Emmanuel Gilissen

Next-Generation Museomics Disentangles One of the Largest Primate Radiations

Guenons (tribe Cercopithecini) are one of the most diverse groups of primates. They occupy all of sub-Saharan Africa and show great variation in ecology, behavior, and morphology. This variation led to the description of over 60 species and subspecies. Here, using next-generation DNA sequencing (NGS) in combination with targeted DNA capture, we sequenced 92 mitochondrial genomes from museum-preserved specimens as old as 117 years. We infer evolutionary relationships and estimate divergence times of almost all guenon taxa based on mitochondrial genome sequences. Using this phylogenetic framework, we infer divergence dates and reconstruct ancestral geographic ranges. We conclude that the extraordinary radiation of guenons has been a complex process driven by, among other factors, localized fluctuations of African forest cover. We find incongruences between phylogenetic trees reconstructed from mitochondrial and nuclear DNA sequences, which can be explained by either incomplete lineage sorting or hybridization. Furthermore, having produced the largest mitochondrial DNA data set from museum specimens, we document how NGS technologies can “unlock” museum collections, thereby helping to unravel the tree-of-life. [Museum collection; next-generation DNA sequencing; primate radiation; speciation; target capture.]

Evolution of Specialized Pyramidal Neurons in Primate Visual and Motor Cortex

The neocortex of primates contains several distinct neuron subtypes. Among these, Betz cells of primary motor cortex and Meynert cells of primary visual cortex are of particular interest for their potential role in specialized sensorimotor adaptations of primates. Betz cells are involved in setting muscle tone prior to fine motor output and Meynert cells participate in the processing of visual motion. We measured the soma volumes of Betz cells, Meynert cells, and adjacent infragranular pyramidal neurons in 23 species of primate and two species of non-primate mammal (Tupaia glis and Pteropus poliocephalus) using unbiased stereological techniques to examine their allometric scaling relationships and socioecological correlations. Results show that Betz somata become proportionally larger with increases in body weight, brain weight, and encephalization whereas Meynert somata remain a constant proportion larger than other visual pyramidal cells. Phylogenetic variance in the volumetric scaling of these neuronal subtypes might be related to species-specific adaptations. Enlargement of Meynert cells in terrestrial anthropoids living in open habitats, for example, might serve as an anatomical substrate for predator detection. Modification of the connectional and physiological properties of these neurons could constitute an important evolutionary mode for species-specific adaptation.

Shared pattern of endocranial shape asymmetries among great apes, anatomically modern humans, and fossil hominins.

Anatomical asymmetries of the human brain are a topic of major interest because of their link with handedness and cognitive functions. Their emergence and occurrence have been extensively explored in human fossil records to document the evolution of brain capacities and behaviour. We quantified for the first time antero-posterior endocranial shape asymmetries in large samples of great apes, modern humans and fossil hominins through analysis of “virtual” 3D models of skull and endocranial cavity and we statistically test for departures from symmetry. Once based on continuous variables, we show that the analysis of these brain asymmetries gives original results that build upon previous analysis based on discrete traits. In particular, it emerges that the degree of petalial asymmetries differs between great apes and hominins without modification of their pattern. We indeed demonstrate the presence of shape asymmetries in great apes, with a pattern similar to modern humans but with a lower variation and a lower degree of fluctuating asymmetry. More importantly, variations in the position of the frontal and occipital poles on the right and left hemispheres would be expected to show some degree of antisymmetry when population distribution is considered, but the observed pattern of variation among the samples is related to fluctuating asymmetry for most of the components of the petalias. Moreover, the presence of a common pattern of significant directional asymmetry for two components of the petalias in hominids implicates that the observed traits were probably inherited from the last common ancestor of extant African great apes and Homo sapiens. These results also have important implications for the possible relationships between endocranial shape asymmetries and functional capacities in hominins. It emphasizes the uncoupling between lateralized activities, some of them well probably distinctive to Homo, and large-scale cerebral lateralization itself, which is not unique to Homo.

Endocranial shape asymmetries in Pan paniscus, Pan troglodytes and Gorilla gorilla assessed via skull based landmark analysis.

