Mammalian Skull Research Articles

Turtle shell and mammal skull resistance to fracture due to predator bites and ground impact

Turtle shell and mammal skull resistance to fracture due to predator bites and ground impact

Highly specialized mammalian skulls from the Late Cretaceous of South America

Dryolestoids are an extinct mammalian group belonging to the lineage leading to modern marsupials and placentals. Dryolestoids are known by teeth and jaws from the Jurassic period of North America and Europe, but they thrived in South America up to the end of the Mesozoic era and survived to the beginnings of the Cenozoic. Isolated teeth and jaws from the latest Cretaceous of South America provide mounting evidence that, at least in western Gondwana, dryolestoids developed into strongly endemic groups by the Late Cretaceous. However, the lack of pre-Late Cretaceous dryolestoid remains made study of their origin and early diversification intractable. Here we describe the first mammalian remains from the early Late Cretaceous of South America, including two partial skulls and jaws of a derived dryolestoid showing dental and cranial features unknown among any other group of Mesozoic mammals, such as single-rooted molars preceded by double-rooted premolars, combined with a very long muzzle, exceedingly long canines and evidence of highly specialized masticatory musculature. On one hand, the new mammal shares derived features of dryolestoids with forms from the Jurassic of Laurasia, whereas on the other hand, it is very specialized and highlights the endemic, diverse dryolestoid fauna from the Cretaceous of South America. Our specimens include only the second mammalian skull known for the Cretaceous of Gondwana, bridging a previous 60-million-year gap in the fossil record, and document the whole cranial morphology of a dryolestoid, revealing an unsuspected morphological and ecological diversity for non-tribosphenic mammals.

The conductivity of neonatal piglet skulls

We report the first measured values of conductivities for neonatal mammalian skull samples. We measured the average radial (normal to the skull surface) conductivity of fresh neonatal piglet skull samples at 1 kHz and found it to be around 30 mS m−1 at ambient room temperatures of about 23 °C. Measurements were made on samples of either frontal or parietal cranial bone, using a saline-filled cell technique. The conductivity value we observed was approximately twice the values reported for adult skulls (Oostendorp et al 2000 IEEE Trans. Biomed. Eng. 47 1487–92) using a similar technique, but at a frequency of around 5 Hz. Further, we found that the conductivity of skull fragments increased linearly with thickness. We found evidence that this was related to differences in composition between the frontal and parietal bone samples tested, which we believe is because frontal bones contained a larger fraction of higher conductivity cancellous bone material.

Ontogenetic relationships between cranium and mandible in coyotes and hyenas

Developing animals must resolve the conflicting demands of survival and growth, ensuring that they can function as infants or juveniles while developing toward their adult form. In the case of the mammalian skull, the cranium and mandible must maintain functional integrity to meet the feeding needs of a juvenile even as the relationship between parts must change to meet the demands imposed on adults. We examine growth and development of the cranium and mandible, using a unique ontogenetic series of known-age coyotes (Canis latrans), analyzing ontogenetic changes in the shapes of each part, and the relationship between them, relative to key life-history events. Both cranial and mandibular development conform to general mammalian patterns, but each also exhibits temporally and spatially localized maturational transformations, yielding a complex relationship between growth and development of each part as well as complex patterns of synchronous growth and asynchronous development between parts. One major difference between cranium and mandible is that the cranium changes dramatically in both size and shape over ontogeny, whereas the mandible undergoes only modest shape change. Cranium and mandible are synchronous in growth, reaching adult size at the same life-history stage; growth and development are synchronous for the cranium but not for the mandible. This synchrony of growth between cranium and mandible, and asynchrony of mandibular development, is also characteristic of a highly specialized carnivore, the spotted hyena (Crocuta crocuta), but coyotes have a much less protracted development, being handicapped relative to adults for a much shorter time. Morphological development does not predict life-history events in these two carnivores, which is contrary to what has been reported for two rodent species. The changes seen in skull shape in successive life-history stages suggest that adult functional demands cannot be satisfied by the morphology characterizing earlier life-history stages.

