Evan A. Simons

The amygdaloid complex mediates learning, memory, and emotions. Understanding cellular and anatomical features specialized in the primate amygdala versus other mammals requires a systematic, anatomically resolved molecular analysis of neuron types. We analyzed five nuclear subdivisions of the primate amygdala with single-nucleus RNA sequencing in macaques, baboons, and humans to examine gene expression profiles for excitatory and inhibitory neurons. Integrated analyses across species identified diverse subtypes of glutamatergic and GABAergic neurons that are highly conserved across primates. Compositional analyses revealed that subdivisions of the primate basolateral complex contain distinct classes of glutamatergic neurons and divergent gene expression profiles for parvalbumin and somatostatin GABAergic neurons. Referencing primate neuron types to transcriptomic atlases of the murine amygdala highlighted primate-specific specializations for glutamatergic neurons and identified which neuron types are conserved across mammals and amygdalar subdivisions. Understanding the molecular heterogeneity of anatomically resolved amygdalar neuron types provides a cellular framework for improving models of how amygdalar circuits contribute to cognition and mental health.

The amygdaloid complex mediates learning, memory, and emotions. Understanding the cellular and anatomical features that are specialized in the amygdala of primates versus other vertebrates requires a systematic, anatomically-resolved molecular analysis of constituent cell populations. We analyzed five nuclear subdivisions of the primate amygdala with single-nucleus RNA sequencing in macaques, baboons, and humans to examine gene expression profiles for excitatory and inhibitory neurons and confirmed our results with single-molecule FISH analysis. We identified distinct subtypes of FOXP2 ⁺ interneurons in the intercalated cell masses and protein-kinase C-δ interneurons in the central nucleus. We also establish that glutamatergic, pyramidal-like neurons are transcriptionally specialized within the basal, lateral, or accessory basal nuclei. Understanding the molecular heterogeneity of anatomically-resolved amygdalar neuron types provides a cellular framework for improving existing models of how amygdalar neural circuits contribute to cognition and mental health in humans by using nonhuman primates as a translational bridge.

Objectives: Geographic variation is an important feature among primates, but the mechanisms underlying it are not well understood. Macaques are geographically widespread and have been translocated to captive populations, providing a prime opportunity to evaluate changes in cranial form in response to a novel environment. Clinal variation was assessed among wild fascicularis‐group macaques and compared to two translocated populations to explore the relative contributions of developmental plasticity and microevolutionary forces in producing geographic variation in cranial form.Materials and Methods: Forty‐five 3D coordinates over the cranium were taken on 380 wild macaques and 56 captive Macaca mulatta from Cayo Santiago, PR and Beaverton, OR. Geographic shape, represented by the singular warp scores from a two‐block partial least squares analysis, and centroid size were regressed against latitude, mean annual temperature, and mean annual precipitation among wild macaques. The two captive populations were compared to wild M. mulatta to assess potential changes in cranial form.Results: Size and geographic shape were highly correlated with latitude in wild macaques, but neither ecological variable was important across the entire cline. Precipitation was important for shape only outside the tropics. Translocated M. mulatta are significantly larger, but not different in shape, compared to wild M. mulatta.Discussion: These results are consistent with previous studies demonstrating cranial form is latitudinally variable among fascicularis‐group macaques, but the potential drivers remain unclear. Size is highly plastic while geographic shape has evolved differentiation at interpopulation and interspecific levels. Variation in cranial morphology likely arises first in size, followed relatively rapidly by evolved modifications to shape.

Objectives The Giles hypothesis posits that differences in the cranial morphology of Pan troglodytes and Gorilla gorilla are largely the result of allometric scaling. However, previous support for the Giles hypothesis was based on bivariate plots of linear measurements. This investigation uses geometric morphometric methods to retest this hypothesis and its prediction that extending the ontogenetic trajectory of a chimpanzee would produce an adult gorilla‐like cranial morphology. Materials and Methods Forty‐three 3D cranial landmarks were collected from an ontogenetic series of 76 Pan troglodytes and 58 Gorilla gorilla specimens. Ontogenetic trajectories of cranial shape change were computed via multivariate regression of Procrustes aligned coordinates against LnCS (size vector) and molar eruption stage (developmental vector). These two vectors were then used in developmental simulations to extend the ontogenetic trajectories of adult chimpanzees. Allometric trajectories of chimpanzees and gorillas were also directly compared using Procrustes ANOVA. Results Pan and Gorilla significantly differ in their allometric trajectories, and none of the Pan developmental simulations resembled actual adult gorillas. Additionally, the more the Pan developmental vector was extended, the more morphologically distinct the simulations became from actual adult gorillas. Discussion Taken together, these results do not support the Giles hypothesis that allometric scaling is primarily responsible for observed morphological differences between chimpanzee and gorilla crania. This investigation demonstrates that neither “growing” a chimpanzee to the size of a gorilla, nor extending a chimpanzee's developmental shape trajectory will result in an adult gorilla‐like cranial morphology as they differ in their patterns of allometry.

