Craig Byron

Bone architecture and disc degeneration in the lumbar spine of mice lacking GDF-8 (myostatin)

GDF‐8, also known as myostatin, is a member of the transforming growth factor‐β superfamily of secreted growth and differentiation factors that is expressed in vertebrate skeletal muscle. Myostatin functions as a negative regulator of skeletal muscle growth and myostatin null mice show a doubling of muscle mass compared to normal mice. We describe here morphology of the lumbar spine in myostatin knockout (Mstn‐/‐) mice using histological and densitometric techniques. The Mstn‐/‐ mice examined in this study weigh approximately 10% more than controls (p < 0.001) but the iliopsoas muscle is over 50% larger in the knockout mice than in wild‐type mice (p < 0.001). Peripheral quantitative computed tomography (pQCT) data from the fifth lumbar vertebra show that mice lacking myostatin have approximately 50% greater trabecular bone mineral density (p = 0.001) and significantly greater cortical bone mineral content than normal mice. Toluidine blue staining of the intervertebral disc between L4–L5 reveals loss of proteoglycan staining in the hyaline end plates and inner annulus fibrosus of the knockout mice. Loss of cartilage staining in the caudal end plate of L4 is due to ossification of the end plate in the myostatin‐deficient animals. Results from this study suggest that increased muscle mass in mice lacking myostatin is associated with increased bone mass as well as degenerative changes in the intervertebral disc.

The Structural Rigidity of the Cranium of Australopithecus africanus: Implications for Diet, Dietary Adaptations, and the Allometry of Feeding Biomechanics

Australopithecus africanus is an early hominin (i.e., human relative) believed to exhibit stress‐reducing adaptations in its craniofacial skeleton that may be related to the consumption of resistant food items using its premolar teeth. Finite element analyses simulating molar and premolar biting were used to test the hypothesis that the cranium of A. africanus is structurally more rigid than that of Macaca fascicularis, an Old World monkey that lacks derived australopith facial features. Previously generated finite element models of crania of these species were subjected to isometrically scaled loads, permitting a direct comparison of strain magnitudes. Moreover, strain energy (SE) in the models was compared after results were scaled to account for differences in bone volume and muscle forces. Results indicate that strains in certain skeletal regions below the orbits are higher in M. fascicularis than in A. africanus. Moreover, although premolar bites produce von Mises strains in the rostrum that are elevated relative to those produced by molar biting in both species, rostral strains are much higher in the macaque than in the australopith. These data suggest that at least the midface of A. africanus is more rigid than that of M. fascicularis. Comparisons of SE reveal that the A. africanus cranium is, overall, more rigid than that of M. fascicularis during premolar biting. This is consistent with the hypothesis that this hominin may have periodically consumed large, hard food items. However, the SE data suggest that the A. africanus cranium is marginally less rigid than that of the macaque during molar biting. It is hypothesized that the SE results are being influenced by the allometric scaling of cranial cortical bone thickness. Anat Rec, 293:583–593, 2010.

Viewpoints: Diet and Dietary Adaptations in Early Hominins: The Hard Food Perspective

Recent biomechanical analyses examining the feeding adaptations of early hominins have yielded results consistent with the hypothesis that hard foods exerted a selection pressure that influenced the evolution of australopith morphology. However, this hypothesis appears inconsistent with recent reconstructions of early hominin diet based on dental microwear and stable isotopes. Thus, it is likely that either the diets of some australopiths included a high proportion of foods these taxa were poorly adapted to consume (i.e., foods that they would not have processed efficiently), or that aspects of what we thought we knew about the functional morphology of teeth must be wrong. Evaluation of these possibilities requires a recognition that analyses based on microwear, isotopes, finite element modeling, and enamel chips and cracks each test different types of hypotheses and allow different types of inferences. Microwear and isotopic analyses are best suited to reconstructing broad dietary patterns, but are limited in their ability to falsify specific hypotheses about morphological adaptation. Conversely, finite element analysis is a tool for evaluating the mechanical basis of form-function relationships, but says little about the frequency with which specific behaviors were performed or the particular types of food that were consumed. Enamel chip and crack analyses are means of both reconstructing diet and examining biomechanics. We suggest that current evidence is consistent with the hypothesis that certain derived australopith traits are adaptations for consuming hard foods, but that australopiths had generalized diets that could include high proportions of foods that were both compliant and tough.

