A finite element analysis of masticatory stress hypotheses

Understanding how the skull transmits and dissipates forces during feeding provides insights into the selective pressures that may have driven the evolution of primate skull morphology. Traditionally, researchers have interpreted masticatory biomechanics in terms of simple global loading regimes applied to simple shapes (i.e., bending in sagittal and frontal planes, dorsoventral shear, and torsion of beams and cylinders). This study uses finite element analysis to examine the extent to which these geometric models provide accurate strain predictions in the face and evaluate whether simple global loading regimes predict strains that approximate the craniofacial deformation pattern observed during mastication. Loading regimes, including those simulating peak loads during molar chewing and those approximating the global loading regimes, were applied to a previously validated finite element model (FEM) of a macaque (Macaca fascicularis) skull, and the resulting strain patterns were compared. When simple global loading regimes are applied to the FEM, the resulting strains do not match those predicted by simple geometric models, suggesting that these models fail to generate accurate predictions of facial strain. Of the four loading regimes tested, bending in the frontal plane most closely approximates strain patterns in the circumorbital region and lateral face, apparently due to masseter muscle forces acting on the zygomatic arches. However, these results indicate that no single simple global loading regime satisfactorily accounts for the strain pattern found in the validated FEM. Instead, we propose that FE models replace simple cranial models when interpreting bone strain data and formulating hypotheses about craniofacial biomechanics.     

Assessment of the role of sutures in a lizard skull: a computer modelling study

Sutures form an integral part of the functioning skull, but their role has long been debated among vertebrate morphologists and palaeontologists. Furthermore, the relationship between typical skull sutures, and those involved in cranial kinesis, is poorly understood. In a series of computational modelling studies, complex loading conditions obtained through multibody dynamics analysis were imposed on a finite element model of the skull of Uromastyx hardwickii, an akinetic herbivorous lizard. A finite element analysis (FEA) of a skull with no sutures revealed higher patterns of strain in regions where cranial sutures are located in the skull. From these findings, FEAs were performed on skulls with sutures (individual and groups of sutures) to investigate their role and function more thoroughly. Our results showed that individual sutures relieved strain locally, but only at the expense of elevated strain in other regions of the skull. These findings provide an insight into the behaviour of sutures and show how they are adapted to work together to distribute strain around the skull. Premature fusion of one suture could therefore lead to increased abnormal loading on other regions of the skull causing irregular bone growth and deformities. This detailed investigation also revealed that the frontal-parietal suture of the Uromastyx skull played a substantial role in relieving strain compared with the other sutures. This raises questions about the original role of mesokinesis in squamate evolution.     

Muscle‐induced loading as an important source of variation in craniofacial skeletal shape

The shape of the craniofacial skeleton is constantly changing through ontogeny and reflects a balance between developmental patterning and mechanical‐load‐induced remodeling. Muscles are a major contributor to producing the mechanical environment that is crucial for “normal” skull development. Here, we use an F₅ hybrid population of Lake Malawi cichlids to characterize the strength and types of associations between craniofacial bones and muscles. We focus on four bones/bone complexes, with different developmental origins, alongside four muscles with distinct functions. We used micro‐computed tomography to extract 3D information on bones and muscles. 3D geometric morphometrics and volumetric measurements were used to characterize bone and muscle shape, respectively. Linear regressions were performed to test for associations between bone shape and muscle volume. We identified three types of associations between muscles and bones: weak, strong direct (i.e., muscles insert directly onto bone), and strong indirect (i.e., bone is influenced by muscles without a direct connection). In addition, we show that although the shape of some bones is relatively robust to muscle‐induced mechanical stimulus, others appear to be highly sensitive to muscular input. Our results imply that the roles for muscular input on skeletal shape extend beyond specific points of origin or insertion and hold significant potential to influence broader patterns of craniofacial geometry. Thus, changes in the loading environment, either as a normal course of ontogeny or if an organism is exposed to a novel environment, may have pronounced effects on skeletal shape via near and far‐ranging effects of muscular loading.     