Occipital Ossification of Balaenopteroid Mysticetes

The bones of the posterior portion of the mammalian skull often exhibit incomplete ossification of the joints between the bones at the time of birth, with complete ossification at some point after birth. The sequence of ossification of these joints in mysticetes can be used to characterize the relative age in the calf and early juvenile ontogenetic stages. This study examined occipital joints ossification of 38 dry prepared neonate specimens in four mysticete species from two families (Eschrichtiidae: Eschrichtius robustus; Balaenopteridae: Balaenoptera acutorostrata, Balaenoptera physalus, and Megaptera novaeangliae). Each of the joints responsible for the fusion of the occiput were examined and rated for degree of ossification. The cranial ossification analysis indicates that E. robustus calves have open occipital joints until ~6 months of age and are born at a less mature stage than closely related balaenopterids. All of the species followed the same sequence of ossification: basioccipital/exoccipital joint, followed by the basioccipital/basisphenoid joint, and completed by the supraoccipital/exoccipital joint.

A new mammal skull from the Lower Cretaceous of China with implications for the evolution of obtuse-angled molars and ‘amphilestid’ eutriconodonts

We report the discovery of Juchilestes liaoningensis, a new genus and species of eutriconodont mammal from the Lujiatun Site of the Lower Cretaceous Yixian Formation (123.2 +/- 1.0 Ma; Lower Aptian). The holotype preserves a partial skull and full dentition. Among eutriconodonts, its lower dentition is similar to taxa formerly assigned to the paraphyletic group of 'amphilestids'. Some have considered 'amphilestid' molars to represent the structural intermediate between the lower molars of the 'triconodont' pattern of cusps in alignment and the fully triangulate and more derived therian molars. However, 'amphilestid' taxa were previously represented only by the lower dentition. Our study reveals, for the first time, the upper dentition and skull structure of an 'amphilestid', and shows that at least some eutriconodonts have an obtuse-angled cusp pattern on molars in middle positions of the long molar series. Its petrosal is similar to those of other eutriconodonts and spalacotheroid 'symmetrodonts'. Our phylogenetic analyses suggest that (i) Juchilestes is most closely related to the Early Cretaceous Hakusanodon from Japan, in the same Eastern Asiatic geographic region; (ii) 'amphilestids' are not monophyletic; and (iii) eutriconodonts might not be a monophyletic group, although this hypothesis must be further tested.

The Evolution of Modularity in the Mammalian Skull II: Evolutionary Consequences

Changes in patterns and magnitudes of integration may influence the ability of a species to respond to selection. Consequently, modularity has often been linked to the concept of evolvability, but their relationship has rarely been tested empirically. One possible explanation is the lack of analytical tools to compare patterns and magnitudes of integration among diverse groups that explicitly relate these aspects to the quantitative genetics framework. We apply such framework here using the multivariate response to selection equation to simulate the evolutionary behavior of several mammalian orders in terms of their flexibility, evolvability and constraints in the skull. We interpreted these simulation results in light of the integration patterns and magnitudes of the same mammalian groups, described in a companion paper. We found that larger magnitudes of integration were associated with a blur of the modules in the skull and to larger portions of the total variation explained by size variation, which in turn can exert a strong evolutionary constraint, thus decreasing the evolutionary flexibility. Conversely, lower overall magnitudes of integration were associated with distinct modules in the skull, to smaller fraction of the total variation associated with size and, consequently, to weaker constraints and more evolutionary flexibility. Flexibility and constraints are, therefore, two sides of the same coin and we found them to be quite variable among mammals. Neither the overall magnitude of morphological integration, the modularity itself, nor its consequences in terms of constraints and flexibility, were associated with absolute size of the organisms, but were strongly associated with the proportion of the total variation in skull morphology captured by size. Therefore, the history of the mammalian skull is marked by a trade-off between modularity and evolvability. Our data provide evidence that, despite the stasis in integration patterns, the plasticity in the magnitude of integration in the skull had important consequences in terms of evolutionary flexibility of the mammalian lineages.

