What do brain endocasts tell us? A comparative analysis of the accuracy of sulcal identification by experts and perspectives in palaeoanthropology.

Palaeoneurology is a complex field as the object of study, the brain, does not fossilize. Studies rely therefore on the (brain) endocranial cast (often named endocast), the only available and reliable proxy for brain shape, size and details of surface. However, researchers debate whether or not specific marks found on endocasts correspond reliably to particular sulci and/or gyri of the brain that were imprinted in the braincase. The aim of this study is to measure the accuracy of sulcal identification through an experiment that reproduces the conditions that palaeoneurologists face when working with hominin endocasts. We asked 14 experts to manually identify well-known foldings in a proxy endocast that was obtained from an MRI of an actual in vivo Homo sapiens head. We observe clear differences in the results when comparing the non-corrected labels (the original labels proposed by each expert) with the corrected labels. This result illustrates that trying to reconstruct a sulcus following the very general known shape/position in the literature or from a mean specimen may induce a bias when looking at an endocast and trying to follow the marks observed there. We also observe that the identification of sulci appears to be better in the lower part of the endocast compared to the upper part. The results concerning specific anatomical traits have implications for highly debated topics in palaeoanthropology. Endocranial description of fossil specimens should in the future consider the variation in position and shape of sulci in addition to using models of mean brain shape. Moreover, it is clear from this study that researchers can perceive sulcal imprints with reasonably high accuracy, but their correct identification and labelling remains a challenge, particularly when dealing with extinct species for which we lack direct knowledge of the brain.

The evolution of human altriciality and brain development in comparative context.

Human newborns are considered altricial compared with other primates because they are relatively underdeveloped at birth. However, in a broader comparative context, other mammals are more altricial than humans. It has been proposed that altricial development evolved secondarily in humans due to obstetrical or metabolic constraints, and in association with increased brain plasticity. To explore this association, we used comparative data from 140 placental mammals to measure how altriciality evolved in humans and other species. We also estimated how changes in brain size and gestation length influenced the timing of neurodevelopment during hominin evolution. Based on our data, humans show the highest evolutionary rate to become more altricial (measured as the proportion of adult brain size at birth) across all placental mammals, but this results primarily from the pronounced postnatal enlargement of brain size rather than neonatal changes. In addition, we show that only a small number of neurodevelopmental events were shifted to the postnatal period during hominin evolution, and that they were primarily related to the myelination of certain brain pathways. These results indicate that the perception of human altriciality is mostly driven by postnatal changes, and they point to a possible association between the timing of myelination and human neuroplasticity.

From fossils to mind.

Fossil endocasts record features of brains from the past: size, shape, vasculature, and gyrification. These data, alongside experimental and comparative evidence, are needed to resolve questions about brain energetics, cognitive specializations, and developmental plasticity. Through the application of interdisciplinary techniques to the fossil record, paleoneurology has been leading major innovations. Neuroimaging is shedding light on fossil brain organization and behaviors. Inferences about the development and physiology of the brains of extinct species can be experimentally investigated through brain organoids and transgenic models based on ancient DNA. Phylogenetic comparative methods integrate data across species and associate genotypes to phenotypes, and brains to behaviors. Meanwhile, fossil and archeological discoveries continuously contribute new knowledge. Through cooperation, the scientific community can accelerate knowledge acquisition. Sharing digitized museum collections improves the availability of rare fossils and artifacts. Comparative neuroanatomical data are available through online databases, along with tools for their measurement and analysis. In the context of these advances, the paleoneurological record provides ample opportunity for future research. Biomedical and ecological sciences can benefit from paleoneurology's approach to understanding the mind as well as its novel research pipelines that establish connections between neuroanatomy, genes and behavior.

Facial asymmetry tracks genetic diversity among Gorilla subspecies.