Calvarial suture interdigitation in hadrosaurids (Ornithischia: Ornithopoda): Perspectives through ontogeny and evolution

Lambeosaurine hadrosaurids exhibited extreme modifications to the skull, where the premaxillae, nasals, and prefrontals were modified to form their iconic supracranial crests. This morphology contrasts with their sister group, Hadrosaurinae, which possessed the plesiomorphic arrangement of bones. Although studies have discussed differences between lambeosaurine and hadrosaurine skull morphology and ontogeny, there is little information detailing suture modifications through ontogeny and evolution. Suture morphology is of particular interest due to its correlation with the mechanical loading of the skull in extant vertebrates. We quantify and contrast the morphology of calvarial sutures in iguanodontians and ontogenetic series of Corythosaurus and Gryposaurus to test whether the evolution of lambeosaurine crests impacted the mechanical loading of the skull. We found that suture interdigitation (SI) increases through ontogeny in hadrosaurids, although this increase is more extreme in Corythosaurus than Gryposaurus, and overall suture complexity (i.e., overall shape) remained constant. Lambeosaurines also have higher SI than other iguanodontians, even in crestless juveniles, suggesting that increased sinuosity is unrelated to the structural support of the crest. Hadrosaurines and basal iguanodontians did not differ. Similarly, lambeosaurines have more complexly shaped sutures than hadrosaurines and basal iguanodontians, while the latter two groups do not differ. Taken together, these results suggest that lambeosaurine calvarial sutures are more interdigitated than other iguanodontians, and although suture sinuosity increased through ontogeny, the suture shape remained constant. These ontogenetic and evolutionary patterns suggest that increased suture complexity in lambeosaurines coincided with crest evolution, and corresponding modifications to their facial skeleton altered the distribution of stress while feeding.     

The effects of muscular dystrophy on craniofacial growth in mice: A study of heterochrony and ontogenetic allometry

Mechanical loading of muscles on bones at their sites of attachment can regulate skeletal morphology. The present study examined the effects of muscle degeneration on craniofacial growth, using two strains of muscular dystrophic mice, Mus musculus, differing in pathological severity. We collected radiographic and weight data longitudinally and digitized radiographs to obtain distances between anatomical landmarks in different functional regions of the skull. We then quantified heterochronic and allometric differences among genotypes and between sexes. Because growth is nonlinear with respect to time, we first used the Gompertz model to obtain heterochronic growth parameters, which were then tested with ANOVA. Ontogenetic allometric analyses examined the scaling relationships between various measurements with linear regressions. For most measurements the severely dystrophic mice are significantly smaller in final size than both the control and the mildly dystrophic mice, which are statistically indistinguishable. Measures of total growth and the neurocranium exhibit more differences among groups in heterochronic parameters of early ontogeny because growth in these regions is controlled primarily by brain expansion that ceases early in development. In contrast, the face and mandible exhibit more differences in later growth parameters possibly because of the increased influence of muscles on these regions as growth progresses. The severely dystrophic mice have flatter, more elongate skulls and mandibles than those of the other two genotypes, concurrent with an absence of muscular forces to stimulate growth in a superior-inferior direction. J. Morphol. 235:1–16, 1998. © 1998 Wiley-Liss, Inc.     

Elastic properties of external cortical bone in the craniofacial skeleton of the rhesus monkey

Knowledge of elastic properties and of their variation in the cortical bone of the craniofacial skeleton is indispensable for creating accurate finite-element models to explore the biomechanics and adaptation of the skull in primates. In this study, we measured elastic properties of the external cortex of the rhesus monkey craniofacial skeleton, using an ultrasonic technique. Twenty-eight cylindrical cortical specimens were removed from each of six craniofacial skeletons of adult Macaca mulatta. Thickness, density, and a set of longitudinal and transverse ultrasonic velocities were measured on each specimen to allow calculation of the elastic properties in three dimensions, according to equations derived from Newton's second law and Hooke's law. The axes of maximum stiffness were determined by fitting longitudinal velocities measured along the perimeter of each cortical specimen to a sinusoidal function. Results showed significant differences in elastic properties between different functional areas of the rhesus cranium, and that many sites have a consistent orientation of maximum stiffness among specimens. Overall, the cortical bones of the rhesus monkey skull can be modeled as orthotropic in many regions, and as transversely isotropic in some regions, e.g., the supraorbital region. There are differences from human crania, suggesting that structural differences in skeletal form relate to differences in cortical material properties across species. These differences also suggest that we require more comparative data on elastic properties in primate craniofacial skeletons to explore effectively the functional significance of these differences, especially when these differences are elucidated through modeling approaches, such as finite-element modeling.     

