The biomechanical significance of the elongated rodent incisor root in the mandible during incision.

Rodents are characterised by a distinctive masticatory apparatus which includes a single pair of enlarged and continually growing incisors. This morphology, termed diprotodonty, has also independently evolved in a number of other mammals, including the aye-aye. This study examined the functional significance of the internal "root" of the elongated rodent-like incisor. The mandibles of four rodents and an aye-aye were modelled to exhibit incrementally shorter incisor roots. Finite element analysis was used to predict stress and strain patterns across the jaw to determine whether the length of the incisor root contributes to the resistance of mechanical forces encountered in the mandible during incision. It was found that von Mises stresses increase in the region of the mandible local to where the incisor is removed, but that the stress distribution across the wider mandible is only minimally affected. Thus, the long internal incisor appears to play a small role in resisting bending forces close to the incisor alveolus, and may act with the arch-like mandibular shape to strengthen the mandible in this region. However, the impact across the whole mandible is relatively limited, suggesting the highly elongate incisor in diprotodont mammals may be principally driven by other factors such as rapid incisor wear.

The multifactorial nature of beak and skull shape evolution in parrots and cockatoos (Psittaciformes).

BACKGROUND: The Psittaciformes (parrots and cockatoos) are characterised by their large beaks, and are renowned for their ability to produce high bite forces. These birds also possess a suite of modifications to their cranial architecture interpreted to be adaptations for feeding on mechanically resistant foods, yet the relationship between cranial morphology and diet has never been explicitly tested. Here, we provide a three-dimensional geometric morphometric analysis of the developmental and biomechanical factors that may be influencing the evolution of psittaciformes' distinctive cranial morphologies. RESULTS: Contrary to our own predictions, we find that dietary preferences for more- or less- mechanically resistant foods have very little influence on beak and skull shape, and that diet predicts only 2.4% of the shape variation in psittaciform beaks and skulls. Conversely, evolutionary allometry and integration together predict almost half the observed shape variation, with phylogeny remaining an important factor in shape identity throughout our analyses, particularly in separating cockatoos (Cacatuoidea) from the true parrots (Psittacoidea). CONCLUSIONS: Our results are similar to recent findings about the evolutionary trajectories of skull and beak shape in other avian families. We therefore propose that allometry and integration are important factors causing canalization of the avian head, and while diet clearly has an influence on beak shape between families, this may not be as important at driving evolvability within families as is commonly assumed.

Mechanical significance of morphological variation in diprotodont incisors.

All rodents possess a single pair of enlarged incisors that grow throughout life. This condition (diprotodonty) is characteristic of Rodentia, but is also found in other mammals such as lagomorphs, hyraxes, the aye-aye and common wombat. This study surveyed lower incisor morphology across extant diprotodonts to examine shape variation within and between rodents and other diprotodonts, and to determine if tooth shape varies in a manner predictable from mechanics. Six linear and area variables were recorded from microCT scans of the mandibles of 33 diprotodont mammals. The curvature of the rodent lower incisors, as measured by the proportion of a circle it occupies, was shown to vary between 20 and 45%, with non-Glires taxa falling outside this range. Relative lengths of the portions of the incisor within and external to the mandible were not significantly correlated when the overall size was taken into account. Cross-sectional geometry of the incisor was significantly correlated with the external length of the incisor. Overall, incisor morphology was shown to vary in a way predictable from ecology and mechanics, in order to resist bending. Among non-rodents, lagomorph incisors closely resemble those of rodents, and, relative to rodents, hyrax and wombat incisors are somewhat smaller but aye-aye incisors are much more extreme in morphology.

Functional tests of the competitive exclusion hypothesis for multituberculate extinction.

Multituberculate mammals thrived during the Mesozoic, but their diversity declined from the mid-late Paleocene onwards, becoming extinct in the late Eocene. The radiation of superficially similar, eutherian rodents has been linked to multituberculate extinction through competitive exclusion. However, characteristics providing rodents with a supposed competitive advantage are currently unknown and comparative functional tests between the two groups are lacking. Here, a multifaceted approach to craniomandibular biomechanics was taken to test the hypothesis that superior skull function made rodents more effective competitors. Digital models of the skulls of four extant rodents and the Upper Cretaceous multituberculate Kryptobaatar were constructed and used (i) in finite-element analysis to study feeding-induced stresses, (ii) to calculate metrics of bite force production and (iii) to determine mechanical resistances to bending and torsional forces. Rodents exhibit higher craniomandibular stresses and lower resistances to bending and torsion than the multituberculate, apparently refuting the competitive exclusion hypothesis. However, rodents optimize bite force production at the expense of higher skull stress and we argue that this is likely to have been more functionally and selectively important. Our results therefore provide the first functional lines of evidence for potential reasons behind the decline of multituberculates in the changing environments of the Paleogene.

