skip to main content


Title: Palatal Biomechanics and Its Significance for Cranial Kinesis in Tyrannosaurus rex
ABSTRACT

The extinct nonavian dinosaurTyrannosaurus rex, considered one of the hardest biting animals ever, is often hypothesized to have exhibited cranial kinesis, or, mobility of cranial joints relative to the braincase. Cranial kinesis inT.rexis a biomechanical paradox in that forcefully biting tetrapods usually possess rigid skulls instead of skulls with movable joints. We tested the biomechanical performance of a tyrannosaur skull using a series of static positions mimicking possible excursions of the palate to evaluate Postural Kinetic Competency inTyrannosaurus. A functional extant phylogenetic bracket was employed using taxa, which exhibit measurable palatal excursions:Psittacus erithacus(fore–aft movement) andGekko gecko(mediolateral movement). Static finite element models ofPsittacus,Gekko, andTyrannosauruswere constructed and tested with different palatal postures using anatomically informed material properties, loaded with muscle forces derived from dissection, phylogenetic bracketing, and a sensitivity analysis of muscle architecture and tested in orthal biting simulations using element strain as a proxy for model performance. Extant species models showed lower strains in naturally occurring postures compared to alternatives. We found that fore–aft and neutral models ofTyrannosaurusexperienced lower overall strains than mediolaterally shifted models. Protractor muscles dampened palatal strains, while occipital constraints increased strains about palatocranial joints compared to jaw joint constraints. These loading behaviors suggest that even small excursions can strain elements beyond structural failure. Thus, these postural tests of kinesis, along with the robusticity of other cranial features, suggest that the skull ofTyrannosauruswas functionally akinetic. Anat Rec, 303:999–1017, 2020. © 2019 Wiley Periodicals, Inc.

 
more » « less
Award ID(s):
1631684
NSF-PAR ID:
10457551
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
The Anatomical Record
Volume:
303
Issue:
4
ISSN:
1932-8486
Format(s):
Medium: X Size: p. 999-1017
Size(s):
["p. 999-1017"]
Sponsoring Org:
National Science Foundation
More Like this
  1. ABSTRACT 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 understanding the function and evolution of the skull in vertebrates. Here, we detail the use of ternary plots for displaying and comparing the 3D orientation of muscle data. First, we illustrate changes in 3D jaw muscle resultants during jaw closing taxa the American alligator (Alligator mississippiensis). Second, we show changes in 3D muscle resultants of jaw muscles across an ontogenetic series of alligators. Third, we compare 3D resultants of jaw muscles of avian-line dinosaurs, including extant (Struthio camelus, Gallus gallus, Psittacus erithacus) and extinct (Tyrannosaurus rex) species to outline the reorganization of jaw muscles that occurred along the line to modern birds. Finally, we compare 3D resultants of jaw muscles of the hard-biting species in our sample (A. mississippiensis, T. rex, P. erithacus) to illustrate how disparate jaw muscle resultants are employed in convergent behaviors in archosaurs. Our findings show that these visualizations of 3D components of jaw muscles are immensely helpful towards identifying patterns of cranial performance, growth and diversity. These tools will prove useful for testing other hypotheses in functional morphology, comparative biomechanics, ecomorphology and organismal evolution. 
    more » « less
  2. Abstract