Ontogenetic scaling of the human nose in a longitudinal sample: Implications for genus Homo facial evolution

Researchers have hypothesized that nasal morphology, both in archaic Homo and in recent humans, is influenced by body mass and associated oxygen consumption demands required for tissue maintenance. Similarly, recent studies of the adult human nasal region have documented key differences in nasal form between males and females that are potentially linked to sexual dimorphism in body size, composition, and energetics. To better understand this potential developmental and functional dynamic, we first assessed sexual dimorphism in the nasal cavity in recent humans to determine when during ontogeny male‐female differences in nasal cavity size appear. Next, we assessed whether there are significant differences in nasal/body size scaling relationships in males and females during ontogeny. Using a mixed longitudinal sample we collected cephalometric and anthropometric measurements from n = 20 males and n = 18 females from 3.0 to 20.0+ years of age totaling n = 290 observations. We found that males and females exhibit similar nasal size values early in ontogeny and that sexual dimorphism in nasal size appears during adolescence. Moreover, when scaled to body size, males exhibit greater positive allometry in nasal size compared to females. This differs from patterns of sexual dimorphism in overall facial size, which are already present in our earliest age groups. Sexually dimorphic differences in nasal development and scaling mirror patterns of ontogenetic variation in variables associated with oxygen consumption and tissue maintenance. This underscores the importance of considering broader systemic factors in craniofacial development and may have important implications for the study of patters craniofacial evolution in the genus Homo. Am J Phys Anthropol 153:52–60, 2014. © 2013 Wiley Periodicals, Inc.     

Functional relationship between skull form and feeding mechanics in Sphenodon, and implications for diapsid skull development

The vertebrate skull evolved to protect the brain and sense organs, but with the appearance of jaws and associated forces there was a remarkable structural diversification. This suggests that the evolution of skull form may be linked to these forces, but an important area of debate is whether bone in the skull is minimised with respect to these forces, or whether skulls are mechanically "over-designed" and constrained by phylogeny and development. Mechanical analysis of diapsid reptile skulls could shed light on this longstanding debate. Compared to those of mammals, the skulls of many extant and extinct diapsids comprise an open framework of fenestrae (window-like openings) separated by bony struts (e.g., lizards, tuatara, dinosaurs and crocodiles), a cranial form thought to be strongly linked to feeding forces. We investigated this link by utilising the powerful engineering approach of multibody dynamics analysis to predict the physiological forces acting on the skull of the diapsid reptile Sphenodon. We then ran a series of structural finite element analyses to assess the correlation between bone strain and skull form. With comprehensive loading we found that the distribution of peak von Mises strains was particularly uniform throughout the skull, although specific regions were dominated by tensile strains while others were dominated by compressive strains. Our analyses suggest that the frame-like skulls of diapsid reptiles are probably optimally formed (mechanically ideal: sufficient strength with the minimal amount of bone) with respect to functional forces; they are efficient in terms of having minimal bone volume, minimal weight, and also minimal energy demands in maintenance.     

Do precocial mammals develop at a faster rate? A comparison of rates of skull development in Sigmodon fulviventer and Mus musculus domesticus

Variation in neonatal maturity among mammals is often explained by variation in gestation length, but species may also differ in developmental rate, a quantity that is difficult to measure because the conventional formalism makes two important and potentially unrealistic assumptions: (1) ontogeny of form can be described by a single line, and (2) species have the same ontogeny of form. We examine two species, one precocial (Sigmodon fulviventer), the other altricial (Mus musculus domesticus), and find that neither assumption is met. Therefore, we introduce an alternative metric, the rate of shape differentiation away from the average neonate. We find that S. fulviventer has a lower developmental rate than M. m. domesticus; consequently, while more mature at birth, S. fulviventer loses ground to M. m. domesticus over time. Surprisingly, despite differences in gestation length and developmental rate, these species reach developmental and life-history milestones at nearly identical degrees of skull shape maturity.     

