Sex estimation of the adult Neandertal Regourdou 1 (Montignac, France): Implications for sexing human fossil remains.

Sex is a biological trait fundamental to the study of hominin fossils. Among the many questions that can be addressed are those related to taxonomy, biological variability, sexual dimorphism, paleoobstetrics, funerary selection, and paleodemography. While new methodologies such as paleogenomics or paleoproteomics can be used to determine sex, they have not been systematically applied to Pleistocene human remains due to their destructive nature. Therefore, we estimated sex from the coxal bone of the newly discovered pelvic remains of the Regourdou 1 Neandertal (Southwest France, MIS 5) based on morphological and metric data employing two methods that have been recently revised and shown to be reliable in multiple studies. Both methods calculate posterior probabilities of the estimate. The right coxal bone of Regourdou 1 was partially reconstructed providing additional traits for sex estimation. These methods were cross validated on 14 sufficiently preserved coxal bones of specimens from the Neandertal lineage. Our results show that the Regourdou 1 individual, whose postcranial skeleton is not robust, is a male, and that previous sex attributions of comparative Neandertal specimens are largely in agreement with those obtained here. Our results encourage additional morphological research of fossil hominins in order to develop a set of methods that are applicable, reliable, and reproducible.

Unraveling the Life History of Past Populations through Hypercementosis: Insights into Cementum Apposition Patterns and Possible Etiologies Using Micro-CT and Confocal Microscopy.

The "teeth-as-tools" hypothesis posits that Neanderthals used their anterior teeth as a tool or a third hand for non-dietary purposes. These non- or para-masticatory activities (e.g., tool-making or food preparation prior to ingestion) have also been described in other past and extant human populations, and other Primates. Cementum is the mineralized tissue that covers the tooth root surface and anchors it to the alveolar bone. Under certain conditions (e.g., mechanical stress, infection), its production becomes excessive (i.e., beyond the physiological state) and is called 'hypercementosis'. Several studies in dental anthropology have established a correlation between the teeth-as-tools and hypercementosis. The present work aims to characterize the different patterns of cementum apposition on archeological teeth and discuss their supposed etiology. Using microtomography and confocal microscopy, the patterns of cementum apposition (i.e., thickness, location, and surface characteristics) were analyzed in 35 hypercementotic teeth (Sains-en-Gohelle, France; 7th-17th c. A.D.). Four groups were identified with distinct hypercementosis patterns: (1) impacted, (2) infected, (3) hypofunctional, and (4) hyperfunctional teeth. Characterizing hypercementosis can contribute to documenting the oral health status (paleopathology) and/or masticatory activity of individuals, even from isolated teeth. This has implications for the study of fossil hominins, particularly Neanderthals, known for their use of anterior teeth as tools and frequent and substantial occurrence of hypercementosis.

Mousterian human fossils from El Castillo cave (Puente Viesgo, Cantabria, Spain).

El Castillo cave is a well-known site because of its Paleolithic archaeology and parietal rock art. This paper is focused on the human remains found by V. Cabrera in the Mousterian Unit XX assigned to MIS 4 and early MIS 3. The fossils consist of one upper left second premolar (ULP4), one incomplete proximal hand phalanx, and one partial femoral head. The tooth and the phalanx were assigned to adults, whereas the femoral head belonged to an immature individual due to the absence of fusion traces to the metaphyseal surface. The external morphology and metrical characterization of the Castillo-1466 (ULP4) tooth crown was quantified and compared to the variability of other Neanderthal dental remains and a sample of modern human populations. We also quantified its 3D enamel thickness distribution, its roots morphology, as well as the presence of chipping, and their possible relation to masticatory or paramasticatory activities. Castillo-1466 shows crown dimensions compatible with middle-sized Neanderthal teeth, but with a remarkably thicker enamel than other Neanderthal premolars, such as Marillac 13. The femoral head and the hand phalanx fragment are compared to published values for Neanderthals, although both partial fossils lack diagnostic features precluding any clear taxonomic diagnostic. Therefore, their attribution to Neanderthals is assumed based on the dating of the layers in which they were discovered. El Castillo cave Mousterian fossils represent another contribution to the knowledge of the Middle Paleolithic populations of Northern Spain, where different sites along the Cantabrian mountains yielded several human remains assigned to MIS 4 and early MIS 3.

Anatomically modern human in the Châtelperronian hominin collection from the Grotte du Renne (Arcy-sur-Cure, Northeast France).

