The primate skull is comprised of complexes including the cranial base, vault and facial region. How these complexes respond to different developmental and growth processes as well as varied selective pressures like diet, locomotion and sexual selection have been investigated in terms of modularity and integration. The concepts of modularity and integration concern the co-variance or independence of these complexes.
Profico et al. used several recent statistical methods to test previous research conclusions suggesting the primate cranial base and facial complex are strongly integrated. The cranium from 11 extant species of the Cercopithecoidea and Hominoidea were studied utilizing geometric morphometrics to investigate shape variation, the presence of evolutionary allometry and modularity or integration.
Shape variation of the primate cranial base and facial complex was assessed by Principal Component Analysis. Among taxa, shape variation of the cranial base reflected patterns in locomotion, cranial base flexion and the size of the foramen magnum. The shape variation of the facial complex reflected size-related and sex-linked morphology, the degree of lower and mid-facial prognathism and associated changes to narrowing of the nasal-orbital regions. Evolutionary allometry was tested by multivariate regression of size on shape and indicated the facial complex but not the cranial base was influenced by evolutionary allometry. Modularity and integration was analyzed using Partial Least Squares to test the degree of co-variation between the facial complex and cranial base which proved to be low. These combined results suggested the cranial base and facial complex complied with the concept of modularity rather than integration contrasting with previous studies.
An important reminder that although a pattern of similarity was found between Pongo pygmaeus and Hylobates lar this does not imply a close biological relationship, rather these taxa share similar cranial base and facial block morphology, potentially as a by-product of orthograde posture and the absence of quadrupedalism found in the other primate taxa with the exception of modern humans which are obligate bipeds. In light of the current findings, a more comprehensive reconsideration may be necessary of the effects from variation in the facial complex and cranial base morphology throughout primate evolution.
Fiorenza L., Bruner E. 2017. Cranial shape variation in adult howler monkeys (Alouatta seniculus). Am. J. Primatol. [link]
Emeritus Professor Colin Groves was an internationally-recognized and respected taxonomist in Mammalogy and Primatology. After completing his PhD dissertation at University College London in 1966 on Gorilla skull variation and taxonomy, Colin was appointed as lecturer at the Australian National University (ANU). Colin was an integral part of the ANU Biological Anthropology Department, welcoming discussions with internationally recognized researchers and undergraduate students alike, always made himself available and believed in an “open-door” policy for teaching. For me, he was an inspirational and influential mentor, teacher, colleague and friend who was an irreplaceable part of the Australian and International Primatology and Anthropology community. An online condolence book has been organised for those wishing to pay their respects.
The International Encyclopedia of Primatology, a new multi-volume resource suited to an academic audience studying human and non-human primates with topics on evolutionary biology, genetics, behaviour, taxonomy and ecology.
Dimitri Neaux and colleagues have published a series of comprehensive analyses on the influence of the cranial base in facial morphology of humans and apes. In one of the papers, they assessed the integration between the face and the two basicranial modules: the sagittal and the lateral cranial base. They tested the covariation between the three sets of 3D landmarks (face vs. midline base and face vs. lateral base) on modern humans and chimpanzees, separately. Only the correlation between the face and the lateral cranial base was significant, confirming the important role of the lateral cranial base in facial morphology. Though the levels of covariation were comparable, the patterns differed between the two species, as taller faces were associated with wider and shorter cranial fossae in chimps and with longer and narrower cranial fossae in humans. In another article, they assessed the relationship between cranial base flexion, facial orientation, and facial shape in modern humans, chimpanzees, and gorillas. Using 3D landmark analysis, they evaluated the within-species patterns of covariation, confirming the intraspecific relationship between facial structures and base flexion. Base flexion is associated with downward rotation of the facial block in both humans and chimps (confirming previous works) but not in gorillas. On the other hand, an upward rotation of the facial block is associated with anterior face vertical elongation on the three species. In humans, facial elongation is also associated with base flexion, which might have been selected during evolution to match the elongation of the nasomaxillary complex, as proposed before. The authors further tested whether increased base flexion is associated with the shortening of the facial length or with the decrease of facial projection. The relationship between base flexion and facial length was only observed in chimps, while facial projection was not related with cranial base flexion in chimpanzees and gorillas. In humans, contrary to what was expected, basicranial flexion was associated with increasing facial projection, which the authors attribute to sexual dimorphism, as males have increased base flexion and facial projection. Again, the main patterns of correlation differed between the species. Cranial base angle is negatively correlated with facial projection in modern humans, with facial length in chimps, and with the angle between the posterior-maxillary plane and the anterior facial plane in gorillas. As the authors conclude, these differences in the patterns of integration might reflect changes in the structural relationships between the face and the cranial base during hominoid evolution.