Early Lens Ablation Causes Dramatic Long-Term Effects on the Shape of Bones in the Craniofacial Skeleton of Astyanax mexicanus

The Mexican tetra, Astyanax mexicanus, exists as two morphs of a single species, a sighted surface morph and a blind cavefish. In addition to eye regression, cavefish have an increased number of taste buds, maxillary teeth and have an altered craniofacial skeleton compared to the sighted morph. We investigated the effect the lens has on the development of the surrounding skeleton, by ablating the lens at different time points during ontogeny. This unique long-term study sheds light on how early embryonic manipulations on the eye can affect the shape of the adult skull more than a year later, and the developmental window during which time these effects occur. The effects of lens ablation were analyzed by whole-mount bone staining, immunohistochemisty and landmark based morphometric analyzes. Our results indicate that lens ablation has the greatest impact on the skeleton when it is ablated at one day post fertilisation (dpf) compared to at four dpf. Morphometric analyzes indicate that there is a statistically significant difference in the shape of the supraorbital bone and suborbital bones four through six. These bones expand into the eye orbit exhibiting plasticity in their shape. Interestingly, the number of caudal teeth on the lower jaw is also affected by lens ablation. In contrast, the shape of the calvariae, the length of the mandible, and the number of mandibular taste buds are unaltered by lens removal. We demonstrate the plasticity of some craniofacial elements and the stability of others in the skull. Furthermore, this study highlights interactions present between sensory systems during early development and sheds light on the cavefish phenotype.     

Of "mice" and mammals: utilizing classical inbred mice to study the genetic architecture of function and performance in mammals

The house mouse is one of the most successful mammals and the premier research animal in mammalian biology. The classical inbred strains of house mice have been artificially modified to facilitate identification of the genetic factors underlying phenotypic variation among these strains. Despite their widespread use in basic and biomedical research, functional and evolutionary morphologists have not taken full advantage of inbred mice as a model for studying the genetic architecture of form, function, and performance in mammals. We illustrate the potential of inbred mice as a model for mammalian functional morphology by examining the genetic architecture of maximum jaw-opening performance, or maximum gape, across 21 classical inbred strains. We find that variation in maximum gape among these strains is heritable, providing the first evidence of a genetic contribution to maximum jaw-opening performance in mammals. Maximum gape exhibits a significant genetic correlation with body size across strains, raising the possibility that evolutionary increases in size frequently resulted in correlated increases in maximum gape (within the constraints of existing craniofacial form) during mammalian evolution. Several craniofacial features that influence maximum gape share significant phenotypic and genetic correlations with jaw-opening ability across these inbred strains. The significant genetic correlations indicate the potential for coordinated evolution of craniofacial form and jaw-opening performance, as hypothesized in several comparative analyses of mammals linking skull form to variation in jaw-opening ability. Functional studies of mammalian locomotion and feeding have only rarely examined the genetic basis of functional and performance traits. The classical inbred strains of house mice offer a powerful tool for exploring this genetic architecture and furthering our understanding of how form, function, and performance have evolved in mammals.     

Finite element scaling analysis of human craniofacial growth

The study of form change is central to traditional cephalometric research. Unfortunately, traditional cephalometric studies operate within systems of measurement that are based on registration and orientation. Measurements produced in registered systems are insufficient for the craniofacial biologist who is interested in locating morphological differences between forms. In this article we apply a registration-free method called finite element scaling analysis in a study of the form change occurring during growth of the normal human craniofacial complex. The method provides form change data that can be summarized at various morphological levels. Twenty normal male individuals are used to analyze the form change that occurs from age 4 to ages 5, 7, 8, 9, 10, 12, 13, and 15 years. The magnitude and direction of growth expressed as shape and size change specific to craniofacial landmarks are presented. Although exceptions occur, our analysis shows that localized size change is, on the average, greater than localized shape change. The relation between size and shape change during growth shows allometry (shape change increasing during growth along with size change) but at a lesser magnitude and slower rate. We conclude that although shape change occurs throughout ontogeny, the magnitude and rate of shape change in relation to size change diminishes as age increases. This analysis represents new insights into the understanding of human craniofacial growth at various levels of morphological integration.     