Around 42,000 years ago, anatomically modern humans appeared in Western Europe to the detriment of indigenous Neanderthal groups. It is during this period that new techno-cultural complexes appear, such as the Châtelperronian that extends from northern Spain to the Paris Basin. The Grotte du Renne (Arcy-sur-Cure) is a key site for discussing the biological identity of its makers. This deposit has yielded several Neanderthal human remains in its Châtelperronian levels. However, the last inventory of the paleoanthropological collection attributed to this techno-complex allowed the identification of an ilium belonging to a neonate (AR-63) whose morphology required a thorough analysis to assess its taxonomic attribution. Using geometric morphometrics, we quantified its morphology and compared it to that of 2 Neanderthals and 32 recent individuals deceased during the perinatal period to explore their morphological variation. Our results indicate a morphological distinction between the ilia of Neanderthals and anatomically modern neonates. Although AR-63 is slightly outside recent variability, it clearly differs from the Neanderthals. We propose that this is due to its belonging to an early modern human lineage whose morphology differs slightly from present-day humans. We also explore different hypotheses about the presence of this anatomically modern neonate ilium among Neanderthal remains.

Palaeogenomics of Upper Palaeolithic to Neolithic European hunter-gatherers.

Modern humans have populated Europe for more than 45,000 years1,2. Our knowledge of the genetic relatedness and structure of ancient hunter-gatherers is however limited, owing to the scarceness and poor molecular preservation of human remains from that period3. Here we analyse 356 ancient hunter-gatherer genomes, including new genomic data for 116 individuals from 14 countries in western and central Eurasia, spanning between 35,000 and 5,000 years ago. We identify a genetic ancestry profile in individuals associated with Upper Palaeolithic Gravettian assemblages from western Europe that is distinct from contemporaneous groups related to this archaeological culture in central and southern Europe4, but resembles that of preceding individuals associated with the Aurignacian culture. This ancestry profile survived during the Last Glacial Maximum (25,000 to 19,000 years ago) in human populations from southwestern Europe associated with the Solutrean culture, and with the following Magdalenian culture that re-expanded northeastward after the Last Glacial Maximum. Conversely, we reveal a genetic turnover in southern Europe suggesting a local replacement of human groups around the time of the Last Glacial Maximum, accompanied by a north-to-south dispersal of populations associated with the Epigravettian culture. From at least 14,000 years ago, an ancestry related to this culture spread from the south across the rest of Europe, largely replacing the Magdalenian-associated gene pool. After a period of limited admixture that spanned the beginning of the Mesolithic, we find genetic interactions between western and eastern European hunter-gatherers, who were also characterized by marked differences in phenotypically relevant variants.

Hypercementosis in Late Pleistocene Homo sapiens fossils from Klasies River Main Site, South Africa.

OBJECTIVE: To examine early Homo sapiens fossils from the Late Pleistocene site of Klasies River Main Site, South Africa for evidence of hypercementosis. The specimens represent seven adult individuals dated to between 119,000 and 58,000 years ago. These observations are contextualized in relation to the incidences of hypercementosis among recent human populations and fossil human samples and the potential etiologies of hypercementosis. DESIGN: The fossils were investigated utilizing micro-CT and nano-CT scanning to visualize and measure cementum apposition on permanent incisor, premolar and molar roots. Cementum thickness was measured at mid-root level, and the volume of the cementum sleeve was calculated for the two fossil specimens that display marked hypercementosis. RESULTS: Two of the fossils display no evidence of cementum hypertrophy. Three exhibit moderate cementum thickening, barely attaining the quantitative threshold for hypercementosis. Two evince marked hypercementosis. One of the Klasies specimens with marked hypercementosis is judged to be an older individual with periapical abscessing. The second specimen is a younger adult, and seemingly similar in age to other Klasies fossils that exhibit only minimal cementum apposition. However, this second specimen exhibits dento-alveolar ankylosis of the premolar and molars. CONCLUSIONS: These two fossils from Klasies River Main Site provide the earliest manifestation of hypercementosis in Homo sapiens.

Insights into the aetiologies of hypercementosis: A systematic review and a scoring system.

OBJECTIVES: This paper aims to better define hypercementosis, investigate its described potential aetiologies, and determine whether there are different patterns of cementum apposition and if they are a function of their supposed aetiology. DESIGN: A literature review was undertaken using the Medline, DOSS, Scopus and Cochrane Library electronic databases. Two co-authors selected the published works independently, extracted the data in accordance with the PRISMA statement. RESULTS: Among 546 articles, 75 articles were finally selected. Eight different supposed aetiologies were identified: (1) intensive masticatory effort, (2) systemic disease, (3) carious lesion and apical periodontitis, (4) impaction, (5) periodontal disease, (6) concrescence, (7) super-eruption, and (8) drugs. Some of these aetiologies can be combined in the same tooth. Hypercementosis manifestations are various in nature and extent with different patterns that may be aetiology-specific. To improve the description and associated consistency in the characterisation of hypercementosis, in this review but also in future studies, we propose a new qualitative scoring system to quickly characterise hypercementosis and determine its most relevant aetiology. CONCLUSIONS: This systematic review demonstrates that hypercementosis is a complex and not yet well-defined condition. Some forms of apposition are specific to a given aetiology. The hypercementosis characterisation may contribute to document the oral condition and/or the individuals masticatory activity.

