Nathan Jeffery

The labyrinthine geometry and functional anatomy of the semicircular canals have intrigued scientists for decades, and there has been considerable interest in understanding how these complex structures grow and develop with evidence emerging from human studies that size maturation occurs exceptionally early by comparison with other systems. Here we seek to extend the empirical evidence base and our understanding by investigating canal ontogeny in a non‐human species. The postnatal development of the murine bony semicircular canals was investigated to determine the timing of size and shape maturation in relation to ossification of the surrounding otic capsule. Using micro‐CT imaging and geometric morphometric analysis of 43 male C57BL/6J mice across six developmental stages (postnatal days 1–48 and 26 months), this study reveals that the semicircular canals undergo rapid growth and shape transformation within the first postnatal week. Ossification begins between P1 and P7, coinciding with the most significant observed increases in canal length and configuration shape. By P14, the canals are fully encased in a thin layer of bone, and subsequent changes are minimal, mostly in size, indicating morphological stabilization. This is further supported by a decrease in size variability as ossification progresses. These findings support the hypothesis that ossification imposes a progressively tighter constraint on canal form, as reflected by the gradual reduction in shape variation past the onset of ossification. Cross‐section area shows negligible variation, suggesting early maturation of this feature. These findings highlight a brief but critical window of morphological plasticity in early postnatal life, with implications for interpreting vestibular development and fossil ontogeny in mammals.

Facial expression is a key component of primate communication, and primates (including humans) have a complex system of facial musculature underpinning this behavior. Human facial musculature is highly variable across individuals, but to date, whether other primate species exhibit a similar level of inter‐individual variation is unknown. Whether individual‐level variation in facial musculature covaries with significant differences in facial movement within the same individual is also unknown. Here, we use facial dissection data from 31 adult rhesus macaques, the largest sample to date, to quantify inter‐individual variation in facial muscle presence. We used a subsample of eight individuals to measure covariation between facial muscle presence and the presence of external facial movements (action units in the Facial Action Coding System, or FACS). We found, in contrast to humans, limited inter‐individual variation in muscle presence, but the zygomatic region exhibited more gross anatomical variation in muscle presence and morphology than any other region of the macaque face. We also found a good correspondence between facial muscle presence and the presence of the associated action units. Our results indicate that the observed variation in rhesus macaque facial expressivity is not likely driven primarily by variation in facial muscle presence but may instead be due to other factors such as learned behavior and/or physiological differences. These findings provide insight into the anatomical basis of inter‐individual variation in facial behavior in primates and suggest potential differences in variation between humans and other primate species.

Spatial growth constraints in the head region can lead to coordinated patterns of morphological variation that pleiotropically modify genetically defined phenotypes as the tissues compete for space. Here we test for such architectural modifications during rhesus macaque (Macaca mulatta) postnatal ontogeny. We captured cranium and brain shape from 153 MRI datasets spanning 13 to 1090 postnatal days and tested for patterns of covariation with measurements of relative brain, eyeball, and masseter muscle size as well as callosal tract length. We find that the shape of the infant (<365 days) macaque cranium was most closely aligned to masseter muscle and brain size measured relative to face size. Infant brain and juvenile (365–1090 days) cranium shape were more closely linked with brain size relative to basicranium and face size. Meanwhile, the juvenile macaque brain shape was dominated by the size of the brain relative to that of the basicranium. Associations with relative eyeball size and commissural tract lengths were weaker. Our results are consistent with a spatial‐packing regime operating during postnatal macaque ontogeny, in which relative growth of the masseter, face and basicranium have a greater influence than brain growth on the overall shape of the cranium and brain.

The semicircular canals (SCCs) transduce angular acceleration of the head into neuronal signals, and their morphology has been used to infer function. Once formed, the bony labyrinth, that surrounds the canals, is tightly regulated and has a very low bone turnover. However, relaxed postnatal inhibition of bone remodelling later in ontogeny may allow for some organised adjustments of shape and size or for greater stochastic variation. In the present study, we test the hypotheses that after birth, the shape and size of the bony canal changes or becomes more variable, or both. We study microCT scans of human perinatal and adult temporal bones using a combination of geometric morphometric analysis and cross‐sectional measures. Results revealed marginal differences of size (<5%), of cross‐sectional shape and of measurement variability. Geometry of the three canals together and their cross‐sectional areas were, however, indistinguishable between perinates and adults. These mixed findings are indicative of diminutive levels of relaxed inhibition superimposed over a constrained template of SCC morphology.

Covariations between anatomical structures are fundamental to craniofacial ontogeny, maturation, and aging and yet are rarely studied in such a cognate fashion. Here, we offer a comprehensive investigation of the human craniofacial complex using freely available software and MRI datasets representing 575 individuals from 0 to 79 years old. We employ both standard craniometrics methods as well as Procrustes‐based analyses to capture and document cross‐sectional trends. Findings suggest that anatomical structures behave primarily as modules, and manifest integrated patterns of shape change as they compete for space, particularly with relative expansions of the brain during early postnatal life and of the face during puberty. Sexual dimorphism was detected in infancy and intensified during adolescence with gender differences in the magnitude and pattern of morphological covariation as well as of aging. These findings partly support the spatial‐packing hypothesis and reveal important insights into phenotypic adjustments to deep‐rooted, and presumably genetically defined, trajectories of morphological size and shape change that characterize the normal human craniofacial life‐course.