Mountain gorillas are particularly inbred compared to other gorillas and even the most inbred human populations. As mountain gorilla skeletal material accumulated during the 1970s, researchers noted their pronounced facial asymmetry and hypothesized that it reflects a population-wide chewing side preference. However, asymmetry has also been linked to environmental and genetic stress in experimental models. Here, we examine facial asymmetry in 114 crania from three Gorilla subspecies using 3D geometric morphometrics. We measure fluctuating asymmetry (FA), defined as random deviations from perfect symmetry, and population-specific patterns of directional asymmetry (DA). Mountain gorillas, with a current population size of about 1000 individuals, have the highest degree of facial FA (explaining 17% of total facial shape variation), followed by Grauer gorillas (9%) and western lowland gorillas (6%), despite the latter experiencing the greatest ecological and dietary variability. DA, while significant in all three taxa, explains relatively less shape variation than FA does. Facial asymmetry correlates neither with tooth wear asymmetry nor increases with age in a mountain gorilla subsample, undermining the hypothesis that facial asymmetry is driven by chewing side preference. An examination of temporal trends shows that stress-induced developmental instability has increased over the last 100 years in these endangered apes.

Assessing complexity in hominid dental evolution: Fractal analysis of great ape and human molars.

OBJECTIVES: Molar crenulation is defined as the accessory pattern of grooves that appears on the occlusal surface of many mammalian molars. Although frequently used in the characterization of species, this trait is often assessed qualitatively, which poses unavoidable subjective biases. The objective of this study is to quantitatively test the variability in the expression of molar crenulation in primates and its association with molar size and diet. METHODS: The variability in the expression of molar crenulation in hominids (human, chimpanzee, gorilla, and orangutan) was assessed with fractal analysis using photographs of first, second and third upper and lower molars. After this, representative values for 29 primate species were used to evaluate the correlation between molar complexity, molar size, and diet using a phylogenetic generalized least squares regression. RESULTS: Results show that there are statistically significant differences in fractal dimensions across hominid species in all molars, with orangutan molars presenting higher values of occlusal complexity. Our results indicate that there is no significant association between molar complexity and molar size or diet. DISCUSSION: Our results show higher levels of occlusal complexity in orangutans, thus supporting previously published observations. Our analyses, however, do not indicate a clear association between molar complexity and molar size or diet, pointing to other factors as the major drivers of complexity. To our knowledge, our study is the first one to use fractal analysis to measure occlusal complexity in primates. Our results show that this approach is a rapid and cost-effective way to measure molar complexity.

The human remains from Axlor (Dima, Biscay, northern Iberian Peninsula).

OBJECTIVES: We provide the description and comparative analysis of all the human fossil remains found at Axlor during the excavations carried out by J. M. de Barandiarán from 1967 to 1974: a cranial vault fragment and seven teeth, five of which likely belonged to the same individual, although two are currently lost. Our goal is to describe in detail all these human remains and discuss both their taxonomic attribution and their stratigraphic context. MATERIALS AND METHODS: We describe external and internal anatomy, and use classic and geometric morphometrics. The teeth from Axlor are compared to Neandertals, Upper Paleolithic, and recent modern humans. RESULTS: Two teeth (a left dm2 , a left di1 ) and the parietal fragment show morphological features consistent with a Neandertal classification, and were found in an undisturbed Mousterian context. The remaining three teeth (plus the two lost ones), initially classified as Neandertals, show morphological features and a general size that are more compatible with their classification as modern humans. DISCUSSION: A left parietal fragment (Level VIII) from a single probably adult Neandertal individual was recovered during the old excavations performed by Barandiarán. Additionally, two different Neandertal children lost deciduous teeth during the formations of levels V (left di1 ) and IV (right dm2 ). In addition, a modern human individual is represented by five remains (two currently lost) from a complex stratigraphic setting. Some of the morphological features of these remains suggest that they may represent one of the scarce examples of Upper Paleolithic modern human remains in the northern Iberian Peninsula, which should be confirmed by direct dating.

Dental evolutionary rates and its implications for the Neanderthal-modern human divergence.

The origin of Neanderthal and modern human lineages is a matter of intense debate. DNA analyses have generally indicated that both lineages diverged during the middle period of the Middle Pleistocene, an inferred time that has strongly influenced interpretations of the hominin fossil record. This divergence time, however, is not compatible with the anatomical and genetic Neanderthal affinities observed in Middle Pleistocene hominins from Sima de los Huesos (Spain), which are dated to 430 thousand years (ka) ago. Drawing on quantitative analyses of dental evolutionary rates and Bayesian analyses of hominin phylogenetic relationships, I show that any divergence time between Neanderthals and modern humans younger than 800 ka ago would have entailed unexpectedly rapid dental evolution in early Neanderthals from Sima de los Huesos. These results support a pre-800 ka last common ancestor for Neanderthals and modern humans unless hitherto unexplained mechanisms sped up dental evolution in early Neanderthals.

