Studying the evolution of brain form requires paleoneruologists to rely on casts from the cranial cavity from fossil species. Due to the lack of soft-tissue preservation in fossils, descriptions of macroanatomy and cytoarchitecture are taken from comparative non-human primates to serve as hypothetical models of early hominin brain form. Using extant non-human primates as models for fossil species ignores the separation of lineages, any specific adaptations and lineage-specific evolution since divergence. Furthermore, extant species risk being relegated as ‘living fossils’ with the issue worsened by the absence of identifiable fossils for either Pan or Gorilla. The untenable assumption is that extant chimpanzee anatomy should resembles the original form prior to the Pan–Homo split. Nonetheless, comparison among living hominoids is still mandatory to investigate the evolutionary radiation of this taxon.
Previous published descriptions of chimpanzee sulcal patterns occur in classic literature but were based on only a few post-mortem dissections. Recently, Falk and colleagues aimed to increase knowledge of chimpanzee sulcal variation by describing sulcal patterns present in in-vivo Magnetic Resonance Imaging (MRI) from eight chimpanzees. Results suggested that, contrary to previous opinion, two sulci do occur in both chimpanzees and humans. To elaborate, these two sulci are the middle-frontal sulcus located in the frontal lobe, and lunate sulcus located between the parietal and occipital lobes.
No quantitative analyses were conducted in this study, but Falk et al. (2018) provide detailed descriptions of the variation between individuals, highlighting why descriptions based on only one or two individuals cannot be used to reliably describe the brain anatomy of a species. The authors argue the presence of the middle-frontal sulcus and lunate sulcus in chimpanzees invalidates previous claims that these sulci represent derived states found only in the human lineage. Further quantitative analyses with much larger samples, including both extant and fossil species will aid in a better understanding of the brain anatomy of humans and other great ape species.
Primates are unique among mammals for having a brain much larger than expected for body size. An important aim in paleoneurology is understanding how cerebral structures reorganized to accomodate primate cerebral expansion. The brain comprises only soft-tissue and does not fossilize so paleoneurologists rely on endocasts, either physical or digital molds of the cranial cavity, to estimate the macro-anatomy of the brain. Continuing computational advances and powerful imaging techniques have allowed the generation of increasingly higher-resolution digital endocasts. Gonzales et al. (2015) generated a high-resolution endocast of the 15 Myr-old fossil cercopithecine Victoriapithecus macinnesi using micro-CT scans. By using computational methods, taphonomic distortion was corrected and a new endocranial volume (ECV) of 35.6 cm3 reported for Victoriapithecus which is much smaller than the previous value 54 cm3. This new, smaller ECV places Victoriapithecus within the range of extant strepsirrhines but outside the range expected of extant and fossil cercopithecoids including the 32 Myr-old fossil species Aegyptopithecus zeuxis which had an ECV within the expected range for fossil cercopithecoids.
Despite Victoriapithecus exhibiting a very small ECV and falling below the range for extant cercopithecoids, the fossil does exhibit the ‘frog-shaped’ sulcal pattern shared only among cercopithecines. This sulcal pattern suggests Victoriapithecus is a cercopithecine, the ‘frog-shaped’ sulcal pattern is such a diagnostic trait that it is not shared by the leaf-eating colobines but only present in cercopithecines. The olfactory bulbs in Victoriapithecus are unusually large relative to the small ECV. Large olfactory bulbs are present in extant strepsirrhines and the fossil catarrhine Aegyptopithecus zeuxis but reduced in all extant and fossil cercopithecoids and hominoids. The presence of small olfactory bulbs in the 18 Myr-old hominoid Proconsul versus the large bulbs in Victoriapithecus suggested olfactory bulb reduction may have evolved independently in both cercopithecoids and hominoids.
Harrington et al. (2016) compared digital endocasts generated from micro-CT of three adapiform fossil primates including the 48 Myr-old Notharctus tenebrosus, 47 Myr-old Smilodectes gracilis and 45 Myr-old Adapis parisiensis. Results of endocranial volume (ECV) were consistent with other studies revealing an ECV of 7.6 cm3 for Notharctus, an ECV of 8.3 cm3 for Smilodectes while Adapis had an ECV of 8.8 cm3. The sulcal morphology of these adapiforms was also consistent with previous studies showing the defining feature of the primate brain, the Sylvian sulcus, is species-specific in these adapiforms. The Sylvian sulcus is well-defined in Adapis, occurs only as a shallow depression in Notharctus but is entirely lacking in Smilodectes. The absence of the Sylvian sulcus in Smilodectes is not understood but as it is absent in other mammals, this may represent a retained ancestral trait from before the divergence of primates from other mammals.
The cerebral organization of Notharctus and Smilodectes showed both possessed larger temporal and occipital lobes relative to brain size with smaller olfactory bulbs and frontal lobes. This trend might indicate cerebral reorganization favoring larger visual-auditory structures located in the temporal-occipital regions of the brain versus smaller visual-olfactory structures in the frontal region. The olfactory bulbs of these adapiforms were small and blunt relative to endocranial volume and predicted body mass but uniquely, Adapis parisiensis had the largest olfactory bulbs, placing it within the range of extant strepsirrhines. These studies reveal how little is understood about primate paleoneurology and the evolutionary trends of different primate lineages with implications for the human fossil record.
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.