Assessing the status of the KNM-ER 42700 fossil using Homo erectus neurocranial development.

Based on ontogenetic data of endocranial shape, it has been proposed that a younger than previously assumed developmental status of the 1.5-Myr-old KNM-ER 42700 calvaria could explain why the calvaria of this fossil does not conform to the shape of other Homo erectus individuals. Here, we investigate (ecto)neurocranial ontogeny in H. erectus and assess the proposed juvenile status of this fossil using recent Homo sapiens, chimpanzees (Pan troglodytes), and Neanderthals (Homo neanderthalensis) to model and discuss changes in neurocranial shape from the juvenile to adult stages. We show that all four species share common patterns of developmental shape change resulting in a relatively lower cranial vault and expanded supraorbital torus at later developmental stages. This finding suggests that ectoneurocranial data from extant hominids can be used to model the ontogenetic trajectory for H. erectus, for which only one well-preserved very young individual is known. However, our study also reveals differences in the magnitudes and, to a lesser extent, directions of the species-specific trajectories that add to the overall shared pattern of neurocranial shape changes. We demonstrate that the very young H. erectus juvenile from Mojokerto together with subadult and adult H. erectus individuals cannot be accommodated within the pattern of the postnatal neurocranial trajectory for humans. Instead, the chimpanzee pattern might be a better 'fit' for H. erectus despite their more distant phylogenetic relatedness. The data are also compatible with an ontogenetic shape trajectory that is in some regards intermediate between that of recent H. sapiens and chimpanzees, implying a unique trajectory for H. erectus that combines elements of both extant species. Based on this new knowledge, neurocranial shape supports the assessment that KNM-ER 42700 is a young juvenile H. erectus if H. erectus followed an ontogenetic shape trajectory that was more similar to chimpanzees than humans.

Early life of Neanderthals.

The early onset of weaning in modern humans has been linked to the high nutritional demand of brain development that is intimately connected with infant physiology and growth rate. In Neanderthals, ontogenetic patterns in early life are still debated, with some studies suggesting an accelerated development and others indicating only subtle differences vs. modern humans. Here we report the onset of weaning and rates of enamel growth using an unprecedented sample set of three late (∼70 to 50 ka) Neanderthals and one Upper Paleolithic modern human from northeastern Italy via spatially resolved chemical/isotopic analyses and histomorphometry of deciduous teeth. Our results reveal that the modern human nursing strategy, with onset of weaning at 5 to 6 mo, was present among these Neanderthals. This evidence, combined with dental development akin to modern humans, highlights their similar metabolic constraints during early life and excludes late weaning as a factor contributing to Neanderthals' demise.

The study of the lower limb entheses in the Neanderthal sample from El Sidrón (Asturias, Spain): How much musculoskeletal variability did Neanderthals accumulate?

Entheses have rarely been systematically studied in the field of human evolution. However, the investigation of their morphological variability (e.g., robusticity) could provide new insight into their evolutionary significance in the European Neanderthal populations. The aim of this work is to study the entheses and joint features of the lower limbs of El Sidrón Neanderthals (Spain; 49 ka), using standardized scoring methods developed on modern samples. Paleobiology, growth, and development of both juveniles and adults from El Sidrón are studied and compared with those of Krapina Neanderthals (Croatia, 130 ka) and extant humans. The morphological patterns of the gluteus maximus and vastus intermedius entheses in El Sidrón, Krapina, and modern humans differ from one another. Both Neanderthal groups show a definite enthesis design for the gluteus maximus, with little intrapopulation variability with respect to modern humans, who are characterized by a wider range of morphological variability. The gluteus maximus enthesis in the El Sidrón sample shows the osseous features of fibrous entheses, as in modern humans, whereas the Krapina sample shows the aspects of fibrocartilaginous ones. The morphology and anatomical pattern of this enthesis has already been established during growth in all three human groups. One of two and three of five adult femurs from El Sidrón and from Krapina, respectively, show the imprint of the vastus intermedius, which is absent among juveniles from those Neanderthal samples and in modern samples. The scant intrapopulation and the high interpopulation variability in the two Neanderthal samples is likely due to a long-term history of small, isolated populations with high levels of inbreeding, who also lived in different ecological conditions. The comparison of different anatomical entheseal patterns (fibrous vs. fibrocartilaginous) in the Neanderthals and modern humans provides additional elements in the discussion of their functional and genetic origin.

The deciduous dentition of Homo naledi: A comparative study.