Brain size and organization in the Middle Pleistocene hominins from Sima de los Huesos. Inferences from endocranial variation.

The Sima de los Huesos (SH) endocranial sample includes 16 complete or partial endocasts corresponding to European Middle Pleistocene hominins. Different anatomical and molecular studies have demonstrated that these hominins are phylogenetically related to Neanderthals, thus making them the earliest unquestionable representatives of the Neanderthal lineage. The description of endocranial variation in this population is fundamental to shedding light on the evolution of the Neanderthal brain. In this contribution, we analyze and describe endocranial variation in this sample, including aspects related to brain size (endocranial volume and encephalization) and brain organization (through qualitative descriptions and quantitative analyses). Our results indicate that the SH hominins show a transitional state between a primitive hominin endocranial configuration (which is found in Homo erectus and non-SH Middle Pleistocene Homo) and the derived configurations found in Neanderthals and modern humans, without a clear anticipation of classic Neanderthal endocranial traits. In comparison with other cranial and postcranial traits that show a fully Neanderthal or clear pre-Neanderthal condition in the SH collection, endocranial variation in these hominins is surprisingly primitive and shows no Neanderthal affinity. These results and the comparison with other cranial traits confirm that Neanderthals evolved in a mosaic fashion. Traits related to mastication (dental, facial and mandibular anatomy) led the Neanderthalization process, whereas neurocranial anatomy must have acquired a fully Neanderthal condition considerably later.

Isolated teeth from La Ferrassie: Reassessment of the old collections, new remains, and their implications.

OBJECTIVES: We provide the description and comparative analysis of six new teeth from the site of La Ferrassie. Our goal is to discuss their taxonomic attribution, and to provide an updated inventory of Neandertal and modern human remains from La Ferrassie in their associated archeological context. MATERIALS AND METHODS: We use external and internal anatomy, classic morphometrics, and geometric morphometrics. The teeth from La Ferrassie are compared to several samples of contemporary Neandertals and upper Paleolithic modern humans and to recent modern humans. RESULTS: Three specimens are classified as Neandertals, two as modern humans, and one remains unclassified. DISCUSSION: Based on the previously known fossil samples and the new teeth reported here, there are currently a minimum of four adult and five immature Neandertal individuals coming from the "Grand Abri" and a minimum of two modern human adult individuals: one from "Grand Abri" and one from "Grotte." It is noteworthy that the spatial distribution of the recovered Neandertal remains is not restricted to the area where the LF1-LF 8 were found but now covers the full extension of the excavated area. Moreover, while both Neandertal and modern human occupations have yielded isolated human remains, the partial-to-complete skeletons only belong to Neandertals. These considerations open new perspectives for the understanding of the occupation and use of the La Ferrassie site.

Heritability of Gray Matter Structural Covariation and Tool Use Skills in Chimpanzees (Pan troglodytes): A Source-Based Morphometry and Quantitative Genetic Analysis.

Nonhuman primates, and great apes in particular, possess a variety of cognitive abilities thought to underlie human brain and cognitive evolution, most notably, the manufacture and use of tools. In a relatively large sample (N = 226) of captive chimpanzees (Pan troglodytes) for whom pedigrees are well known, the overarching aim of the current study was to investigate the source of heritable variation in brain structure underlying tool use skills. Specifically, using source-based morphometry (SBM), a multivariate analysis of naturally occurring patterns of covariation in gray matter across the brain, we investigated (1) the genetic contributions to variation in SBM components, (2) sex and age effects for each component, and (3) phenotypic and genetic associations between SBM components and tool use skill. Results revealed important sex- and age-related differences across largely heritable SBM components and associations between structural covariation and tool use skill. Further, shared genetic mechanisms appear to account for a heritable link between variation in both the capacity to use tools and variation in morphology of the superior limb of the superior temporal sulcus and adjacent parietal cortex. Findings represent the first evidence of heritability of structural covariation in gray matter among nonhuman primates.