Convergent evolution in the Euarchontoglires.

Convergence-the independent evolution of similar phenotypes in distantly related clades-is a widespread and much-studied phenomenon. An often-cited, but hitherto untested, case of morphological convergence is that between the aye-aye and squirrels. The aye-aye (Daubentonia madagascariensis) is a highly unusual lemuriform primate that has evolved a dentition similar to that of rodents: it possesses large, ever-growing incisors which it uses to strip the bark from trees in order to feed on wood-boring beetle larvae. Indeed, such is the similarity that some of the earliest classifications of the aye-aye placed it in the squirrel genus Sciurus Here, we aimed to test the degree of convergence between the skulls and lower jaws of squirrels and the aye-aye. Three-dimensional landmarks were recorded from the crania and mandibles of 46 taxa representing the majority of families in the Euarchontoglires. Results were plotted as phylomorphospaces and convergence measures were calculated. The convergence between squirrels and the aye-aye was shown to be statistically significant for both the cranium and mandible, although the mandibles seem to converge more closely in shape. The convergence may indicate strong functional drivers of morphology in these taxa, i.e. the use of the incisors to produce high bite forces during feeding. Overall, we have shown that this classic case of convergence stands up to quantitative analysis.

The shapes of bird beaks are highly controlled by nondietary factors.

Bird beaks are textbook examples of ecological adaptation to diet, but their shapes are also controlled by genetic and developmental histories. To test the effects of these factors on the avian craniofacial skeleton, we conducted morphometric analyses on raptors, a polyphyletic group at the base of the landbird radiation. Despite common perception, we find that the beak is not an independently targeted module for selection. Instead, the beak and skull are highly integrated structures strongly regulated by size, with axes of shape change linked to the actions of recently identified regulatory genes. Together, size and integration account for almost 80% of the shape variation seen between different species to the exclusion of morphological dietary adaptation. Instead, birds of prey use size as a mechanism to modify their feeding ecology. The extent to which shape variation is confined to a few major axes may provide an advantage in that it facilitates rapid morphological evolution via changes in body size, but may also make raptors especially vulnerable when selection pressures act against these axes. The phylogenetic position of raptors suggests that this constraint is prevalent in all landbirds and that breaking the developmental correspondence between beak and braincase may be the key novelty in classic passerine adaptive radiations.

The morphology of the mouse masticatory musculature.

The mouse has been the dominant model organism in studies on the development, genetics and evolution of the mammalian skull and associated soft-tissue for decades. There is the potential to take advantage of this well studied model and the range of mutant, knockin and knockout organisms with diverse craniofacial phenotypes to investigate the functional significance of variation and the role of mechanical forces on the development of the integrated craniofacial skeleton and musculature by using computational mechanical modelling methods (e.g. finite element and multibody dynamic modelling). Currently, there are no detailed published data of the mouse masticatory musculature available. Here, using a combination of micro-dissection and non-invasive segmentation of iodine-enhanced micro-computed tomography, we document the anatomy, architecture and proportions of the mouse masticatory muscles. We report on the superficial masseter (muscle, tendon and pars reflecta), deep masseter, zygomaticomandibularis (anterior, posterior, infraorbital and tendinous parts), temporalis (lateral and medial parts), external and internal pterygoid muscles. Additionally, we report a lateral expansion of the attachment of the temporalis onto the zygomatic arch, which may play a role in stabilising this bone during downwards loading. The data presented in this paper now provide a detailed reference for phenotypic comparison in mouse models and allow the mouse to be used as a model organism in biomechanical and functional modelling and simulation studies of the craniofacial skeleton and particularly the masticatory system.

The mechanical significance of morphological variation in the macaque mandibular symphysis during mastication.