Networks linking single genes to multiple phenotypic outcomes can be founded on local anatomical interactions as well as on systemic factors like biochemical products. Here we explore the effects of such interactions by investigating the competing spatial demands of brain and masticatory muscle growth within the hypermuscular myostatin‐deficient mouse model and in computational simulations. Mice that lacked both copies of the myostatin gene (‐/‐) and display gross hypermuscularity, and control mice that had both copies of the myostatin gene (+/+) were sampled at 1, 7, 14 and 28 postnatal days. A total of 48 mice were imaged with standard as well as contrast‐enhanced microCT. Size metrics and landmark configurations were collected from the image data and were analysed alongside in silico models of tissue expansion. Findings revealed that: masseter muscle volume was smaller in ‐/‐ mice at day 1 but became, and remained thereafter, larger by 7 days; ‐/‐ endocranial volumes begin and remained smaller; ‐/‐ enlargement of the masticatory muscles was associated with caudolateral displacement of the calvarium, lateral displacement of the zygomatic arches, and slight dorsal deflection of the face and basicranium. Simulations revealed basicranial retroflexion (flattening) and dorsal deflection of the face associated with muscle expansion and abrogative covariations of basicranial flexion and ventral facial deflection associated with endocranial expansion. Our findings support the spatial‐packing theory and highlight the importance of understanding the harmony of competing spatial demands that can shape and maintain mammalian skull architecture during ontogeny.

Insular gigantism—evolutionary increases in body size from small-bodied mainland ancestors—is a conceptually significant, but poorly studied, evolutionary phenomenon. Gigantism is widespread on Mediterranean islands, particularly among fossil and extant dormice. These include an extant giant population of Eliomys quercinus on Formentera, the giant Balearic genus † Hypnomys and the exceptionally large † Leithia melitensis of Pleistocene Sicily. We quantified patterns of cranial and mandibular shape and their relationships to head size (allometry) among mainland and insular dormouse populations, asking to what extent the morphology of island giants is explained by allometry. We find that gigantism in dormice is not simply an extrapolation of the allometric trajectory of their mainland relatives. Instead, a large portion of their distinctive cranial and mandibular morphology resulted from the population- or species-specific evolutionary shape changes. Our findings suggest that body size increases in insular giant dormice were accompanied by the evolutionary divergence of feeding adaptations. This complements other evidence of ecological divergence in these taxa, which span predominantly faunivorous to herbivorous diets. Our findings suggest that insular gigantism involves context-dependent phenotypic modifications, underscoring the highly distinctive nature of island faunas.

Cranial form is closely allied to diet and feeding behavior in the Canidae, with the force and velocity of jaw‐closing depending on the bony morphology of the skull and mandible, and the mass, architecture, and siting of the jaw adductor muscles. Previously, little has been reported on the details of the form and function of canid jaw adductor muscles, with earlier studies basing functional hypotheses on data derived from dry skull specimens. Here we use empirically derived muscle data from fresh‐frozen specimens to explore the architecture of the muscles, and to inform finite element analyses models that predict bite force and strain energy in 12 species of wild canid. The inclusion of muscle architectural detail is shown to influence masticatory muscle force production capability calculations, indicating that muscles with longer fascicles were disadvantaged compared to muscles with shorter fascicles. No clear patterns of allometry were detected. Dietary groups were differentiated by temporalis fascicle angles, which, when allied with the differentiation of rostral length reported in previous studies, may further contribute to specializations of fast jaw‐closing or forceful jaw‐closing species. The most biomechanically demanding masticatory function is canine biting, and the highest strain energy values were reported in this loading condition, particularly in the zygomatic arches and caudal rostrum. Specific head shapes may be constrained by size, with scaled strain energy models predicting that some bony morphologies may only be viable in species with small body masses.

Reconstructions of habitual activity in past populations and extinct human groups is a primary goal of paleoanthropological research. Muscle attachment scars (entheses) are widely considered as indicators of habitual activity and many attempts have been made to use them for this purpose. However, their interpretation remains equivocal due to methodological limitations and a paucity of empirical data supporting an interaction between systematic muscle forces and entheseal morphology. We have recently addressed the first issue with precise three-dimensional measuring protocols and rigorous multivariate analysis focusing on the patterns among different entheses rather than comparing each entheseal structure separately. In a previous study, the resulting entheseal correlations reflected synergistic muscle groups that separated individuals according to their lifelong occupational activities. Here we address the second issue by applying this methodology to existing micro-computed tomography data from rats that have undergone muscle stimulation under experimental conditions. In contrast to previous animal studies, we relied on blind analytical procedures across two research institutions and controlled for most factors of interindividual variability. Results demonstrated that the multivariate associations among different entheseal surfaces can directly reflect repetitive muscle recruitment and provide essential information on muscle use.

Self-motion triggers complementary visual and vestibular reflexes supporting image-stabilization and balance. Translation through space produces one global pattern of retinal image motion (optic flow), rotation another. We examined the direction preferences of direction-sensitive ganglion cells (DSGCs) in flattened mouse retinas in vitro. Here we show that for each subtype of DSGC, direction preference varies topographically so as to align with specific translatory optic flow fields, creating a neural ensemble tuned for a specific direction of motion through space. Four cardinal translatory directions are represented, aligned with two axes of high adaptive relevance: the body and gravitational axes. One subtype maximizes its output when the mouse advances, others when it retreats, rises or falls. Two classes of DSGCs, namely, ON-DSGCs and ON-OFF-DSGCs, share the same spatial geometry but weight the four channels differently. Each subtype ensemble is also tuned for rotation. The relative activation of DSGC channels uniquely encodes every translation and rotation. Although retinal and vestibular systems both encode translatory and rotatory self-motion, their coordinate systems differ.