In general, members of the Primate Order possess larger brains for body size than other mammals, with modern humans (Homo sapiens) evolving the largest brains. The Internal Carotid Artery (ICA) provides blood supply to the brain but there are distinct anatomical differences between the primate groups. While vascular and other soft-tissues are very rarely fossilised, evidence of the ICA passage is retained where it was encapsulated in bony tubes or as distinct grooves of the endocranial surface. The ICA evolved in primates from two main pathways in the auditory complex: the promontory artery branched from the cochlear space to supply blood to the brain while the stapedial artery branched from the obturator foramen of the stapes to provide blood to the cerebral meninges and the orbito-facial complex. Primate groups are recognised by ICA anatomy: Within the Strepsirrhini, Lorisiformes and Cheirogaleids both lack the stapedial and promontory arteries with the External Carotid Artery (ECA) supplying blood to the brain instead of the ICA; whereas, non-Cheirogaleids possess the ICA and stapedial artery but often retain a much smaller promontory artery, while the anthropoids (apes and monkeys) lack the stapedial artery entirely retaining only the promontory artery.
The evolution of these distinct differences was examined by comparing living and fossil primates and reconstructing the hypothetical phylogenetic pathways. The size differences between the stapedial and promontory arteries were compared to endocranial volume (ECV) to investigate the influence on brain size. Only the size of the promontory artery had a consistent correlation with brain size. There was no reported correlation between brain size and size of the stapedial artery, with the stapedial only correlating with size of the promontory artery. This suggests that throughout primate evolution, the trend for body and brain size increases caused the stapedial artery to become restricted as head size increased but size of the obturator foramen did not scale equally with the head. Most early primates evolved a reduction in the size of the stapedial artery and quickly accommodated an increase in the promontory artery allowing even greater blood flow to the brain and driving the encephalisation process and the eventual loss of the stapedial artery in anthropoids.
The mature primate brain consists of many layers with the outer layer or cerebral cortex forming folds known as sulci and gyri. During embryonic development, the brain is divided into zones with the inner-most ventricular zone where neurons are formed and a series of cytoarchitecturally distinct layers forming plates radiating outward. The subplate is located between the inner ventricular zone and the outer cortical plate hosting the migration of neurons allowing brain expansion. Most embryonic brain research is conducted on non-primate mammals but there are substantial differences in the development of the non-primate and primate brain. A very recent study utilized existing primate tissue databases to examine the embryonic development of the subplate zone in non-human and human primates. Duque et al. found during that development of the macaque brain, once the neurons have migrated to the subplate they then are pushed downward by axons derived from the subcortical layer before further compression occurs from further axonal development originating from the cortical layer. The implications of this force acting on the neurons within the subplate suggests that thickness of the subplate differs unevenly throughout the brain potentially due to an increased axonal density. Duque et al. suggest the density of axonal fibers increases with demand for more connectivity between brain regions with those areas possessing a high-demand for greater complexity causing a thicker subplate.
Changes at the cellular-level of the subplate also have implications for the development of the cerebral convolutions such as sulci and gyri. It was recently posed that the folding patterns in the human brain are the result of mechanical forces related to the subplate and outer expansion of the cerebral cortex. Tallinen et al. showed through numeric and physical simulations with the support of MRI that during fetal development the subplate stabilizes while the outer cortical plate continues to expand. The final stages of growth see the cortical layer undergo extensive gyrification to form the folding patterns we see in the adult human brain. Overall, a better understanding of human neurobiology informed through non-human primate neurobiology offers a glimpse into the evolutionary pathways which led to the evolution of modern humans.
New PhD student in our network! Alannah Pearson is now beginning her project on temporal lobes evolution in human and non-human primates, with a special focus on paleoneurology and functional craniology. She will be supervised by an amazing team of experts, including David Polly (Indiana University) and Colin Groves, Alison Behie and Katharine Balolia (Australian National University). A short presentation, in her own words: “I was born in Australia in 1985 and I am currently a PhD candidate at the Australian National University in Canberra. I completed a Bachelor of Arts in Archaeology and Palaeoanthropology before an Honours year specialising in Biological Anthropology analysing pre-collected craniometric data from populations in India before comparing these to William White Howells’ global craniometric datasets to assess population affinities. I recently completed a Master of Philosophy in Palaeoanthropology using CT of hominoid cranial bones examining inter- and intraspecific shape variation, phylogenetic signal, allometric and non-allometric differences. I also conducted phylogenetic analyses using Neighbour-Joining and Continuous Trait Maximum Likelihood methods. I am interested in the evolution of extant and fossil primate cranial morphology, shape and size differences between taxa. I recently became fascinated with primate cerebral evolution and shape variation with this being the direction of my PhD project. When not studying physical anthropology, I like to write fiction novels and I am currently working toward publication. I also have a keen interest in digital photography, particularly landscape and wildlife photography.” Welcome at the Laboratory of Hominid Paleoneurobiology!