The Feeding Biomechanics and Dietary Ecology of Paranthropus boisei

The African Plio‐Pleistocene hominins known as australopiths evolved derived craniodental features frequently interpreted as adaptations for feeding on either hard, or compliant/tough foods. Among australopiths, Paranthropus boisei is the most robust form, exhibiting traits traditionally hypothesized to produce high bite forces efficiently and strengthen the face against feeding stresses. However, recent mechanical analyses imply that P. boisei may not have been an efficient producer of bite force and that robust morphology in primates is not necessarily strong. Here we use an engineering method, finite element analysis, to show that the facial skeleton of P. boisei is structurally strong, exhibits a strain pattern different from that in chimpanzees (Pan troglodytes) and Australopithecus africanus, and efficiently produces high bite force. It has been suggested that P. boisei consumed a diet of compliant/tough foods like grass blades and sedge pith. However, the blunt occlusal topography of this and other species suggests that australopiths are adapted to consume hard foods, perhaps including grass and sedge seeds. A consideration of evolutionary trends in morphology relating to feeding mechanics suggests that food processing behaviors in gracile australopiths evidently were disrupted by environmental change, perhaps contributing to the eventual evolution of Homo and Paranthropus. Anat Rec, 298:145–167, 2015.

The Global Impact of Sutures Assessed in a Finite Element Model of a Macaque Cranium

The biomechanical significance of cranial sutures in primates is an open question because their global impact is unclear, and their material properties are difficult to measure. In this study, eight suture‐bone functional units representing eight facial sutures were created in a finite element model of a monkey cranium. All the sutures were assumed to have identical isotropic linear elastic material behavior that varied in different modeling experiments, representing either fused or unfused sutures. The values of elastic moduli employed in these trials ranged over several orders of magnitude. Each model was evaluated under incisor, premolar, and molar biting conditions. Results demonstrate that skulls with unfused sutures permitted more deformations and experienced higher total strain energy. However, strain patterns remained relatively unaffected away from the suture sites, and bite reaction force was likewise barely affected. These findings suggest that suture elasticity does not substantially alter load paths through the macaque skull or its underlying rigid body kinematics. An implication is that, for the purposes of finite element analysis, omitting or fusing sutures is a reasonable modeling approximation for skulls with small suture volume fraction if the research objective is to observe general patterns of craniofacial biomechanics under static loading conditions. The manner in which suture morphology and ossification affect the mechanical integrity of skulls and their ontogeny and evolution awaits further investigation, and their viscoelastic properties call for dynamic simulations. Anat Rec 293:1477–1491, 2010.

Craniofacial Morphology in Myostatin-deficient Mice

GDF-8 (myostatin) is a negative growth regulator of skeletal muscle, and myostatin-deficient mice are hypermuscular. Muscle size and force production are thought to influence growth of the craniofacial skeleton. To test this relationship, we compared masticatory muscle size and craniofacial dimensions in myostatin-deficient and wild-type CD-1 control mice. Myostatin-deficient mice had significantly (p < 0.01) greater body (by 18%) and masseter muscle weight (by 83%), compared with wild-type controls. Significant differences (p < 0.05) were noted for cranial vault length, maxillary length, mandibular body length, and mandibular shape index. Significant correlations were noted between masseter muscle weight and mandibular body length (r = 0.68; p < 0.01), cranial vault length (r = −0.57; p < 0.05), and the mandibular shape index (r = −0.56; p < 0.05). Masticatory hypermuscularity resulted in significantly altered craniofacial morphology, probably through altered biomechanical stress. These findings emphasize the important role that masticatory muscle function plays in the ontogeny of the cranial vault, the maxilla, and, most notably, the mandible.

Unexpected locomotor behaviour: brachiation by an Old World monkey ( Pygathrix nemaeus ) from Vietnam

More than 70 h of positional behaviour data were collected on the red-shanked douc langur Pygathrix nemaeus, Delacour’s langur Trachypithecus delacouri, Hatinh langur Trachypithecus laotum, and the white-cheeked crested gibbon Hylobates leucogenys in January and February of 2001 at the Endangered Primate Rescue Center of Cuc Phuong National Park, Ninh Binh Province, Vietnam. Equal amounts of instantaneous and continuous bout data were collected for each of the four species. All animals were housed in enclosures of 10 × 5 × 3.5 m with similar substrates, and lived in small, species-appropriate social groups. The positional behaviour of white-cheeked crested gibbons was as expected with > 80% of locomotor bouts and 60% of postures being suspensory in nature. The positional behaviour of the Delacour’s and Hatinh langurs was similar to that reported in the literature for other Asian colobines with > 90% of the locomotor bouts being quadrupedal walking, running, and bounding on tops of arboreal supports. Postures were dominated by sitting in and sitting out with forelimb suspension associated with < 10% of these behaviours. The positional behaviour of the red-shanked douc langur is intermediate in nature between the Delacour’s and Hatinh langur and the white-cheeked crested gibbon. Locomotion is nearly evenly divided between arm-swinging (46%) and quadrupedal walking and running bouts (54%). Forelimb suspensory postures were three times more frequent for the red-shanked douc langur than they were for the Delacour’s langur.