In 2013, 2014 new hominin remains were uncovered in the Dinaledi chamber of the Rising Star cave system in South Africa. In 2015 Berger and colleagues identified these remains as belonging to a new species Homo naledi (Berger et al., 2015). Subsequent comparative studies of the skull, postcrania and permanent dentition have supported this taxonomic affiliation (Harcourt-Smith et al., 2015; Kivell et al., 2015; Irish et al., 2018). The deciduous teeth can offer unique insights into hominin evolution. Due to their early onset and rapid development their morphology is thought to be under stronger genetic control and less influenced by environment than are the permanent teeth. In this study we compared the H. naledi deciduous teeth from the 2013-2014 excavations to samples representing much of the hominin clade including Australopithecus afarensis, Australopithecus africanus, Paranthropus boisei, Paranthropus robustus, early Homo, Homo antecessor, Homo erectus s.l., Homo floresiensis, Middle Pleistocene Homo, Homo neanderthalensis, early Homo sapiens and recent H. sapiens from Sub-Saharan Africa. By making such a broad morphological comparison, we aimed to contextualize the Dinaledi hominins and to further assess the validity of their taxonomic assignment. Our analysis of the deciduous teeth revealed a unique combination of features that mirror (but also expand) that found in the permanent teeth. This mosaic includes an asymmetrical lower canine with a distal tubercle, an upper first molar with a large hypocone and epicrista associated with a mesial cuspule, a molarized lower first molar resembling Paranthropus, and upper and lower second molars that resemble later Homo in their lack of accessory cusps. The unique combination of deciduous dental characters supports previous studies assigning H. naledi to a new species, although its phylogenetic position vis-à-vis other Homo species remains ambiguous.

Mandibular ramus shape variation and ontogeny in Homo sapiens and Homo neanderthalensis.

As the interface between the mandible and cranium, the mandibular ramus is functionally significant and its morphology has been suggested to be informative for taxonomic and phylogenetic analyses. In primates, and particularly in great apes and humans, ramus morphology is highly variable, especially in the shape of the coronoid process and the relationship of the ramus to the alveolar margin. Here we compare ramus shape variation through ontogeny in Homo neanderthalensis to that of modern and fossil Homo sapiens using geometric morphometric analyses of two-dimensional semilandmarks and univariate measurements of ramus angulation and relative coronoid and condyle height. Results suggest that ramus, especially coronoid, morphology varies within and among subadult and adult modern human populations, with the Alaskan Inuit being particularly distinct. We also identify significant differences in overall anterosuperior ramus and coronoid shapes between H. sapiens and H. neanderthalensis, both in adults and throughout ontogeny. These shape differences are subtle, however, and we therefore suggest caution when using ramus morphology to diagnose group membership for individual specimens of these taxa. Furthermore, we argue that these morphologies are unlikely to be representative of differences in masticatory biomechanics and/or paramasticatory behaviors between Neanderthals and modern humans, as has been suggested by previous authors. Assessments of ontogenetic patterns of shape change reveal that the typical Neanderthal ramus morphology is established early in ontogeny, and there is little evidence for divergent postnatal ontogenetic allometric trajectories between Neanderthals and modern humans as a whole. This analysis informs our understanding of intraspecific patterns of mandibular shape variation and ontogeny in H. sapiens and can shed further light on overall developmental and life history differences between H. sapiens and H. neanderthalensis.

The growth pattern of Neandertals, reconstructed from a juvenile skeleton from El Sidrón (Spain).

Ontogenetic studies help us understand the processes of evolutionary change. Previous studies on Neandertals have focused mainly on dental development and inferred an accelerated pace of general growth. We report on a juvenile partial skeleton (El Sidrón J1) preserving cranio-dental and postcranial remains. We used dental histology to estimate the age at death to be 7.7 years. Maturation of most elements fell within the expected range of modern humans at this age. The exceptions were the atlas and mid-thoracic vertebrae, which remained at the 5- to 6-year stage of development. Furthermore, endocranial features suggest that brain growth was not yet completed. The vertebral maturation pattern and extended brain growth most likely reflect Neandertal physiology and ontogenetic energy constraints rather than any fundamental difference in the overall pace of growth in this extinct human.

An analysis of dental development in Pleistocene Homo using skeletal growth and chronological age.