Differential FGF Ligands and FGF Receptors Expression Pattern in Frontal and Parietal Calvarial Bones

The mammalian skull vault consists mainly of 5 flat bones, the paired frontals and parietals, and the unpaired interparietal. All of these bones are formed by intramembranous ossification within a layer of mesenchyme, the skeletogenic membrane, located between the dermal mesenchyme and the meninges surrounding the brain. While the frontal bones are of neural crest in origin, the parietal bones arise from mesoderm. The present study is a characterization of frontal and parietal bones at their molecular level, aiming to highlight distinct differences between the neural crest-derived frontal and mesodermal-derived parietal bone. We performed a detailed comparative gene expression profile of FGF ligands and their receptors known to play crucial role in skeletogenesis. This analysis revealed that a differential expression pattern of the major FGF osteogenic molecules and their receptors exists between the neural crest-derived frontal bone and the paraxial mesoderm-derived parietal bone. Particularly, the expression of ligands such as Fgf-2, Fgf-9 and Fgf-18 was upregulated in frontal bone on embryonic day 17.5, postnatal day 1 and postnatal day 60 mice. Frontal bone also elaborated higher levels of Fgf receptor 1, 2 and 3 transcripts versus parietal bone. Taken together, these data suggest that the frontal bone is a domain with higher FGF-signaling competence than parietal bone.

The Evolution of Modularity in the Mammalian Skull I: Morphological Integration Patterns and Magnitudes

Morphological integration refers to the modular structuring of inter-trait relationships in an organism, which could bias the direction and rate of morphological change, either constraining or facilitating evolution along certain dimensions of the morphospace. Therefore, the description of patterns and magnitudes of morphological integration and the analysis of their evolutionary consequences are central to understand the evolution of complex traits. Here we analyze morphological integration in the skull of several mammalian orders, addressing the following questions: are there common patterns of inter-trait relationships? Are these patterns compatible with hypotheses based on shared development and function? Do morphological integration patterns and magnitudes vary in the same way across groups? We digitized more than 3,500 specimens spanning 15 mammalian orders, estimated the correspondent pooled within-group correlation and variance/covariance matrices for 35 skull traits and compared those matrices among the orders. We also compared observed patterns of integration to theoretical expectations based on common development and function. Our results point to a largely shared pattern of inter-trait correlations, implying that mammalian skull diversity has been produced upon a common covariance structure that remained similar for at least 65 million years. Comparisons with a rodent genetic variance/covariance matrix suggest that this broad similarity extends also to the genetic factors underlying phenotypic variation. In contrast to the relative constancy of inter-trait correlation/covariance patterns, magnitudes varied markedly across groups. Several morphological modules hypothesized from shared development and function were detected in the mammalian taxa studied. Our data provide evidence that mammalian skull evolution can be viewed as a history of inter-module parcellation, with the modules themselves being more clearly marked in those lineages with lower overall magnitude of integration. The implication of these findings is that the main evolutionary trend in the mammalian skull was one of decreasing the constraints to evolution by promoting a more modular architecture.

On the phylogenetic relationships of Vincelestes neuquenianus

This short review paper compares the lower jaw and lower dentition of the small Mesozoic mammal Vincelestes neuquenianus with some other Laurasian and Gondwanan taxa. On this basis a set of 90 characters recognised by recent authors was assembled and used to construct a cladogram. The topology suggests that the early Cretaceous mammal from Patagonia, Vincelestes, is nested within a clade comprising ‘other Gondwanan mammals’, separated from Laurasian taxa. In general, because there is a lack of Mesozoic mammal skulls from Gondwana, meaning that the skull of Vincelestes can only be compared with cranial material from Laurasia, an incomplete understanding of relationships has resulted in earlier studies. The prototribosphenic condition of Vincelestes is supported by the cladistic analysis presented here and permits a number of interesting speculations because it is of later age than Jurassic tribosphenic mammals from Gondwana. It is proposed that the tribosphenic condition may have developed first amongst taxa on Pangea, before the separation of Laurasia and Gondwana.

Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: testing a new model using mice

The hypothesis that variation in craniofacial shape within and among species is influenced by spatial packing has a long history in comparative anatomy, particularly in terms of primates. This study develops and tests three alternative models of spatial packing to address how and to what extent the cranial base angle is influenced by variation in brain and facial size. The models are tested using mouse strains with different mutations affecting craniofacial growth. Although mice have distinctive crania with small brains, long faces, and retroflexed cranial bases, the results of the study indicate that the mouse cranial base flexes to accommodate larger brain size relative to cranial base length. In addition, the mouse cranial base also extends, but to a lesser degree, to accommodate larger face size relative to cranial base length. In addition, interactions between brain size, face size, and the widths and lengths of the components of the cranial base account for a large percentage of variation in cranial base angle. The results illustrate the degree to which the cranial base is centrally embedded within the covariation structure of the craniofacial complex as a whole.

TGF-β mediated Msx2 expression controls occipital somites-derived caudal region of skull development

Craniofacial development involves cranial neural crest (CNC) and mesoderm-derived cells. TGF-β signaling plays a critical role in instructing CNC cells to form the craniofacial skeleton. However, it is not known how TGF-β signaling regulates the fate of mesoderm-derived cells during craniofacial development. In this study, we show that occipital somites contribute to the caudal region of mammalian skull development. Conditional inactivation of Tgfbr2 in mesoderm-derived cells results in defects of the supraoccipital bone with meningoencephalocele and discontinuity of the neural arch of the C1 vertebra. At the cellular level, loss of TGF-β signaling causes decreased chondrocyte proliferation and premature differentiation of cartilage to bone. Expression of Msx2, a critical factor in the formation of the dorsoventral axis, is diminished in the Tgfbr2 mutant. Significantly, overexpression of Msx2 in Myf5-Cre;Tgfbr2 flox/flox mice partially rescues supraoccipital bone development. These results suggest that the TGF-β/Msx2 signaling cascade is critical for development of the caudal region of the skull.

On Chaliminia musteloides (Eucynodontia: Tritheledontidae) from the Late Triassic of Argentina, and a phylogeny of Ictidosauria

ABSTRACT A new specimen of Chaliminia musteloides Bonaparte is described from the upper section of the Los Colorados Formation (Late Carnian–Early Norian) of Argentina. A cladistic analysis of ictidosaurians supports its monophyly. Chaliminia and Elliotherium, grouped in the new subfamily Chalimininae, were placed as sister taxa to the new subfamily Pachygenelinae, which includes Pachygenelus, Diarthrognathus, and Tritheledon. Irajatherium is basal to both subfamilies as a stem Tritheledontidae. Riograndia represents the most basal non-tritheledontid ictidosaurian. The resulting tree topology agrees with the age of the fossil record of each ictidosaurian species. Although our analysis does not test the relationship of ictidosaurians with regard to Mammaliaformes, it is clear from our tree that ictidosaurians are closely related to them. Several derived characters seem to have been acquired convergently in both lineages and relate to food processing, development of primary chewing musculature and ancillary structures. In other aspects, ictidosaurians remained very conservative, or reverted to ancestral morphologies, such as the presence of interpterygoidal-vacuities. Analysis of the vacuities indicates that they represent an ancestral condition that facilitated the development of the mammalian skull base constituted by the reduced pterygoids, the basisphenoid, and posteriorly the development of the presphenoid by the ventral extension of the braincase. Possibly, the main factors in the remodeling of this area are the development of the sphenoid sinus and the forward and ventral expansion of the cranial cavity. The re-acquisition of interpterygoid vacuities among ictidosaurians could be the result of a paedomorphic (neotenic or progenetic) alteration of the developmental pattern.

