Taxonomic and sex differences in sagittal cresting among gracile and robust capuchin monkeys

Sagittal crests are observed among some primate species, including early extinct hominins, however the majority of research investigating sagittal cresting among extant primates has been confined to catarrhines. Sagittal cresting has not been well-investigated among capuchin monkeys, and understanding whether there are taxonomic differences in the frequency and pattern of sagittal cresting among gracile and robust capuchin species, or whether sagittal crest expression is only confined to the males of some species, may yield important insights in a comparative context, to better understand the underlying basis for the frequency and pattern of sagittal cresting among australopithecine species. In the research presented here, I investigate whether there are interspecific differences in the frequency and pattern of sagittal cresting, and sexual dimorphism in cresting frequency among six capuchin species, representing three gracile capuchin species (Cebus albifrons, Cebus capucinus and Cebus olivaceus) and three robust capuchin species (Cebus apella, Cebus macrocephalus and Cebus libidinosus). I collected sagittal cresting data for 279 dentally mature cranial specimens using 3D models. There are interspecific differences in the frequency of sagittal cresting among capuchin species, with four out of the six species investigated (C. capucinus, C. apella, C. macrocephalus and C. libidinosus) showing sagittal crests. There are significant sex differences in the frequency of sagittal cresting in C. capucinus and robust capuchin species (C. apella, C. libidinosus, C. macrocephalus). I further show that there are interspecific differences in the pattern of sagittal cresting among the four species that exhibit sagittal crests. Sagittal cresting in C. capucinus occurs in the posterior region of the neurocranium, in contrast to the robust capuchin species, whose sagittal crests mainly extend from anterior to bregma, to the posterior cranial region at the midline. The underlying reasons for interspecific and sex differences in the frequency and pattern of sagittal cresting among species are yet to be elucidated, and may be associated with dietary, habitat or socioecological differences among capuchin groups

Comparisons of age-at-death distributions among extinct hominins and extant nonhuman primates indicate normal mortality

Acknowledgements The authors wish to thank the anonymous reviewers and the editor for their constructive and helpful feedback, which has undoubtedly improved this manuscript.Peer reviewedPostprin

Sagittal crest formation in great apes and gibbons

The frequency of sagittal crest expression and patterns of sagittal crest growth and development have been documented in hominoids, including some extinct hominin taxa, and the more frequent expression of the sagittal crest in males has been traditionally linked with the need for larger-bodied individuals to have enough attachment area for the temporalis muscle. In the present study, we investigate sagittal cresting in a dentally mature sample of four hominoid taxa (Pan troglodytes schweinfurthii, Gorilla gorilla gorilla, Pongo pygmaeus pygmaeus and Hylobates lar). We investigate whether sagittal crest size increases with age beyond dental maturity in males and females of G. g. gorilla and Po. pyg. pygmaeus, and whether these taxa show sex differences in the timing of sagittal crest development. We evaluate the hypothesis that the larger sagittal crest of males may not be solely due to the requirement for a larger surface area than the un-crested cranial vault can provide for the attachment of the temporalis muscle, and present data on sex differences in temporalis muscle attachment area and sagittal crest size relative to cranial size. Gorilla g. gorilla and Po. pyg. pygmaeus males show significant relationships between tooth wear rank and sagittal crest size, and they show sagittal crest size differences between age groups that are not found in females. The sagittal crest emerges in early adulthood in the majority of G. g. gorilla males, whereas the percentage of G. g. gorilla females possessing a sagittal crest increases more gradually. Pongo pyg. pygmaeus males experience a three-fold increase in the number of specimens exhibiting a sagittal crest in mid-adulthood, consistent with a secondary growth spurt. Gorilla g. gorilla and Po. pyg. pygmaeus show significant sex differences in the size of the temporalis muscle attachment area, relative to cranial size, with males of both taxa showing positive allometry not shown in females. Gorilla g. gorilla males also show positive allometry for sagittal crest size relative to cranial size. Our results suggest that although patterns of sagittal crest expression have limited utility for taxonomy and phylogeny reconstruction, they could be useful for reconstructing aspects of social behaviour in some extinct hominin taxa. In particular, our results in G. g. gorilla and Po. pyg. pygmaeus, which suggest that the size of sagittal crests in males cannot be solely explained by the surface area required for attachment of the temporalis muscle, offer partial support for the hypothesis that large sagittal crests form in response to sexual selection and may play a role in social signalling

Comparative Context of Hard‐Tissue Sexual Dimorphism in Early Hominins: Implications for Alpha Taxonomy

Sexual dimorphism is one of the main factors confounding attempts to generate sound alpha taxonomic hypotheses in the early hominin fossil record. To better understand how between‐sex variation may confound alpha taxonomic assessments, we consider some of the factors that drive hard‐tissue sexual dimorphism in extant primates. We review the socioecological correlates of body size sexual dimorphism, how sexual selection may be associated with craniofacial sexual dimorphism in the context of visual signaling, and how sex‐specific patterns of growth and development in primates contribute to intra‐specific variation. To illustrate how variation associated with inferred sexual dimorphism has the potential to confound alpha taxonomic assessments in early hominins, we focus on its impact on our understanding of a single taxon, Paranthropus boisei. We suggest that regions of the skeleton likely to be influenced by sexual selection should be avoided when generating alpha taxonomic hypotheses

Relative facial width, and its association with canine size and body mass among chimpanzees and bonobos: Implications for understanding facial width‐to‐height ratio expression among human populations