OBJECTIVES: This study takes a new approach to interpreting dental development in Pleistocene Homo in comparison with recent modern humans. As rates of dental development and skeletal growth are correlated given age in modern humans, using age and skeletal growth in tandem yields more accurate dental development estimates. Here, I apply these models to fossil Homo to obtain more individualized predictions and interpretations of their dental development relative to recent modern humans. MATERIALS AND METHODS: Proportional odds logistic regression models based on three recent modern human samples (N = 181) were used to predict permanent mandibular tooth development scores in five Pleistocene subadults: Homo erectus/ergaster, Neanderthals, and anatomically modern humans (AMHs). Explanatory variables include a skeletal growth indicator (i.e., diaphyseal femoral length), and chronological age. RESULTS: AMHs Lagar Velho 1 and Qafzeh 10 share delayed incisor development, but exhibit considerable idiosyncratic variation within and across tooth types, relative to each other and to the reference samples. Neanderthals Dederiyeh 1 and Le Moustier 1 exhibit delayed incisor coupled with advanced molar development, but differences are reduced when femoral diaphysis length is considered. Dental development in KNM-WT 15,000 Homo erectus/ergaster, while advanced for his age, almost exactly matches the predictions once femoral length is included in the models. DISCUSSION: This study provides a new interpretation of dental development in KNM-WT 15000 as primarily reflecting his faster rates of skeletal growth. While the two AMH specimens exhibit considerable individual variation, the Neanderthals exhibit delayed incisor development early and advanced molar development later in ontogeny.

Brain development is similar in Neanderthals and modern humans.

While the braincase of adult Neanderthals had a similar volume to that of modern humans from the same period, differences in endocranial shape suggest that brain morphology differed between modern humans and Neanderthals. When and how these differences arose during evolution and development is a topic of ongoing research, with potential implications for species-specific differences in brain and cognitive development, and in life history [1,2]. Earlier research suggested that Neanderthals followed an ancestral mode of brain development, similar to that of our closest living relatives, the chimpanzees [2-4]. Modern humans, by contrast, were suggested to follow a uniquely derived mode of brain development just after birth, giving rise to the characteristically globular shape of the adult human brain case [2,4,5]. Here, we re-examine this hypothesis using an extended sample of Neanderthal infants. We document endocranial development during the decisive first two years of postnatal life. The new data indicate that Neanderthals followed largely similar modes of endocranial development to modern humans. These findings challenge the notion that human brain and cognitive development after birth is uniquely derived [2,4].

Neandertal growth: what are the costs?

Energetic approaches have been increasingly used to address key issues in Neandertal palaeoecology and palaeobiology. Previous research has focused exclusively on the energy requirements of adults and highlights the high energy demands of these individuals compared with modern humans. Less attention has been paid to the energy requirements of sub-adult Neandertals, even though this age group could provide clues for a better understanding of Neandertal life history. Accordingly, herein, we estimate the energy costs of maintenance and growth in Neandertal infants and children from one to six years of age and compare these costs with values for modern humans. Statural growth models for two modern human populations (Beasain and Evenki) and an average Neandertal model population are used to establish weight growth models. In turn, these models of body weight growth are used to estimate key components of energetic variables (basal metabolic rate, total energy expenditure, energy of growth and daily energy requirements). Between three and six years of age, Neandertal children have slightly lower basal and growth energy costs than do modern humans of the same age, due primarily to their smaller body mass and slower growth rates. The reduction in energy allocated to growth is likely the result of metabolic adaptations to other somatic factors and thermal stress. Data from contemporary human infants and children suggest that even mild cold stress increases non-shivering thermogenesis, thus elevating metabolic needs by 50% or more. These results suggest that thermal stress likely played a strong role in shaping the delayed developmental patterns and lower energy allocated to growth during early life in Neandertals relative to Homo sapiens.

In search of our direct ancestor an anthropological and orthodontic summary.

This paper reviews the development of human facial anatomy in H Erectus, Neanderthal and modern man. Modern orthodontic measurements are used to compare different jaw size and relationships.

New information on the modifications of the Neandertal suprainiac fossa during growth and development and on its etiology.

The question of whether suprainiac depressions observed on Neandertals and in other human samples are homologous is widely discussed. Recently (Balzeau and Rougier, 2010), we ascertained the autapomorphic status of the Neandertal suprainiac fossa as a depression showing specific external bone features together with a thinning of the diploic layer with no substantial remodeling nor variation in the external table thickness. A suprainiac fossa with these characteristics is systematically present on Neandertals from the earliest developmental stages on, and since the beginning of the differentiation of the Neandertal lineage. Here, we present a detailed analysis of the micro-CT dataset (resolution of 50 µm) of the occipital bone of the La Ferrassie 8 Neandertal child, whose proposed age-at-death is around 2 years, and we compare it to the adult condition as represented by La Chapelle-aux-Saints 1 (resolution of 122 µm). We describe and quantify the boundaries between the different structural layers of the occipital bone, namely the external and internal tables and the diploic layer. We also describe very fine details of the diploic layer structure that had never before been observed on fossil hominins. This study illustrates for the first time that the internal particularities that make the suprainiac fossa a Neandertal autapomorphy are evident early during growth and development. Moreover, we demonstrate that the developmental pattern and causes of expression for the features observed in modern humans and Neandertals are certainly different, indicating that these features are not homologous traits from evolutionary and functional perspectives. Consequently, we confirm the autapomorphic status of the Neandertal suprainiac fossa.