Feeding mechanisms in bats: variation within the constraints of flight

By any standard, bats are a successful group of mammals and the evolution of flight and echolocation were certainly key innovations behind their success. That is only part of the story, however. Bats have diversified into trophic niches that range from insectivory to feeding on blood, fruit, or nectar. While flight places fundamental constraints on the shape of the postcranial skeleton, skull shape in bats is remarkably diverse. Morphological studies of individual families and sympatric assemblages demonstrate that variation in skull shape is clearly associated with trophic specialization. Field experiments demonstrate that species-specific biting behaviors during feeding are common and analyses indicate that the evolution of cranial morphology and feeding behavior are correlated. Modeling experiments further suggest that feeding (loading) behaviors and skull shape are functionally linked. If the skulls of bats are under selective pressure for minimal mass because of the energetic demands of flight, then they may be more "optimized" to meet mechanical demands than are the skulls of other mammals. This would make bats a unique model system for studying the evolution of diversity in skull shape and its functional implications for the evolution of feeding strategies in mammals.

Epigenetic interactions and the structure of phenotypic variation in the cranium

Understanding the developmental and genetic basis for evolutionarily significant morphological variation in complex phenotypes such as the mammalian skull is a challenge because of the sheer complexity of the factors involved. We hypothesize that even in this complex system, the expression of phenotypic variation is structured by the interaction of a few key developmental processes. To test this hypothesis, we created a highly variable sample of crania using four mouse mutants and their wild-type controls from similar genetic backgrounds with developmental perturbations to particular cranial regions. Using geometric morphometric methods we compared patterns of size, shape, and integration in the sample within and between the basicranium, neurocranium, and face. The results highlight regular and predictable patterns of covariation among regions of the skull that presumably reflect the epigenetic influences of the genetic perturbations in the sample. Covariation between relative widths of adjoining regions is the most dominant factor, but there are other significant axes of covariation such as the relationship between neurocranial size and basicranial flexion. Although there are other sources of variation related to developmental perturbations not analyzed in this study, the patterns of covariation created by the epigenetic interactions evident in this sample may underlie larger scale evolutionary patterns in mammalian craniofacial form.

Effects of developmental and functional interactions on mouse cranial variability through late ontogeny

The mammalian skull performs a variety of functions and its growth and development mirrors this complexity. Cranial growth and development have been actively studied for many years. Despite this interest, the variation in the patterns and processes of skull growth has attracted little attention. An important and unanswered question is the extent to which patterns of cranial covariation and variation are dynamically reworked throughout postnatal growth. To address this question, we examine patterns of variability in random-bred mouse skulls aged 35, 90, and 150 days. Using a battery of both Procrustes coordinate and Euclidean distance-based methods, we measure mean shape, canalization, developmental stability, and morphological integration in these skulls. We predict that the patterns of variability are dynamic, particularly between the youngest and the two oldest age groups due to the influence of functional effects such as postweaning mastication. We also hypothesize that patterns of variability are structured by the same functional and developmental factors that have been shown to influence cranial growth in primates. Our results indicate that contrary to our predictions, patterns of canalization, developmental stability, and morphological integration are stabilized before 35 days. The mean shape, however, changed significantly with growth. We found that only the facial region showed significant integration as predicted by the functional matrix model used in other studies of integration. These results indicate that phenotypic integration in these mice does not closely match those found for primate species, suggesting that comparisons between species should be made with care.

Cranial Modularity Shifts during Mammalian Evolution

The mammalian skull has been studied as several separate functional components for decades, but the study of modularity is a more recent, integrative approach toward quantitative examination of independent subsets of highly correlated traits, or modules. Although most studies of modularity focus on developmental and genetic systems, phenotypic modules have been noted in many diverse morphological structures. However, few studies have provided empirical data for comparing modules across higher taxonomic levels, limiting the ability to assess the broader evolutionary significance of modularity. This study uses 18-32 three-dimensional cranial landmarks to analyze phenotypic modularity in 106 mammalian species and demonstrates that cranial modularity is generally conserved in the evolution of therian mammals (marsupials and placentals) but differs between therians and monotremes, the two extant subclasses of Mammalia. Within therians, cluster analyses identify six distinct modules, but only three modules display significant integration in all species. Monotremes display only two highly integrated modules. Specific hypotheses of functional and developmental influences on cranial bones were tested. Theoretical correlation matrices for bones were constructed on the basis of shared function, tissue origin, or mode of ossification, and all three of these models are significantly correlated with observed correlation matrices for the mammalian cranium.