A cerebellar substrate for cognition evolved multiple times independently in mammals.

Given that complex behavior evolved multiple times independently in different lineages, a crucial question is whether these independent evolutionary events coincided with modifications to common neural systems. To test this question in mammals, we investigate the lateral cerebellum, a neurobiological system that is novel to mammals, and is associated with higher cognitive functions. We map the evolutionary diversification of the mammalian cerebellum and find that relative volumetric changes of the lateral cerebellar hemispheres (independent of cerebellar size) are correlated with measures of domain-general cognition in primates, and are characterized by a combination of parallel and convergent shifts towards similar levels of expansion in distantly related mammalian lineages. Results suggest that multiple independent evolutionary occurrences of increased behavioral complexity in mammals may at least partly be explained by selection on a common neural system, the cerebellum, which may have been subject to multiple independent neurodevelopmental remodeling events during mammalian evolution.

Morphological integration in the gorilla, chimpanzee, and human neck.

OBJECTIVES: Although integration studies are important to understand the evolution of organisms' traits across phylogenies, vertebral integration in primates is still largely unexplored. Here we describe and quantify patterns of morphological integration and modularity in the subaxial cervical vertebrae (C3-C7) in extant hominines incorporating the potential influence of size. MATERIALS AND METHODS: Three-dimensional landmarks were digitized on 546 subaxial cervical vertebrae from 141 adult individuals of Gorilla gorilla, Pan troglodytes, and Homo sapiens. Integration and modularity, and the influence of size effects, were quantified using geometric morphometric approaches. RESULTS: All subaxial cervical vertebrae from the three species show a strong degree of integration. Gorillas show the highest degree of integration; conversely, humans have the lowest degree of integration. Analyses of allometric regression residuals show that size is an important factor promoting integration in gorillas, with lesser influence in chimpanzees and almost no effect in humans. DISCUSSION: Results point to a likely ancestral pattern of integration in non-human hominines, whereby the degree of integration decreases from cranial to caudal positions. Humans deviate from this pattern in the cranialmost (C3) and, to a lesser extent, in the caudalmost (C7) vertebrae, which are less integrated. These differences can be tentatively related to the emergence of bipedalism due to the presence of modern human-like C3 in australopiths, which still preserve a more chimpanzee-like C7.

How Primate Brains Vary and Evolve.

Studies of brain evolution tend to focus on differences across species rather than on variation within species. A new study measures and compares intraspecific variation in macaque and human brain anatomy to explore the effect that short-term diversity has on long-term evolution.

The Late Neandertal permanent lower left third premolar from Walou Cave (Trooz, Belgium) and its context.

OBJECTIVES: We describe a hominin permanent lower left third premolar unearthed in 1997 at Walou Cave (Belgium), found in direct association with a Mousterian lithic industry, in a layer directly dated to 40-38,000 years BP. MATERIALS AND METHODS: The taxonomical attribution of the tooth is addressed through comparative morphometric analyses, and stable isotope analyses aimed at determining the diet of the individual. RESULTS: The Walou P3 plots within the Neandertal range of variation and is significantly different from recent modern humans in all morphometric assessments. The isotope data showed that like other Neandertals, the Walou individual acquired its dietary proteins primarily from terrestrial food sources. DISCUSSION: We discuss the implications of the existence of a clearly Neandertal premolar dating to the period of the Middle to Upper Paleolithic transition in the Meuse river basin.

Exceptional Evolutionary Expansion of Prefrontal Cortex in Great Apes and Humans.

One of the enduring questions that has driven neuroscientific enquiry in the last century has been the nature of differences in the prefrontal cortex of humans versus other animals [1]. The prefrontal cortex has drawn particular interest due to its role in a range of evolutionarily specialized cognitive capacities such as language [2], imagination [3], and complex decision making [4]. Both cytoarchitectonic [5] and comparative neuroimaging [6] studies have converged on the conclusion that the proportion of prefrontal cortex in the human brain is greatly increased relative to that of other primates. However, considering the tremendous overall expansion of the neocortex in human evolution, it has proven difficult to ascertain whether this extent of prefrontal enlargement follows general allometric growth patterns, or whether it is exceptional [1]. Species' adherence to a common allometric relationship suggests conservation through phenotypic integration, while species' deviations point toward the occurrence of shifts in genetic and/or developmental mechanisms. Here we investigate prefrontal cortex scaling across anthropoid primates and find that great ape and human prefrontal cortex expansion are non-allometrically derived features of cortical organization. This result aligns with evidence for a developmental heterochronic shift in human prefrontal growth [7, 8], suggesting an association between neurodevelopmental changes and cortical organization on a macroevolutionary scale. The evolutionary origin of non-allometric prefrontal enlargement is estimated to lie at the root of great apes (∼19-15 mya), indicating that selection for changes in executive cognitive functions characterized both great ape and human cortical organization.