Reassessment of the La Ferrassie 3 Neandertal ossicular chain.

The ossicular chain in La Ferrassie 3 was briefly described in the monograph on the La Ferrassie Neandertal children, but to date has not been the subject of detailed study. We provide new data on these important fossils and re-examine some previous suggestions of derived Neandertal features in the middle ear ossicles based on more limited evidence. The malleus shows a curved lateral margin of the manubrium and a relatively large head. The incus shows a tall articular facet, a depressed area on the medial surface of the body, a straight anterior border of the long process and a more closed angle between the processes. The stapes shows an asymmetrical configuration of the crura, with an anteriorly skewed head, and generally small dimensions, including a smaller and relatively wider stapedial footplate. These same features can also be seen in the few other Neandertal ear ossicles known, suggesting that a consistent anatomical pattern characterizes the Neandertal ossicular chain. While the phylogenetic polarity of many of these features remains to be clarified, the asymmetrical stapes and anteriorly skewed stapedial head appear to be derived Neandertal features. In addition, while the larger malleus head and incus articular facet in La Ferrassie 3 might reflect larger body mass in Neandertals, the larger stapes footplates in Homo sapiens cannot be explained by changes in body mass. Indeed, H. sapiens seems to depart from the general mammalian pattern in combining an increase in stapes footplate size with a decrease in body mass. Although the malleus/incus lever ratio in La Ferrassie 3 is similar to that in H. sapiens, Neandertals appear to be characterized by a slightly different spatial relationship and articulation of the ossicular chain within the tympanic cavity. While only limited inferences can be drawn regarding hearing ability based on the ossicles, the few physiologically relevant dimensions in the La Ferrassie 3 ear bones are similar to H. sapiens.

Differences between Neandertal and modern human infant and child growth models.

Studying the emergence of distinctive human growth patterns is essential to understanding the evolution of our species. The large number of Neandertal fossils makes this species the best candidate for a comparative study of growth patterns in archaic and modern humans. Here, Neandertal height growth during infancy and early childhood is described using a mathematical model. Height growth velocities for individuals five years old or younger are modelled as age functions based on different estimates of height and age for a set of ten Neandertal infants and children. The estimated heights of each Neandertal individual are compared with those of two modern human populations based on longitudinal and cross-sectional data. The model highlights differences in growth velocity during infancy (from the age of five months onward). We find that statural growth in Neandertal infants is much slower than that seen in modern humans, Neandertal growth is similar to modern humans at birth, but decreases around the third or fourth month. The markedly slower growth rates of Neandertal infants may be attributable to ontogenetic constraints or to metabolic stress, and contribute to short achieved adult stature relative to modern humans.

A uniquely modern human pattern of endocranial development. Insights from a new cranial reconstruction of the Neandertal newborn from Mezmaiskaya.

The globular braincase of modern humans is distinct from all fossil human species, including our closest extinct relatives, the Neandertals. Such adult shape differences must ultimately be rooted in different developmental patterns, but it is unclear at which point during ontogeny these group characteristics emerge. Here we compared internal shape changes of the braincase from birth to adulthood in Neandertals (N = 10), modern humans (N = 62), and chimpanzees (N = 62). Incomplete fossil specimens, including the two Neandertal newborns from Le Moustier 2 and Mezmaiskaya, were reconstructed using reference-based estimation methods. We used 3D geometric morphometrics to statistically compare shapes of virtual endocasts extracted from computed-tomographic scans. Throughout the analysis, we kept track of possible uncertainties due to the missing data values and small fossil sample sizes. We find that some aspects of endocranial development are shared by the three species. However, in the first year of life, modern humans depart from this presumably ancestral pattern of development. Newborn Neandertals and newborn modern humans have elongated braincases, and similar endocranial volumes. During a 'globularization-phase' modern human endocasts change to the globular shape that is characteristic for Homo sapiens. This phase of early development is unique to modern humans, and absent from chimpanzees and Neandertals. Our results support the notion that Neandertals and modern humans reach comparable adult brain sizes via different developmental pathways. The differences between these two human groups are most prominent directly after birth, a critical phase for cognitive development.

Virtual neanderthals.

Our closest hominid relatives may have died out 30,000 years before the arrival of the computer, but thanks to modern genomics and scanning technology, they are now very present in the 21st century and can even help us understand our own species.