrate feeding apparatus. The jaw musculature is housed in the skull whose morphology reflects a compromise between multiple functions, including feeding, housing sensory structures, and defense, and the skull constrains jaw muscle geometry. Thus, jaw muscle anatomy may be suboptimally oriented for the production of bite force. Crocodylians are a group of vertebrates that generate the highest bite forces ever measured with a flat skull suited to their aquatic ambush predatory style. However, basal members of the crocodylian line (e.g., Prestosuchus) were terrestrial predators with plesiomorphically tall skulls, and thus the origin of modern crocodylians involved a substantial reorganization of the feeding apparatus and its jaw muscles. Here, we reconstruct jaw muscles across a phylogenetic range of crocodylians and fossil suchians to investigate the impact of skull flattening on muscle anatomy. We used imaging data to create 3D models of extant and fossil suchians that demonstrate the evolution of the crocodylian skull, using osteological correlates to reconstruct muscle attachment sites. We found that jaw muscle anatomy in early fossil suchians reflected the ancestral archosaur condition but experienced progressive shifts in the lineage leading to Metasuchia. In early fossil suchians, musculus adductor mandibulae posterior and musculus pterygoideus (mPT) were of comparable size, but by Metasuchia, the jaw musculature is dominated by mPT. As predicted, we found that taxa with flatter skulls have less efficient muscle orientations for the production of high bite force. This study highlights the diversity and evolution of jaw muscles in one of the great transformations in vertebrate evolution.
Synopsis
High-resolution imaging, 3D modeling, and quantitative analyses are equipping evolutionary biologists with new approaches to understanding the variation and evolution of the musculoskeletal system. However, challenges with interpreting DiceCT data and higher order use of modeled muscles have not yet been fully explored, and the error in and accuracy of some digital methods remain unclear. West Indian Anolis lizards are a model clade for exploring patterns in functional adaptation, ecomorphology, and sexual size dimorphism in vertebrates. These lizards possess numerous jaw muscles with potentially different anatomies that sculpt the adductor chamber of the skull. Here we test approaches to quantifying the musculoskeletal shape of the heads of two species of Anolis: A. pulchellus and A. sagrei. We employ comparative approaches such as DiceCT segmentation of jaw muscles, 3D surface attachment mapping, and 3D landmarking with the aim of exploring muscle volumes, 3D muscle fiber architecture, and sexual dimorphism of the skull. We then compare sources of measurement error in these 3D analyses while also presenting new 3D musculoskeletal data from the Anolis feeding apparatus. These findings demonstrate the accessibility and repeatability of these emerging techniques as well as provide details regarding the musculoskeletal anatomy of the heads of A. pulchellus and A. sagrei which show potential for further research of comparative biomechanics and evolution in the clade.
The avian head is unique among living reptiles in its combination of relatively large brain and eyes, coupled with relatively small adductor jaw muscles. These derived proportions lend themselves to a trade‐off hypothesis, wherein adductor size was reduced over evolutionary time as a means (or as a consequence) of neurosensory expansion. In this study, we examine this evolutionary hypothesis through the lens of development by describing the jaw‐adductor anatomy of developing chickens, Gallus gallus, and comparing the volumetric expansion of these developing muscles with growth trajectories of the brain and eye. Under the trade‐off hypothesis, we predicted that the jaw muscles would grow with negative allometry relative to brain and eyes, and that osteological signatures of a relatively large adductor system, as found in most nonavian dinosaurs, would be differentially expressed in younger chicks. Results did not meet these expectations, at least not generally, with muscle growth exhibiting positive allometry relative to that of brain and eye. We propose three, nonmutually exclusive explanations: (1) these systems do not compete for space, (2) these systems competed for space in the evolutionary past, and growth of the jaw muscles was truncated early in development (paedomorphosis), and (3) trade‐offs in developmental investment in these systems are limited temporally to the perinatal period. These explanations are considered in light of the fossil record, and most notably the skull of the stem bird Ichthyornis, which exhibits an interesting combination of plesiomorphically large adductor chamber and apomorphically large brain.
In vertebrates, active movement is driven by muscle forces acting on bones, either directly or through tendinous insertions. There has been much debate over how muscle size and force are reflected by the muscular attachment areas (AAs). Here we investigate the relationship between the physiological cross-sectional area (PCSA), a proxy for the force production of the muscle, and the AA of hindlimb muscles in Nile crocodiles and five bird species. The limbs were held in a fixed position whilst blunt dissection was carried out to isolate the individual muscles. AAs were digitised using a point digitiser, before the muscle was removed from the bone. Muscles were then further dissected and fibre architecture was measured, and PCSA calculated. The raw measures, as well as the ratio of PCSA to AA, were studied and compared for intra-observer error as well as intra- and interspecies differences. We found large variations in the ratio between AAs and PCSA both within and across species, but muscle fascicle lengths are conserved within individual species, whether this was Nile crocodiles or tinamou. Whilst a discriminant analysis was able to separate crocodylian and avian muscle data, the ratios for AA to cross-sectional area for all species and most muscles can be represented by a single equation. The remaining muscles have specific equations to represent their scaling, but equations often have a relatively high success at predicting the ratio of muscle AA to PCSA. We then digitised the muscle AAs of Coelophysis bauri, a dinosaur, to estimate the PCSAs and therefore maximal isometric muscle forces. The results are somewhat consistent with other methods for estimating force production, and suggest that, at least for some archosaurian muscles, that it is possible to use muscle AA to estimate muscle sizes. This method is complementary to other methods such as digital volumetric modelling.