Brain enlargement and dental reduction were not linked in hominin evolution.

The large brain and small postcanine teeth of modern humans are among our most distinctive features, and trends in their evolution are well studied within the hominin clade. Classic accounts hypothesize that larger brains and smaller teeth coevolved because behavioral changes associated with increased brain size allowed a subsequent dental reduction. However, recent studies have found mismatches between trends in brain enlargement and posterior tooth size reduction in some hominin species. We use a multiple-variance Brownian motion approach in association with evolutionary simulations to measure the tempo and mode of the evolution of endocranial and dental size and shape within the hominin clade. We show that hominin postcanine teeth have evolved at a relatively consistent neutral rate, whereas brain size evolved at comparatively more heterogeneous rates that cannot be explained by a neutral model, with rapid pulses in the branches leading to later Homo species. Brain reorganization shows evidence of elevated rates only much later in hominin evolution, suggesting that fast-evolving traits such as the acquisition of a globular shape may be the result of direct or indirect selection for functional or structural traits typical of modern humans.

Gradients in cytoarchitectural landscapes of the isocortex: Diprotodont marsupials in comparison to eutherian mammals.

Although it has been claimed that marsupials possess a lower density of isocortical neurons compared with other mammals, little is known about cross-cortical variation in neuron distributions in this diverse taxonomic group. We quantified upper-layer (layers II-IV) and lower-layer (layers V-VI) neuron numbers per unit of cortical surface area in three diprotodont marsupial species (two macropodiformes, the red kangaroo and the parma wallaby, and a vombatiform, the koala) and compared these results to eutherian mammals (e.g., xenarthrans, rodents, primates). In contrast to the notion that the marsupial isocortex contains a low density of neurons, we found that neuron numbers per unit of cortical surface area in several marsupial species overlap with those found in eutherian mammals. Furthermore, neuron numbers vary systematically across the isocortex of the marsupial mammals examined. Neuron numbers under a unit of cortical surface area are low toward the frontal cortex and high toward the caudo-medial (occipital) pole. Upper-layer neurons (i.e., layers II-IV) account for most of the variation in neuron numbers across the isocortex. The variation in neuron numbers across the rostral to the caudal pole resembles primates. These findings suggest that diprotodont marsupials and eutherian mammals share a similar cortical architecture despite their distant evolutionary divergence.

The heritability of chimpanzee and human brain asymmetry.

Human brains are markedly asymmetric in structure and lateralized in function, which suggests a relationship between these two properties. The brains of other closely related primates, such as chimpanzees, show similar patterns of asymmetry, but to a lesser degree, indicating an increase in anatomical and functional asymmetry during hominin evolution. We analysed the heritability of cerebral asymmetry in chimpanzees and humans using classic morphometrics, geometric morphometrics, and quantitative genetic techniques. In our analyses, we separated directional asymmetry and fluctuating asymmetry (FA), which is indicative of environmental influences during development. We show that directional patterns of asymmetry, those that are consistently present in most individuals in a population, do not have significant heritability when measured through simple linear metrics, but they have marginally significant heritability in humans when assessed through three-dimensional configurations of landmarks that reflect variation in the size, position, and orientation of different cortical regions with respect to each other. Furthermore, genetic correlations between left and right hemispheres are substantially lower in humans than in chimpanzees, which points to a relatively stronger environmental influence on left-right differences in humans. We also show that the level of FA has significant heritability in both species in some regions of the cerebral cortex. This suggests that brain responsiveness to environmental influences, which may reflect neural plasticity, has genetic bases in both species. These results have implications for the evolvability of brain asymmetry and plasticity among humans and our close relatives.