The embryonic origins of avian cephalic and cervical muscles and associated connective tissues

The objective of these experiments was to determine the embryonic origins of craniofacial and cervical voluntary muscles and associated connective tissues in the chick. To accomplish this, suspected primordia, including somitomeres 3-7, somites 1-7, and cephalic neural crest primordia have been transplanted from quail into chick embryos. Quail cells can be detected by the presence of a species-specific nuclear marker. The results are summarized as follows: (table; see text) These results indicate that muscles associated with branchial arch skeletal structures are derived from paraxial mesoderm, as are all other voluntary muscles in the vertebrate embryo. Thus, theories of vertebrate ontogeny and phylogeny based in part on proposed unique features of branchiomeric muscles must be critically reappraised. In addition, many of these cephalic muscles are composites of two separate primordia: the myogenic stem cells of mesodermal origin and the supporting and connective tissues derived from the neural crest or lateral plate mesoderm. Defining these embryonic origins is a necessary prerequisite to understanding how the mesenchymal primordia of cephalic muscles and connective tissues interact to form patterned, species-unique musculoskeletal systems.     

Skull ontogeny and modularity in two species of Lagenorhynchus: Morphological and ecological implications

Comparisons of skull shape between closely related species can provide information on the role that phylogeny and function play in cranial evolution. We used 3D‐anatomical landmarks in order to study the skull ontogeny of two closely related species, Lagenorhynchus obscurus and Lagenorhynchus australis , with a total sample of 52 skulls. We found shared trends between species, such as the relative compression of the neurocranium and the enlargement of the rostrum during ontogeny. However, these are common mammalian features, associated with prenatal brain development and sensory capsules. Moreover, we found a posterior displacement of the external nares and infraorbital foramina, and a strong development of the rostrum in an anteroposterior direction. Such trends are associated with the process of telescoping and have been observed in postnatal ontogeny of other odontocetes, suggesting a constraint in the pattern. Interspecific differences related to the deepness of facial region, robustness of the feeding apparatus and rostrum orientation may be related with the specific lifestyles of L. obscurus and L. australis . We also tested the presence of three different modules in the skull (basicranium, neurocranium, rostrum), all of which presented strong integration. Only the rostrum showed a different ontogenetic trajectory between species. Even though we detected directional asymmetry, changes in this feature along ontogeny were not detectable. Because asymmetry may be related to echolocation, our results suggest a functional importance of directional asymmetry from the beginning of postnatal life. J. Morphol. 278:203–214, 2017. © 2016 Wiley Periodicals,Inc.     

The importance of craniofacial sutures in biomechanical finite element models of the domestic pig

Craniofacial sutures are a ubiquitous feature of the vertebrate skull. Previous experimental work has shown that bone strain magnitudes and orientations often vary when moving from one bone to another, across a craniofacial suture. This has led to the hypothesis that craniofacial sutures act to modify the strain environment of the skull, possibly as a mode of dissipating high stresses generated during feeding or impact. This study tests the hypothesis that the introduction of craniofacial sutures into finite element (FE) models of a modern domestic pig skull would improve model accuracy compared to a model without sutures. This allowed the mechanical effects of sutures to be assessed in isolation from other confounding variables. These models were also validated against strain gauge data collected from the same specimen ex vivo. The experimental strain data showed notable strain differences between adjacent bones, but this effect was generally not observed in either model. It was found that the inclusion of sutures in finite element models affected strain magnitudes, ratios, orientations and contour patterns, yet contrary to expectations, this did not improve the fit of the model to the experimental data, but resulted in a model that was less accurate. It is demonstrated that the presence or absence of sutures alone is not responsible for the inaccuracies in model strain, and is suggested that variations in local bone material properties, which were not accounted for by the FE models, could instead be responsible for the pattern of results.     