Character evolution in the orbital region of the Afrotheria

AbstractThe orbit or eye socket is a highly plastic area of the mammalian skull. There is significant variation within and between the different mammalian orders in the size and position of the bones and foramina that contribute to this region. For this reason, orbital characters are often used in attempts to determine the relationships of the various mammalian groups. This study describes the orbital region of the Afrotheria, the proposed group of endemic African mammals that comprises the paenungulates (elephants, manatees and dugongs, and hyraxes), elephant‐shrews, aardvarks, golden moles and tenrecs. Evolution within the Afrotherian orbit is then explored by scoring 19 orbital characters in each Afrotherian genus, and plotting the character state changes on to previously existing phylogenies of the Afrotheria. These phylogenies were all produced from recent molecular work. It was found that there is a great deal of variation in the orbital region within the Afrotheria, most notably in the size of the lacrimal and its contacts with other bones, the appearance of the palatine in the orbit and the structure of the zygomatic arch. Overall, orbital characters strongly supported an elephant‐hyrax clade over the more traditional grouping of elephants and sirenians (Tethytheria) within the paenungulates. There was also support for a monophyletic Tenrecoidea (a clade of tenrecs plus golden moles). Additionally, it was shown that there is a great deal of variation in the orbital region among the genera of the Tenrecidae and the Macroscelididae.

Phenotypic integration of neurocranium and brain

Evolutionary history of Mammalia provides strong evidence that the morphology of skull and brain change jointly in evolution. Formation and development of brain and skull co-occur and are dependent upon a series of morphogenetic and patterning processes driven by genes and their regulatory programs. Our current concept of skull and brain as separate tissues results in distinct analyses of these tissues by most researchers. In this study, we use 3D computed tomography and magnetic resonance images of pediatric individuals diagnosed with premature closure of cranial sutures (craniosynostosis) to investigate phenotypic relationships between the brain and skull. It has been demonstrated previously that the skull and brain acquire characteristic dysmorphologies in isolated craniosynostosis, but relatively little is known of the developmental interactions that produce these anomalies. Our comparative analysis of phenotypic integration of brain and skull in premature closure of the sagittal and the right coronal sutures demonstrates that brain and skull are strongly integrated and that the significant differences in patterns of association do not occur local to the prematurely closed suture. We posit that the current focus on the suture as the basis for this condition may identify a proximate, but not the ultimate cause for these conditions. Given that premature suture closure reduces the number of cranial bones, and that a persistent loss of skull bones is demonstrated over the approximately 150 million years of synapsid evolution, craniosynostosis may serve as an informative model for evolution of the mammalian skull.

Some rare species of mammals from Burma present in the Bombay Natural History Society collection

© Zoo Outreach Organisation; www.zoosprint.org Manuscript 1334; Received 21 February 2005; Revised received 26 November 2005; Finally accepted 10 December 2005; Date of publication 21 January 2006 2199 March 2006 | ISSN 0973-2535 (Print edition); 0973-2551 (Online edition) The BNHS had undertaken a systematic survey of the mammals of the Indian subcontinent from 1911 to 1923. Besides the Indian states the specimens were also collected from various parts of Burma (presently Myanmar) and Ceylon (Sri Lanka). The purpose of the survey was to secure a systematic series of wellpreserved skins and skulls of mammals for a comprehensive study of the status, variation and distribution of the species. The areas from Burma covered under the survey were N. Shan States, Dry Zone, Central Burma, Mt. Popa, S. Tenasserim, Chindwin River, Chin Hills, Pegu, Prome, Mergui Archipelago and Toungoo. The collection of squirrels obtained on both banks of the Chindwin river forms the most magnificent collection, providing striking evidence that the river Chindwin forms a sharp line of demarcation to the eastward and westward extension of the different species of squirrels. All these mammal specimens are kept in dry preservation in the collection of BNHS.