Platyrrhines (or New World Monkeys – NWM) inhabit South America and there are currently 5 families and 151 species, possessing traits not found in Catarrhines (Apes and Old World Monkeys of Africa and Asia). The NWM fossil record is fragmentary, with the earliest fossil specimens found in Argentina and dated to the middle Miocene (~ 22 million years ago), and more recent fossil remains found on the Caribbean islands and dated to the Late Pleistocene or early Holocene (~ 20-5 thousand years ago). The evolutionary relationships among living NWM and fossil species remain highly speculative. However, Woods et al. (2018) reported the successful recovery of ancient DNA from a Jamaican fossil species Xenothrix, closely related to living species of the Callicebinae, the Titi monkeys. The continuing uncertainty surrounding NWM evolutionary history has resulted in several Caribbean fossil NWM assigned as tentative ancestral species to living howler monkeys (genus Alouatta) based on similarities of highly prognathic faces, robust crania and smaller than expected brain size or endocranial volume (ECV).
A recent study by Halenar-Price & Tallman (2019) examined cranial shape and potential correlation with ECV in three Caribbean fossil and four living NWM genera. Patterns of cranial shape were determined for each living NWM species using geometric morphometrics and, once controlling for absolute size and phylogeny, the correlation with ECV was investigated using an encephalization quotient (EQ). Results from statistical tests for a correlation between cranial shape and brain size indicated no strong support for common trend for cranial shape describing the entire NWM clade, with the overall effect of cranial shape change in living NWM only slightly associated with brain size or ECV (less than 10%). Instead, cranial shape change was very species-specific, with species often differing in cranial width, cranial base flexion and globularity of the cranial vault. The howler monkeys had the lowest association between ECV and cranial shape, while the saki monkeys (genus Pithecia), showed greater links between ECV and cranial shape change associated with seed-eating diet and presence of cranial crests.
To examine fossil NWM and the role of encephalization on cranial shape, phylogeny was accommodated and fossil NWM added to the analyzes. Results indicated that Dominican Republic fossil NWM Antillothrix had a higher encephalization quotient (EQ) than living howler monkeys and was instead within range of titi monkeys (genus Callicebus), while Brazilian fossil NWM Cartelles was within the range of living howler monkeys. However, the Cuban fossil NWM Paralouatta was below the range of living howler monkeys. This study highlighted that the combined presence of facial prognathism, robust cranial form and smaller than expected brain size in NWM was strongly influenced by species-specific patterns related to diet, physiological and ecological adaptations, where, in very generalized terms, similarities between fossil and living new world monkeys do not necessarily indicate shared evolutionary associations.
Here a recent study on the cranial morphology of howler monkeys, and an article on atelids and ethnozoology.
The gray mouse lemur (Microcebus murinus) is a small Madagascan primate, averaging 12 cm length and weighing between 60-120 grams. Despite the diminutive size, mouse lemurs are increasingly used in medical studies of Alzheimer’s disease and similar neurological disease processes found in humans. Mouse lemurs often live to 12 years or more in the wild, which combined with torpor (a form of short-term hibernation) may be associated with the longer lifespans. Considering mouse lemurs have prolonged lifespans, it is probably not surprising that they also experience age-related brain atrophy. Nadkarni et al. (2019) address the absence of a dedicated mouse lemur brain atlas through in-vivo MRI scanning 34 mouse lemurs, investigating age-related brain atrophy and the neuroanatomy of Microcebus murinus in a comparative context. Results showed that most of the cerebral cortex was affected with age-related brain atrophy including the primary visual cortex and, although the remainder of the primary sensory areas were unaffected by atrophy, an even higher amount of atrophy was found in the sub-cortical brain regions including the thalamus, hippocampus and amygdala. All previous studies of mouse lemur neuroanatomy have been conducted with histological atlases. However, Nadkarni and colleagues compared mouse lemur cerebral to cortical volumes using high-quality MRI, finding that contrary to histology studies, mouse lemurs had similar cortical to cerebral volume indices to other primate species and were not to be considered a “lesser primate” species as has been previously argued. The proportion of cerebral white matter was the highest in humans, before a continual decrease in macaques and smaller monkeys with the lowest white matter volumes observed in mouse lemurs. The trend for increasing white matter volumes in primates, culminating with the highest values in humans, has often been argued as necessary for reinforcing intra-cerebral connectivity, hypothesized as an important process in primate brain evolution.
Included with this study of mouse lemurs, Nadkarni and colleagues also produced an accompanying MRI in-vivo brain atlas which includes 120 labelled brain structures specific to Microcebus murinus which to-date, has been unavailable. The accessibility of a brain atlas specific for mouse lemurs removes the time-consuming process of manual MRI segmentation, allowing quick and direct comparison of brain regions with other primates for a comparative evolutionary context and in medical research for Alzheimer’s disease.
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.