Catarrhine symphyseal morphology displays considerable variation. Although this has been related to dentition, phylogeny, sexual dimorphism, and facial orientation, most emphasis has been given to the functional significance of the symphysis to mechanical loading during mastication. The current state of knowledge regarding the mechanical significance of the symphysis is based on a combination of in vivo experimental and comparative studies on Macaca fascicularis. These approaches have provided considerable insight into the stereotypical patterns of loading in the symphyseal region during chewing and hypotheses related to the associated symphyseal morphologies. Finite element analysis (FEA) was used to assess how in silico manipulation translates into the mechanical loading hypotheses previously proposed experimentally. In particular, this study tests the form-function relationship of the symphysis of an adult M. fascicularis mandible during lateral transverse bending and dorsoventral shear of the mandibular symphysis, and a series of modified hypothetical morphologies including absence/presence of tori and variation in the inclination and depth of the symphysis. FEA results of this study support previous findings that stresses associated with lateral transverse bending and dorsoventral shear of the mandibular symphysis can be minimized via an increased labio-lingual thickness in the superior transverse torus, an oblique symphyseal inclination, and/or an increased symphyseal depth. The finding that reduction of strains related to lateral transverse bending and dorsoventral shear can be achieved through a number of different morphologies contributes to our understanding of the influence of morphological and/or developmental constraints, such as dental development, on symphyseal form.

Combining geometric morphometrics and functional simulation: an emerging toolkit for virtual functional analyses.

The development of virtual methods for anatomical reconstruction and functional simulation of skeletal structures offers great promise in evolutionary and ontogenetic investigations of form-function relationships. Key developments reviewed here include geometric morphometric methods for the analysis and visualization of variations in form (size and shape), finite element methods for the prediction of mechanical performance of skeletal structures under load and multibody dynamics methods for the simulation and prediction of musculoskeletal function. These techniques are all used in studies of form and function in biology, but only recently have they been combined in novel ways to facilitate biomechanical modelling that takes account of variations in form, can statistically compare performance, and relate performance to form and its covariates. Here we provide several examples that illustrate how these approaches can be combined and we highlight areas that require further investigation and development before we can claim a mature theory and toolkit for a statistical biomechanical framework that unites these methods.

The mechanical function of the periodontal ligament in the macaque mandible: a validation and sensitivity study using finite element analysis.

Whilst the periodontal ligament (PDL) acts as an attachment tissue between bone and tooth, hypotheses regarding the role of the PDL as a hydrodynamic damping mechanism during intraoral food processing have highlighted its potential importance in finite element (FE) analysis. Although experimental and constitutive models have correlated the mechanical function of the PDL tissue with its anisotropic, heterogeneous, viscoelastic and non-linear elastic nature, in many FE simulations the PDL is either present or absent, and when present is variably modelled. In addition, the small space the PDL occupies and the inability to visualize the PDL tissue using µCT scans poses issues during FE model construction and so protocols for the PDL thickness also vary. In this paper we initially test and validate the sensitivity of an FE model of a macaque mandible to variations in the Young's modulus and the thickness of the PDL tissue. We then tested the validity of the FE models by carrying out experimental strain measurements on the same mandible in the laboratory using laser speckle interferometry. These strain measurements matched the FE predictions very closely, providing confidence that material properties and PDL thickness were suitably defined. The FE strain results across the mandible are generally insensitive to the absence and variably modelled PDL tissue. Differences are only found in the alveolar region adjacent to the socket of the loaded tooth. The results indicate that the effect of the PDL on strain distribution and/or absorption is restricted locally to the alveolar bone surrounding the teeth and does not affect other regions of the mandible.

Balancing the spatial demands of the developing dentition with the mechanical demands of the catarrhine mandibular symphysis.

The superior transverse torus of the catarrhine mandible has been shown to effectively reduce bending at the symphysis during unilateral postcanine biting. While the adult superior transverse torus contains trabecular bone, the juvenile one is almost entirely filled by developing permanent incisors until their eruption. This study uses finite elements analysis (FEA) to investigate whether the presence of developing incisors in the juvenile symphysis increases strains on the superior transverse torus. Two FE models of a juvenile Macaca fascicularis mandible were created: one included all the developing teeth; the second was modified to remove the incisor tooth crypts by filling them with trabecular bone. The models were loaded identically to simulate static physiological unilateral biting on dp(4) and strain magnitudes, patterns and distributions of the two FE models were compared. The FEA results show a notable increase in strain magnitudes by up to 40% when the developing incisors are present. The results indicate that, in order to maintain the same symphyseal strain magnitudes during chewing, the presence of the incisors in the symphysis necessitates a larger superior transverse torus in the juvenile than would be required if the superior transverse torus did not house the developing incisors. These results highlight the adaptational balance of the symphyseal morphology throughout ontogeny between biomechanics and the spatial demands of the developing dentition. Based on the findings we therefore propose that the spatial requirements of the developing incisors during ontogeny can act as a constraint on the functional adaptation and subsequent adult morphology observed in the catarrhine mandibular symphysis.