Evolution of a complex phenotype with biphasic ontogeny: Contribution of development versus function and climatic variation to skull modularity in toads

The theory of morphological integration and modularity predicts that if functional correlations among traits are relevant to mean population fitness, the genetic basis of development will be molded by stabilizing selection to match functional patterns. Yet, how much functional interactions actually shape the fitness landscape is still an open question. We used the anuran skull as a model of a complex phenotype for which we can separate developmental and functional modularity. We hypothesized that functional modularity associated to functional demands of the adult skull would overcome developmental modularity associated to bone origin at the larval phase because metamorphosis would erase the developmental signal. We tested this hypothesis in toad species of the Rhinella granulosa complex using species phenotypic correlation pattern (P‐matrices). Given that the toad species are distributed in very distinct habitats and the skull has important functions related to climatic conditions, we also hypothesized that differences in skull trait covariance pattern are associated to differences in climatic variables among species. Functional and hormonal‐regulated modules are more conspicuous than developmental modules only when size variation is retained on species P‐matrices. Without size variation, there is a clear modularity signal of developmental units, but most species have the functional model as the best supported by empirical data without allometric size variation. Closely related toad species have more similar climatic niches and P‐matrices than distantly related species, suggesting phylogenetic niche conservatism. We infer that the modularity signal due to embryonic origin of bones, which happens early in ontogeny, is blurred by the process of growth that occurs later in ontogeny. We suggest that the species differing in the preferred modularity model have different demands on the orbital functional unit and that species contrasting in climate are subjected to divergent patterns of natural selection associated to neurocranial allometry and T3 hormone regulation.     

Cranial growth in normal and low-protein-fed Saimiri. An environmental heterochrony

Protein malnutrition has a significant and measurable effect on the rate and timing of growth. Heterochrony is generally viewed as the study of evolutionary changes in the relative rates and timing of growth and development. Although changes in growth commonly result from experimental manipulations of diet, nobody has previously attempted to explain such changes from a heterochronic perspective. We use a heterochronic perspective to compare a group of squirrel monkeys fed a low-protein diet to individuals on a high-protein diet, but, in contrast to previous works, we focus particularly on the effects of environmental and not genetic factors. In the present study, Gould's (1977) and Godfrey and Sutherland's (1996) methodologies for studying heterochrony, as well as geometric morphometrics, are used to compare two groups of Saimiri sciureus boliviensis. Two groups of Saimiri were constructed on the basis of the protein content in their diets: a high-protein group (HP) (N=12) and a low-protein group (LP) (N=12). All individuals are males born in captivity. Two major functional components of the skull, the neurocranium and the face, were analysed. Four minor components were studied in each major component. Comparison of craniofacial ontogeny patterns based on major and minor components suggests that changes in the skull of LP animals can be explained by heterochrony. The skull of LP animals exhibits isomorphism produced by proportioned dwarfism. Our results suggest that heterochrony can be environmentally, rather than exclusively genetically, induced. The study of genetic assimilation (Waddington, 1953, 1956; see Scharloo, 1991; Hallgrimsson et al., 2002) has demonstrated that environmentally induced phenotypes often have a genetic basis, and thus parallel changes can be easily induced genetically. It is possible that proportioned dwarfism is far more common than currently appreciated.     

Shape, variance and integration during craniogenesis: contrasting marsupial and placental mammals

Studies of morphological integration can provide insight into developmental patterns, even in extinct taxa known only from skeletal remains, thus making them an important tool for studies of evolutionary development. However, interpreting patterns of integration and assessing their significance for organismal evolution requires detailed understanding of the developmental interactions that shape integration and how those interactions change through ontogeny. Thus far, relatively little comparative data have been produced for this important topic, and the data that do exist are overwhelmingly from humans and their close relatives or from laboratory models such as mice. Here, we compare data on shape, variance and integration through postnatal ontogeny for a placental mammal, the least shrew, Cryptotis parva, and a marsupial mammal, the gray short-tailed opossum, Monodelphis domestica. Cranial variance decreased dramatically from early to late ontogeny in Cryptotis, but remained stable through ontogeny in Monodelphis, potentially reflecting functional constraints related to the short gestation and early ossification of oral bones in marsupials. Both Cryptotis and Monodelphis showed significant changes in cranial integration through ontogeny, with a mixture of increased, decreased and stable levels of integration in different cranial regions. Of particular note is that Monodelphis showed an unambiguous decrease in integration of the oral region through ontogeny, potentially relating to their early ossification. Selection at different stages of development may have markedly different effects if patterns of integration change substantially through ontogeny. Our results suggest that high integration of the oral region combined with functional constraints for suckling during early postnatal ontogeny may drive the stagnant variance observed in Monodelphis and potentially other marsupials.