Philip G. Cox

The dormice are a family of small- to medium-sized rodents found across Europe, Asia and Africa. The current extant diversity is represented by 29 species across nine genera (Holden-Musser et al., ...

Leporid lagomorphs, the rabbits and hares, exhibit unique cranial traits that distinguish them from their closest relatives, the Ochotonidae (pikas), and all other mammals. Among these features, the intracranial joint stands out as the only example of cranial kinesis in mammals and is hypothesised to dissipate kinetic energy during high‐speed locomotion. Despite its potential functional importance, the morphology of the joint remains understudied. High complexity in other cranial sutures has been associated with behavioural traits such as feeding and head butting. In this study, we quantified the complexity of the intracranial joint using two independent metrics and explored its relationships with overall cranial shape, locomotor mode, cranial size and body mass, burrowing habit, and facial tilt angle. We found significant correlations between complexity and locomotor mode as well as with facial tilt angle, indicating that cursorial species have less complex sutures and highlighting a potential link between the complexity of suture interdigitation and facial tilting. However, complexity did not correlate with size or burrowing habit. Our findings shed more light on the functional anatomy of the leporid cranium and emphasise the need for further research on ontogenetic development, biomechanics, and behaviour to fully understand the evolutionary and functional significance of these unique cranial traits.

The mechanical properties of dietary items are known to influence skull morphology, either through evolution or by phenotypic plasticity. Here, we investigated the impact of supplementary feeding of peanuts on the morphology of red squirrels (Sciurus vulgaris) from five populations in Britain (North Scotland, Borders, Jersey and two temporally distinct populations from Formby (Merseyside)). Stable isotope analysis confirmed dietary ecology in 58 specimens. Geometric morphometrics were used to analyse three-dimensional and two-dimensional shape variation across 113 crania and 388 mandibles, respectively. Nitrogen isotope ratios (δ15N) were lower in the 1990s and 2010s Formby squirrels (suggesting a diet with an increased proportion of peanuts), and higher in other populations. Significant differences in cranio-mandibular shape were found between all populations, with 1990s Formby red squirrels exhibiting a morphology associated with reduced masticatory efficiency. This effect was partially reversed following a reduction in supplementary feeding of peanuts. We propose that these morphological changes are related to the reduced mechanical effort needed to process peanuts relative to naturally occurring food items. This could be an example of diet-induced plastic changes to the skeleton in non-muroid wild mammals, although further research is needed to exclude other driving factors such as genetics.

Invasive gray squirrels (Sciurus carolinensis) have replaced the native red squirrel (Sciurus vulgaris) across much of Great Britain over the last century. Several factors have been proposed to underlie this replacement, but here we investigated the potential for dietary competition in which gray squirrels have better feeding performance than reds and are thus able to extract nutrition from food more efficiently. In this scenario, we hypothesized that red squirrels would show higher stress, strain, and deformation across the skull than gray squirrels. To test our hypotheses, we created finite element models of the skull of a red and a gray squirrel and loaded them to simulate biting at the incisor, at two different gapes, and at the molar. The results showed similar distributions of strains and von Mises stresses in the two species, but higher stress and strain magnitudes in the red squirrel, especially during molar biting. Few differences were seen in stress and strain distributions or magnitudes between the two incisor gapes. A geometric morphometric analysis showed greater deformations in the red squirrel skull at all bites and gapes. These results are consistent with our hypothesis and indicate increased biomechanical performance of the skull in gray squirrels, allowing them to access and process food items more efficiently than red squirrels.

Glires (rodents, lagomorphs and their fossil kin) is the most speciose and arguably most diversified clade of living placentals. Different lineages within the Glires evolved basically opposite chewing movements: a mostly transversal power stroke in lagomorphs, and a mostly proal power stroke in rodents, but the ancestral condition for Glires is still unclear. To address this knowledge gap, we studied the mandibles of Chinese Palaeocene Glires representing the duplicidentate (lagomorph-like; Mimotona) and simplicidentate (rodent-like; Eomylus and Heomys) lineages. To assess the mechanical resistance of mandibles to bending and torsion, we calculated the section modulus. The dentaries differ greatly in morphology and the region where the maximum grinding force was likely applied. The early Palaeocene Mimotona lii and the middle Palaeocene Mimotona robusta and Heomys orientalis all show a pattern of increasing strength moving posteriorly along the mandible, similar to sciurids and the mountain beaver. By contrast, the late Palaeocene Eomylus sp. mandible was strongest in the m1 region, a pattern seen in lagomorphs and the stem placental Zofialestes. Our results indicate the early diversification of mandible structure of Glires, demonstrate a mixture of duplicidentate and simplicidentate characters among the basal Glires and suggest an early occurrence of a lagomorph-like morphotype. This article is part of the theme issue ‘The mammalian skull: development, structure and function’.