In studies of ontogenetic allometry, ontogenetic scaling has often been invoked to explain cranial morphological differences between smaller and larger forms of closely related taxa. These scaled variants in shape have been hypothesized to be the result of the extension or truncation of common growth allometries. In this scenario, change in size is the determining factor, perhaps under direct selection, and changes in cranial shapes are byproducts, not under direct selection themselves. However, many of these conclusions are based on studies that used bivariate generalizations of shape. Even among multivariate analyses of growth allometries, there are discrepancies as to the prevalence of ontogenetic scaling among primates, how shared the trajectories need to be, and which taxa evince properties of scaled variants. In this investigation, we use a large, comparative ontogenetic sample, geometric morphometric methods, and multivariate statistical tests to examine ontogenetic allometry and evaluate if differences in cranial shape among closely related catarrhines of varying sizes are primarily driven by size divergence, that is, ontogenetic scaling. We then evaluate the hypothesis of size as a line of least evolutionary resistance in catarrhine cranial evolution. We found that patterns of ontogenetic allometry vary among taxa, indicating that ontogenetic scaling sensu stricto does not often account for most morphological differences and that large and small taxa within clades are generally not scaled variants. The presence of a variety of ontogenetic pathways for the evolution of cranial shapes provides indirect evidence for selection acting directly on the cranial shape, rather than on size alone.

Objectives: Magnitudes of morphological integration may constrain or facilitate craniofacial shape variation. The aim of this study was to analyze how the magnitude of integration in the skull of Macaca fascicularis changes throughout ontogeny in relation to developmental and/or functional modules.Materials and methods: Geometric morphometric methods were used to analyze the magnitude of integration in the macaque cranium and mandible in 80 juvenile and 40 adult M. fascicularis specimens. Integration scores in skull modules were calculated using integration coefficient of variation (ICV) of eigenvalues based on a resampling procedure. Resultant ICV scores between the skull as a whole, and developmental and/or functional modules were compared using Mann–Whitney U tests.Results: Results showed that most skull modules were more tightly integrated than the skull as a whole, with the exception of the chondrocranium in juveniles without canines, the chondrocranium/face complex and the mandibular corpus in adults, and the mandibular ramus in all juveniles. The chondrocranium/face and face/mandibular corpus complexes were more tightly integrated in juveniles than adults, possibly reflecting the influences of early brain growth/development, and the changing functional demands of infant suckling and later masticatory loading. This is also supported by the much higher integration of the mandibular ramus in adults compared with juveniles.Discussion: Magnitudes of integration in skull modules reflect developmental/functional mechanisms in M. fascicularis. However, the relationship between “evolutionary flexibility” and developmental/functional mechanisms was not direct or simple, likely because of the complex morphology, multifunctionality, and various ossification origins of the skull.

Previous investigations of the primate talo‐crural joint (TCJ; specifically on the talus and distal tibia) have demonstrated that substrate preference significantly influences morphology, but this association is not necessarily found in subadults. This has been interpreted as the result of a plastic, behaviorally induced response of bone due to substrate use. In this investigation, we use geometric morphometric and phylogenetic comparative methods to investigate ontogenetic phenotypic plasticity in the catarrhine TCJ. Osteological specimens from four African hominoid and four cercopithecid species, divided into subadult and adult developmental stages based on molar eruption, formed the study group. We tested for phylogenetic signal in the shape of both the talar and tibial articular surfaces, at both developmental stages. We then used phylomorphospaces to examine the evolution of shape differences at each developmental stage for each element, and to determine if substrate usage is associated with shape in this phylogenetic context. A significant phylogenetic signal was found for both articular surfaces in subadults, but not adults. In phylomorphospace, both talar and tibial articular morphologies show an association with substrate preference in adults, but not in subadults. Our results provide confirmation of the significant effect of habitual substrate usage and the consequences of bone remodeling during ontogeny on the shape and presentation of the TCJ. These results also suggest caution when using adult talo‐tibial shapes to evaluate phylogenetic relationships as TCJ morphology can be considered as a palimpsest, with substrate usage overwriting phylogenetic information in adult specimens. Anat Rec, 302:1977–1984, 2019. © 2019 American Association for Anatomy