    The evolution of avian cranial kinesis is a phenomenon in part responsible for the remarkable diversity of avian feeding adaptations observable today. Although osteological, developmental and behavioral features of the feeding system are frequently studied, comparatively little is known about cranial joint skeletal tissue composition and morphology from a microscopic perspective. These data are key to understanding the developmental, biomechanical and evolutionary underpinnings of kinesis. Therefore, here we investigated joint microstructure in juvenile and adult mallard ducks (Anas platyrhynchos; Anseriformes). Ducks belong to a diverse clade of galloanseriform birds, have derived adaptations for herbivory and kinesis, and are model organisms in developmental biology. Thus, new insights into their cranial functional morphology will refine our understanding of avian cranial evolution. A total of five specimens (two ducklings and three adults) were histologically sampled, and two additional specimens (a duckling and an adult) were subjected to micro‐computed tomographic scanning. Five intracranial joints were sampled: the jaw joint (quadrate‐articular); otic joint (quadrate‐squamosal); palatobasal joint (parasphenoid‐pterygoid); the mandibular symphysis (dentary‐dentary); and the craniofacial hinge (a complex flexion zone involving four different pairs of skeletal elements). In both the ducklings and adults, the jaw, otic and palatobasal joints are all synovial, with a synovial cavity and articular cartilage on each surface (i.e. bichondral joints) ensheathed in a fibrous capsule. The craniofacial hinge begins as an ensemble of patent sutures in the duckling, but in the adult it becomes more complex: laterally it is synovial; whereas medially, it is synostosed by a bridge of chondroid bone. We hypothesize that it is chondroid bone that provides some of the flexible properties of this joint. The heavily innervated mandibular symphysis is already fused in the ducklings and remains as such in the adult. The results of this study will serve as reference for documenting avian cranial kinesis from a microanatomical perspective. The formation of: (i) secondary articular cartilage on the membrane bones of extant birds; and (ii) their unique ability to form movable synovial joints within two or more membrane bones (i.e. within their dermatocranium) might have played a role in the origin and evolution of modern avian cranial kinesis during dinosaur evolution.

     
    more » « less
  3. Abstract

    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.

     
    more » « less
  4. Abstract

    A snake‐like body plan and burrowing lifestyle characterize numerous vertebrate groups as a result of convergent evolution. One such group is the amphisbaenians, a clade of limbless, fossorial lizards that exhibit head‐first burrowing behavior. Correlated with this behavior, amphisbaenian skulls are more rigid and coossified than those of nonburrowing lizards. However, due to their lifestyle, there are many gaps in our understanding of amphisbaenian anatomy, including how their cranial osteology varies among individuals of the same species and what that reveals about constraints on the skull morphology of head‐first burrowing taxa. We investigated intraspecific variation in the cranial osteology of amphisbaenians using seven individuals of the trogonophidDiplometopon zarudnyi. Variation in both skull and individual skull element morphology was examined qualitatively and quantitatively through three‐dimensional (3D) models created from microcomputed tomography data. Qualitative examination revealed differences in the number and position of foramina, the interdigitation between the frontals and parietal, and the extent of coossification among the occipital complex, fused basioccipital and parabasisphenoid (“parabasisphenoid‐basioccipital complex”), and elements X. We performed 3D landmark‐based geometric morphometrics for the quantitative assessment, revealing shape differences in the skull, premaxilla, maxilla, frontal, and parietal. The observed intraspecific variation may be the result of different stages of ontogenetic development or biomechanical optimization for head‐first burrowing. For example, variation in the coossification of the occipital region suggests a potential ontogenetic coossification sequence. Examination of these areas of variation across other head‐first burrowing taxa will help determine if the variation is clade‐specific or part of a broader macroevolutionary pattern of head‐first burrowing.

     
    more » « less
  5. null (Ed.)
    Synopsis Fish perform many complex manipulation behaviors without hands or flexible muscular tongues, instead relying on more than 20 movable skeletal elements in their highly kinetic skulls. How fish use their skulls to accomplish these behaviors, however, remains unclear. Most previous mechanical models have represented the fish skull using one or more planar four-bar linkages, which have just a single degree of freedom (DoF). In contrast, truncated-cone hydrodynamic models have assumed up to five DoFs. In this study, we introduce and validate a 3D mechanical linkage model of a fish skull that incorporates the pectoral girdle and mandibular and hyoid arches. We validate this model using an in vivo motion dataset of suction feeding in channel catfish and then use this model to quantify the DoFs in the fish skull, to categorize the motion patterns of the cranial linkage during feeding, and to evaluate the association between these patterns and food motion. We find that the channel catfish skull functions as a 17-link, five-loop parallel mechanism. Despite having 19 potential DoFs, we find that seven DoFs are sufficient to describe most of the motion of the cranial linkage, consistent with the fish skull functioning as a multi-DoF, manipulation system. Channel catfish use this linkage to generate three different motion patterns (rostrocaudal wave, caudorostral wave, and compressive wave), each with its own associated food velocity profile. These results suggest that biomechanical manipulation systems must have a minimum number of DoFs to effectively control objects, whether in water or air. 
    more » « less