Insular gigantism is an evolutionary phenomenon whereby small animals become bigger on islands compared to their mainland relatives. The abundance of insular giant taxa in the fossil record suggests the presence of a universal “giant niche” present on islands, with resource limitation as a potential driver for this process. However, insular habitats are ecologically diverse, suggesting that island taxa adopt different survival strategies, including adaptations for foraging behaviours. Here we used finite element analysis to evaluate insular feeding niche adaptations in some of the most extreme examples of insular gigantism: Mediterranean giant dormice. We calculated stress, strain and mechanical advantage during incisor and molar biting for three extinct insular giant species (Leithia melitensis, Hypnomys morpheus, H. onicensis), an extant giant (Eliomys quercinus ophiusae), and their extant non-giant mainland relative, the generalist-feeder Eliomys quercinus. Our results show that dietary adaptations vary between giant taxa on different islands, and can occur relatively rapidly. Furthermore, the functional mandibular morphology in some insular taxa indicate adaptations moving away from a generalist feeding strategy towards greater trophic specialization. We show that the “insular giant niche” varies between islands and across time periods, arguing against a universal ecological driver for insular gigantism in small mammals.

The process of feeding in mammals is achieved by moving the mandible relative to the cranium to bring the teeth into and out of occlusion. This process is especially complex in rodents which have a highly specialized configuration of jaw adductor muscles. Here, we used the computational technique of multi-body dynamics analysis (MDA) to model feeding in the red (Sciurus vulgaris) and grey squirrel (Sciurus carolinensis) and determine the relative contribution of each jaw-closing muscle in the generation of bite forces. The MDA model simulated incisor biting at different gapes. A series of ‘virtual ablation experiments' were performed at each gape, whereby the activation of each bilateral pair of muscles was set to zero. The maximum bite force was found to increase at wider gapes. As predicted, the superficial and anterior deep masseter were the largest contributors to bite force, but the temporalis had only a small contribution. Further analysis indicated that the temporalis may play a more important role in jaw stabilization than in the generation of bite force. This study demonstrated the ability of MDA to elucidate details of red and grey squirrel feeding biomechanics providing a complement to data gathered viain vivoexperimentation.

Background: The leporid lagomorphs (rabbits and hares) are adapted to running and leaping (some more than others) and consequently have unique anatomical features that distinguish them from ochotonid lagomorphs (pikas) and from their rodent relatives. Two traits that have received some attention are fenestration of the lateral wall of the maxilla and facial tilting. These features are known to correlate with specialised locomotory form in that the faster running species will generally have fenestration that occupies the dorsal and the anteroventral surface of the maxillary corpus and a more acute facial tilt angle. Another feature is an intracranial joint that circumscribes the back of the skull, thought to facilitate skull mobility. This joint separates the anterior portion of the cranium (including the dentition, rostrum and orbit) from the posterior portion of the cranium (which encompasses the occipital and the auditory complex). Aside from the observation that the intracranial joint is absent in pikas (generalist locomotors) and appears more elaborate in genera with cursorial and saltatorial locomotory habits, the evolutionary history, biomechanical function and comparative anatomy of this feature in leporids lacks a comprehensive evaluation. Methodology: The present work analysed the intracranial joint, facial tilting and lateral fenestration of the wall of the maxilla in the context of leporid evolutionary history using a Bayesian inference of phylogeny (18 genera, 23 species) and ancestral state reconstruction. These methods were used to gather information about the likelihood of the presence of these three traits in ancestral groups. Results: Our phylogenetic analyses found it likely that the last common ancestor of living leporids had some facial tilting, but that the last common ancestor of all lagomorphs included in the dataset did not. We found that it was likely that the last common ancestor of living leporids had fenestration that occupies the dorsal, but not the anteroventral, surface of the maxillary corpus. We also found it likely that the last common ancestor of living leporids had an intracranial joint, but that the last common ancestor of all living lagomorphs did not. These findings provide a broader context to further studies of evolutionary history and will help inform the formulation and testing of functional hypotheses.

Body size and shape play fundamental roles in organismal function and it is expected that animals may possess body proportions that are well-suited to their ecological niche. Tetrapods exhibit a diverse array of body shapes, but to date this diversity in body proportions and its relationship to ecology have not been systematically quantified. Using whole-body skeletal models of 410 extinct and extant tetrapods, we show that allometric relationships vary across individual body segments thereby yielding changes in overall body shape as size increases. However, we also find statistical support for quadratic relationships indicative of differential scaling in small-medium versus large animals. Comparisons of locomotor and dietary groups highlight key differences in body proportions that may mechanistically underlie occupation of major ecological niches. Our results emphasise the pivotal role of body proportions in the broad-scale ecological diversity of tetrapods.

Measures of attachment or accommodation area on the skeleton are a popular means of rapidly generating estimates of muscle proportions and functional performance for use in large-scale macroevolutionary studies. Herein, we provide the first evaluation of the accuracy of these muscle area assessment (MAA) techniques for estimating muscle proportions, force outputs and bone loading in a comparative macroevolutionary context using the rodent masticatory system as a case study. We find that MAA approaches perform poorly, yielding large absolute errors in muscle properties, bite force and particularly bone stress. Perhaps more fundamentally, these methods regularly fail to correctly capture many qualitative differences between rodent morphotypes, particularly in stress patterns in finite-element models. Our findings cast doubts on the validity of these approaches as means to provide input data for biomechanical models applied to understand functional transitions in the fossil record, and perhaps even in taxon-rich statistical models that examine broad-scale macroevolutionary patterns. We suggest that future work should go back to the bones to test if correlations between attachment area and muscle size within homologous muscles across a large number of species yield strong predictive relationships that could be used to deliver more accurate predictions for macroevolutionary and functional studies.