Rudimentary Pedal Grasping in Mice and Implications for Terminal Branch Arboreal Quadrupedalism

We use an outbred laboratory mouse strain (ICR/CD‐1, Charles River Laboratories, Inc.) to model a type of preprimate locomotion associated with rudimentary pedal grasping. Ten male mice were assigned to either control or climbing groups (n = 5 per group). Climbing mice lived within a specialized terrarium that included ∼7.5 m of thin branches (5 and 10 cm long) with a thickness of 3.3mm, arranged in a reticulated canopy. Food, water, and a nest site were placed among the branches. To discourage mice from palmigrade or digitigrade locomotion, the floor of the terrarium was flooded with a few centimeters of water. Climbing mice were placed in this setting upon weaning and reared for 3 months until they were mature in size. Litter, and age‐matched controls were also maintained for comparison with climbers. Climbing mice quickly acclimated to the requirements of the fine‐branch model using the foot and tail for grasping and balance. At maturity, climbing and control mice exhibited minor, but significant, morphological plasticity. For climbers, this includes a greater angle of the femoral neck, larger patellar groove index, relatively shorter talar neck length, and more circular talar head aspect ratio (P < 0.10). Climbers also exhibit increased curvature of the distal third metacarpal, decreased talar head angle, and relatively longer caudal vertebrae transverse processes (P < 0.05). These results in a small‐bodied eutherian mammal suggest that facultative hallucial opposability and coordinated tail use enable a kind of grasping active arboreal quadrupedality relevant to the latest stages of pre‐euarchontan evolution. In light of these data, we hypothesize that a unique advantage of mouse‐sized mammals is that they exhibit a highly flexible body plan allowing them to engage in a diverse array of anatomical positions without requiring specific limb morphologies. J. Morphol.,2011.

The role of the sutures in biomechanical dynamic simulation of a macaque cranial finite element model: Implications for the evolution of craniofacial form

The global biomechanical impact of cranial sutures on the face and cranium during dynamic conditions is not well understood. It is hypothesized that sutures act as energy absorbers protecting skulls subjected to dynamic loads. This hypothesis predicts that sutures have a significant impact on global patterns of strain and cranial structural stiffness when analyzed using dynamic simulations; and that this global impact is influenced by suture material properties. In a finite element model developed from a juvenile Rhesus macaque cranium, five different sets of suture material properties for the zygomaticotemporal sutures were tested. The static and dynamic analyses produced similar results in terms of strain patterns and reaction forces, indicating that the zygomaticotemporal sutures have limited impact on global skull mechanics regardless of loading design. Contrary to the functional hypothesis tested in this study, the zygomaticotemporal sutures did not absorb significant amounts of energy during dynamic simulations regardless of loading speed. It is alternatively hypothesized that sutures are mechanically significant only insofar as they are weak points on the cranium that must be shielded from unduly high stresses so as not to disrupt vitally important growth processes. Thus, sutural and overall cranial form in some vertebrates may be optimized to minimize or otherwise modulate sutural stress and strain. Anat Rec, 2012.

Cranial suture morphology and its relationship to diet in Cebus.

Cranial sutures are complex morphological structures. Four Cebus species (C. albifrons, C. apella, C. capucinus, C. olivaceus) are used here to test the hypothesis that sagittal suture complexity is enhanced in animals that eat materially challenging foods. These primates are ideal for such comparative studies because they are closely related and some are known to exhibit differences in the material properties of the foods they ingest and masticate. Specifically, Cebus apella is notable among members of this genus for ingesting food items of high toughness as well as consistently demonstrating a relatively robust cranial morphology. Consistent with previous studies, C. apella demonstrates significantly more robust mandibular and temporal fossa morphology. Also, C. apella possesses sagittal sutures that are more complex than congenerics. These data are used to support the hypothesis that cranial suture complexity is increased in response to consuming diets with more obdurate material properties. One interpretation of this hypothesis is that, compared to non-apelloids, total strain in the apelloid cranial suture connective tissue environment is elevated due to increased jaw muscle activity by increases in either force magnitudes or the number of chewing events. It is argued that greater masticatory function enhances the growth and modeling of cranial suture interdigitation. These data show that cranial suture complexity is one more hard tissue feature from the skull that might be used to inform hypotheses of dietary functional morphology.