Brain shape asymmetries or petalias consist of the extension of one cerebral hemisphere beyond the other. A larger frontal or caudal projection is usually coupled with a larger lateral extent of the more projecting hemisphere relative to the other. The concurrence of these petalial components is characteristic of hominins. Studies aimed at quantifying petalial asymmetries in human and great ape endocasts rely on the definition of the midline of the endocranial surface. Studies of brain material show that, at least in humans, most of the medial surface of the left occipital lobe distorts along the midline and protrudes on to the right side, making it difficult for midline and corresponding left and right reference point identification. In order to accurately quantify and compare brain shape asymmetries in extant hominid species, we propose here a new protocol based on the objective definition of cranial landmarks. We describe and quantify for the first time in three dimensions the positions of frontal and occipital protrusions in large samples of Pan paniscus, Pan troglodytes and Gorilla gorilla. This study confirms the existence of frontal and occipital petalias in African apes. Moreover, the detailed analysis of the 3D structure of these petalias reveals shared features, as well as features that are unique to the different great ape species.

Comparative Neuropathology of Brain Aging in Primates

aKastor Neurobiology of Aging Laboratories and Fishberg Research Center for Neurobiology, Departments of bGeriatrics and Adult Development, cRadiology, dOtolaryngology and ePathology, Mount Sinai School of Medicine, fDepartment of Anthropology, Columbia University, gNew York Consortium in Evolutionary Primatology, New York, N.Y., hDivision of Neurobiology, Behavior, and Genetics, Bioqual Inc., Rockville, Md., and iFoundation for Comparative and Conservation Biology, Rockville, Md., USA; jDepartment of Anatomical Sciences, University of the Witwatersrand, Parktown, South Africa

Assessing endocranial variations in great apes and humans using 3D data from virtual endocasts

Modern humans are characterized by their large, complex, and specialized brain. Human brain evolution can be addressed through direct evidence provided by fossil hominid endocasts (i.e. paleoneurology), or through indirect evidence of extant species comparative neurology. Here we use the second approach, providing an extant comparative framework for hominid paleoneurological studies. We explore endocranial size and shape differences among great apes and humans, as well as between sexes. We virtually extracted 72 endocasts, sampling all extant great ape species and modern humans, and digitized 37 landmarks on each for 3D generalized Procrustes analysis. All species can be differentiated by their endocranial shape. Among great apes, endocranial shapes vary from short (orangutans) to long (gorillas), perhaps in relation to different facial orientations. Endocranial shape differences among African apes are partly allometric. Major endocranial traits distinguishing humans from great apes are endocranial globularity, reflecting neurological reorganization, and features linked to structural responses to posture and bipedal locomotion. Human endocasts are also characterized by posterior location of foramina rotunda relative to optic canals, which could be correlated to lesser subnasal prognathism compared to living great apes. Species with larger brains (gorillas and humans) display greater sexual dimorphism in endocranial size, while sexual dimorphism in endocranial shape is restricted to gorillas, differences between males and females being at least partly due to allometry. Our study of endocranial variations in extant great apes and humans provides a new comparative dataset for studies of fossil hominid endocasts.

Cellular scaling rules for the brain of afrotherians

Quantitative analysis of the cellular composition of rodent, primate and eulipotyphlan brains has shown that non-neuronal scaling rules are similar across these mammalian orders that diverged about 95 million years ago, and therefore appear to be conserved in evolution, while neuronal scaling rules appear to be free to vary in evolution in a clade-specific manner. Here we analyze the cellular scaling rules that apply to the brain of afrotherians, believed to be the first clade to radiate from the common eutherian ancestor. We find that afrotherians share non-neuronal scaling rules with rodents, primates and eulipotyphlans, as well as the coordinated scaling of numbers of neurons in the cerebral cortex and cerebellum. Afrotherians share with rodents and eulipotyphlans, but not with primates, the scaling of number of neurons in the cortex and in the cerebellum as a function of the number of neurons in the rest of the brain. Afrotheria also share with rodents and eulipotyphlans the neuronal scaling rules that apply to the cerebral cortex. Afrotherians share with rodents, but not with eulipotyphlans nor primates, the neuronal scaling rules that apply to the cerebellum. Importantly, the scaling of the folding index of the cerebral cortex with the number of neurons in the cerebral cortex is not shared by either afrotherians, rodents, or primates. The sharing of some neuronal scaling rules between afrotherians and rodents, and of some additional features with eulipotyphlans and primates, raise the interesting possibility that these shared characteristics applied to the common eutherian ancestor. In turn, the clade-specific characteristics that relate to the distribution of neurons along the surface of the cerebral cortex and to its degree of gyrification suggest that these characteristics compose an evolutionarily plastic suite of features that may have defined and distinguished mammalian groups in evolution.