Tooth root and craniomandibular morphological integration in the common chimpanzee (Pan troglodytes): alternative developmental models for the determinants of root length.

BACKGROUND/AIMS: Root length is strongly related to tooth stability but demonstrates considerable intraspecific variation. Previous studies have demonstrated an intraspecific relationship between root length and facial length in diverse mammalian taxa. These findings are indicative of plasticity in root length but with no clear developmental mechanism. This study aims to further these findings by identifying patterns of covariance between postcanine tooth root length and the whole integrated craniofacial skeleton in order to allow more refined hypotheses of the underlying developmental mechanisms to be proposed. METHODS: 2D landmark coordinates were obtained from lateral radiographs of 27 adult Pan troglodytes skulls. The landmark configurations were divided into two blocks, one of craniofacial landmarks and another of landmarks related to mandibular tooth roots. Covariation of the two blocks was determined using partial least squares analysis. RESULTS: The correlation coefficient between the first pair of singular warps is 0.76, highly significant (p<0.02) and not sex related. Visualisation of this correlation shows a clear pattern of increasing root length variation along the tooth row with increasing facial height but not length. CONCLUSIONS: The findings support previous conclusions that tooth roots demonstrate plasticity during their development. A correlation between root length variation along the tooth row and facial height rather than length can be interpreted in the context of previous findings of maxillary and mandibular rotation and compensatory remodeling during development. It is therefore proposed that the observed root length plasticity is due to variation in the eruptive distance associated with compensatory jaw rotation during development.

The facial skeleton of the chimpanzee-human last common ancestor.

This review uses the current morphological evidence to evaluate the facial morphology of the hypothetical last common ancestor (LCA) of the chimpanzee/bonobo (panin) and human (hominin) lineages. Some of the problems involved in reconstructing ancestral morphologies so close to the formation of a lineage are discussed. These include the prevalence of homoplasy and poor phylogenetic resolution due to a lack of defining derived features. Consequently the list of hypothetical features expected in the face of the LCA is very limited beyond its hypothesized similarity to extant Pan. It is not possible to determine with any confidence whether the facial morphology of any of the current candidate LCA taxa (Ardipithecus kadabba, Ardipithecus ramidus, Orrorin tugenensis and Sahelanthropus tchadensis) is representative of the LCA, or a stem hominin, or a stem panin or, in some cases, a hominid predating the emergence of the hominin lineage. The major evolutionary trends in the hominin lineage subsequent to the LCA are discussed in relation to the dental arcade and dentition, subnasal morphology and the size, position and prognathism of the facial skeleton.

The ontogeny of sexual dimorphism in the facial skeleton of the African apes.

This paper aims to test the contribution of ontogenetic scaling to sexual dimorphism of the facial skeleton in the African apes. Specifically, it addresses whether males and females of each species share a common postnatal ontogenetic shape trajectory for the facial skeleton. Where trajectories are found to differ, it is tested whether male and female trajectories: 1) diverge early, or 2) diverge later after sharing a common trajectory earlier in the postnatal period. Where ontogenetic shape trajectories are found to be shared, it is also tested whether males and females are ontogenetically scaled. This study uses geometric morphometric analyses of 28 landmarks from the facial skeletons of 137 G. g. gorilla (62 adults; 75 juveniles), 95 P. paniscus (34 adults; 61 juveniles), and 115 P. t. troglodytes (58 adults; 57 juveniles). On average, males and females share a common ontogenetic shape trajectory until around the eruption of the second permanent molars. In addition, for the same period, males and females in each species share a common ontogenetic scaling trajectory. After this period, males and females diverge both from each other and from the common juvenile ontogenetic shape and scaling trajectories within each species. Thus, the male and female facial skeleton shows ontogenetic scaling until around the point of the eruption of the second molar (i.e., around puberty and the development of secondary sexual characteristics), but subsequent sexual dimorphism occurs via divergent trajectories and not via ontogenetic scaling.