Objectives: Facial width‐to‐height ratio (fWHR) has been widely investigated in the context of its role in visual communication, though there is a lack of consensus about how fWHR serves as a social signal. To better understand fWHR variation in a comparative context, we investigate the associations between fWHR and canine crown height (CCH) and body mass, respectively, among two chimpanzee subspecies (Pan troglodytes schweinfurthii, Pan troglodytes troglodytes) and bonobos (Pan paniscus). Materials and Methods: We collected landmark data from 3D surface models of 86 Pan cranial specimens to quantify fWHR and upper CCH, and to estimate body mass. We used Spearman's r and Kruskal‐Wallis tests to test for significant relationships among variables, and to assess sexual dimorphism. Results: There is an inverse relationship between fWHR and CCH in both sexes of Pan, however there are interpopulation differences in the relationship between fWHR and CCH among Pan taxa. Pan paniscus have relatively wide faces and small canine crowns, and wide faces in Pan t. schweinfurthii males may be driven by body size constraints. Pan troglodytes and Pan paniscus show fWHR dimorphism, and Pan paniscus have significantly higher fWHRs than do either Pan troglodytes subspecies. Discussion: Our findings indicate that CCH and facial breadth may serve subtly different signaling functions among Pan taxa. Further research into the circumstances in which wide faces evolved among chimpanzees and bonobos will likely afford deeper insights into the function of relatively wide faces in the context of visual signaling among humans and our extinct hominin relatives

Nanostructure-specific X-ray tomography reveals myelin levels, integrity and axon orientations in mouse and human nervous tissue

Myelin insulates neuronal axons and enables fast signal transmission, constituting a key component of brain development, aging and disease. Yet, myelin-specific imaging of macroscopic samples remains a challenge. Here, we exploit myelin’s nanostructural periodicity, and use small-angle X-ray scattering tensor tomography (SAXS-TT) to simultaneously quantify myelin levels, nanostructural integrity and axon orientations in nervous tissue. Proof-of-principle is demonstrated in whole mouse brain, mouse spinal cord and human white and gray matter samples. Outcomes are validated by 2D/3D histology and compared to MRI measurements sensitive to myelin and axon orientations. Specificity to nanostructure is exemplified by concomitantly imaging different myelin types with distinct periodicities. Finally, we illustrate the method’s sensitivity towards myelin-related diseases by quantifying myelin alterations in dysmyelinated mouse brain. This non-destructive, stain-free molecular imaging approach enables quantitative studies of myelination within and across samples during development, aging, disease and treatment, and is applicable to other ordered biomolecules or nanostructures

Sexual dimorphism, growth and development beyond dental maturity in the cranium of extant hominoid primates

Sexual size dimorphism is a useful predictor of sociality in primates based on the association between male intrasexual competition and male size, relative to female size. Less considered ideas include the relationship between sexual dimorphism of facial traits and socioecological variability and the notion that females may obtain reproductive advantages from larger body size or facial morphology, similar to what is observed in males. In the present research, I investigate the morphological correlates of social and non-social variables to understand whether the facial skeleton, including the sagittal crest, carries a social signal. I adopt the heterochronic framework advocated by Shea (1986) to understand how sexual dimorphism is attained. I examine craniofacial size and shape dimorphism, growth and development in five extant hominoid primate taxa (Homo sapiens, Pan t. schweinfurthii, Gorilla g. gorilla, Pongo p. pygmaeus and Hylobates lar) to understand whether sex-specific patterns of facial dimorphism, growth and development are associated with social and life history variables. I use 3D surface data to quantify cranial size and shape using 3D co-ordinate landmarks, surface area data and linear measurements. Geometric morphometric techniques are used to calculate size and shape variables, including Procrustes distances between male and female average shapes, and visualisation of shape differences using Principal component scores. Marital system explains a small, but significant, amount of craniofacial size and shape variation in modern humans, and patterns of shape dimorphism in the brow ridge of Pan t. schweinfurthii and Gorilla g. gorilla, and in the mid-face of Gorilla g. gorilla and Pongo p. pygmaeus, indicate that sex-specific shape of these regions may be morphologically conserved. Sagittal crest emergence in Gorilla g. gorilla and Pongo p. pygmaeus males cannot be explained by mastication alone and is likely to be, in part, a result of sexual selection. Future studies, adopting a heterochronic approach to sexual dimorphism, are likely to afford detailed inferences about the relationship between morphological and behavioural variables and may have applications in reconstructing extinct hominoid social behaviour

One Genus or Two? Evaluating Whether Gracile and Robust Capuchin Monkeys are Validly Classified as Separate Genera Based on Craniofacial Shape. Craniofacial shape dataset.

Assessments of whether closely related species should be classified into more than one genus have been a longstanding source of controversy in primatology. For example, researchers hold differing opinions about whether cebine species should be classified into one or two genera. In this study, we investigated whether craniofacial shape is a reliable taxonomic indicator among cebines and statistically evaluated whether the magnitude of craniofacial shape differences observed among gracile and robust capuchin species is consistent with a two-genus taxonomic framework. We quantify craniofacial shape using 3D landmark data taken from 72 surface models, representing five cebine species (Cebus albifrons, C. capucinus, C. olivaceus, C. (Sapajus) libidinosus, and C. (S.) macrocephalus). We find that although statistically significant shape differences exist between gracile and robust capuchins in all four craniofacial regions investigated (face and palate, basicranium, calvarium, and frontal region of the calvarium), the magnitude of shape differences between species pairs does not support gracile and robust species being classified into separate genera. The shape of the frontal region of the calvarium and the face and palate show the highest magnitude of shape differences between the gracile and robust capuchin groups, and both regions are good taxonomic predictors, showing correct classification rates of 97% and 96%, respectively. At the species-level, face and palate shape is the only craniofacial measure that consistently shows high correct classification rates among species (84-97% for combined-sex analyses). Our findings suggest that robust capuchin species that are often assigned to Sapajus may be more appropriately considered as Cebus under a single-genus framework for cebines based on craniofacial shape evidence.</p