Cross-sectional area of the elephant corpus callosum: comparison to other eutherian mammals

The current study reports our findings of the relationship between cross-sectional area of the corpus callosum and brain mass in over 100 eutherian mammal species. We were specifically interested in determining whether the elephant had a corpus callosum the size that would be expected for eutherian mammal with a brain mass of approximately 5000 g, or whether a different morphology had evolved. To answer this question we first analysed data from primates, other eutherian mammals and cetaceans, finding that primates and other eutherian mammals showed a positive allometric relationship between the two variables, such that larger brains had a relatively larger corpus callosum. Interestingly, primates have a slightly larger corpus callosum than other eutherian mammals, but showed a similar allometric scaling to this group. The cetaceans had a both absolutely and relatively small corpus callosum compared to other mammals and showed isometric scaling with brain mass. The six elephants studied herein had the largest absolute corpus callosums recorded to date; however, relative to the mass of their brain, the size of the corpus callosum was what would be expected of a typical eutherian mammal with a brain mass of approximately 5000 g. The data for elephants hinted at sexual dimorphism in size of the corpus callosum, with female elephants having both an absolute and relatively larger callosum than the males. If this observation is supported in future studies, the elephants will be the first non-primate species to show sexual dimorphism in this neural character. The results are discussed in both an evolutionary and functional context.

Nuclear organisation of some immunohistochemically identifiable neural systems in three Afrotherian species—Potomogale velox, Amblysomus hottentotus and Petrodromus tetradactylus

The present study describes the organisation of the cholinergic, catecholaminergic, and serotonergic neurons in the brains of the giant otter shrew, the Hottentot golden mole and the four-toed sengi, and the orexinergic (hypocretinergic) system in the giant otter shrew and four-toed sengi. The aim of the present study was to investigate the possible differences in the nuclear complement of these neural systems in comparison to previous studies on other Afrotherian species and mammalian species in general. Brains of the golden mole, sengi and giant otter shrew were coronally sectioned and immunohistochemically stained with antibodies against cholineacetyl-transferase, tyrosine hydroxylase, serotonin and orexin-A. The majority of nuclei revealed in the current study were similar among the species investigated, to other Afrotherian species, and to mammals generally, but certain differences in the nuclear complement highlighted phylogenetic interrelationships. The golden mole was observed to have cholinergic interneurons in the cerebral cortex, hippocampus, olfactory bulb and amygdala. The four-toed sengi had cholinergic neurons in both colliculi and in the cochlear nucleus, but lacked the catecholaminergic A15d group in the hypothalamus. In both the golden mole and the four-toed sengi, the locus coeruleus (A6d group) was made up of few neurons. The golden mole also exhibited an unusual foreshortening of the brain, such that a major (mesencephalic?) flexure in the brainstem was evident.

Virtual endocranial cast of earliest Eocene Diacodexis (Artiodactyla, Mammalia) and morphological diversity of early artiodactyl brains

The study of brain evolution, particularly that of the neocortex, is of primary interest because it directly relates to how behavioural variations arose both between and within mammalian groups. Artiodactyla is one of the most diverse mammalian clades. However, the first 10 Myr of their brain evolution has remained undocumented so far. Here, we used high-resolution X-ray computed tomography to investigate the endocranial cast of Diacodexis ilicis of earliest Eocene age. Its virtual reconstruction provides unprecedented access to both metric parameters and fine anatomy of the most complete endocast of the earliest artiodactyl. This picture is assessed in a broad comparative context by reconstructing endocasts of 14 other Early and Middle Eocene representatives of basal artiodactyls, allowing the tracking of the neocortical structure of artiodactyls back to its simplest pattern. We show that the earliest artiodactyls share a simple neocortical pattern, so far never observed in other ungulates, with an almond-shaped gyrus instead of parallel sulci as previously hypothesized. Our results demonstrate that artiodactyls experienced a tardy pulse of encephalization during the Late Neogene, well after the onset of cortical complexity increase. Comparisons with Eocene perissodactyls show that the latter reached a high level of cortical complexity earlier than the artiodactyls.