Dental Paleobiology in a Juvenile Neanderthal (Combe-Grenal, Southwestern France).

Combe-Grenal site (Southwest France) was excavated by F. Bordes between 1953 and 1965. He found several human remains in Mousterian levels 60, 39, 35 and especially 25, corresponding to MIS 4 (~75-70/60 ky BP) and with Quina Mousterian lithics. One of the fossils found in level 25 is Combe-Grenal IV, consisting of a fragment of the left corpus of a juvenile mandible. This fragment displays initial juvenile periodontitis, and the two preserved teeth (LLP4 and LLM1) show moderate attrition and dental calculus. The SEM tartar analysis demonstrates the presence of cocci and filamentous types of bacteria, the former being more prevalent. This result is quite different from those obtained for the two adult Neanderthals Kebara 2 and Subalyuk 1, where more filamentous bacteria appear, especially in the Subalyuk 1 sample from Central Europe. These findings agree with the available biomedical data on periodontitis and tartar development in extant individuals, despite the different environmental conditions and diets documented by numerous archeological, taphonomical and geological data available on Neanderthals and present-day populations. New metagenomic analyses are extending this information, and despite the inherent difficulties, they will open important perspectives in studying this ancient human pathology.

Isotopic calcium biogeochemistry of MIS 5 fossil vertebrate bones: application to the study of the dietary reconstruction of Regourdou 1 Neandertal fossil.

The calcium isotopic composition (δ44/42Ca) of bone and tooth enamel can be used for dietary reconstructions of extant and extinct mammals. In natural conditions, the δ44/42Ca value of bone and teeth varies according to dietary intake with a constant isotopic offset of about -0.6‰. Owing to the poor conservation of collagen, carbon (C), and nitrogen (N) isotopic compositions of the Regourdou Mousterian site (MIS 5, Dordogne, France) previously failed to provide any paleodietary information. Therefore, to reconstruct the trophic chain, we have measured calcium (Ca) isotopes from fossil bone samples of the fauna from the Regourdou site, as well as from three bone samples of the Regourdou 1 Neandertal specimen. The results show a taxon-dependent patterning of the Ca isotopic compositions: herbivores generally have higher δ44/42Ca values than carnivores. All the δ44/42Ca values of Regourdou 1 are low (<-1.6‰), placing this specimen amid carnivores. Using a bone-muscle Ca isotopic offset determined on extant animals, we further show that the δ44/42Ca value of the Regourdou 1 diet, and that of most carnivores, cannot be accounted for by the consumption of meat only, as plants and meat have indistinguishable δ44/42Ca values. Mass balance calculations indicate that the low δ44/42Ca values of the Neandertal's carnivorous diet are explained by the ingestion of bone marrow containing as little as 1% trabecular bone. Our results show that the Regourdou 1 Neanderthal consumed a mixture of various herbivorous prey, as well as trabecular bone, which probably occurred when marrow was ingested, by accident or intentionally.

Pluridisciplinary evidence for burial for the La Ferrassie 8 Neandertal child.

The origin of funerary practices has important implications for the emergence of so-called modern cognitive capacities and behaviour. We provide new multidisciplinary information on the archaeological context of the La Ferrassie 8 Neandertal skeleton (grand abri of La Ferrassie, Dordogne, France), including geochronological data -14C and OSL-, ZooMS and ancient DNA data, geological and stratigraphic information from the surrounding context, complete taphonomic study of the skeleton and associated remains, spatial information from the 1968-1973 excavations, and new (2014) fieldwork data. Our results show that a pit was dug in a sterile sediment layer and the corpse of a two-year-old child was laid there. A hominin bone from this context, identified through Zooarchaeology by Mass Spectrometry (ZooMS) and associated with Neandertal based on its mitochondrial DNA, yielded a direct 14C age of 41.7-40.8 ka cal BP (95%), younger than the 14C dates of the overlying archaeopaleontological layers and the OSL age of the surrounding sediment. This age makes the bone one of the most recent directly dated Neandertals. It is consistent with the age range for the Châtelperronian in the site and in this region and represents the third association of Neandertal taxa to Initial Upper Palaeolithic lithic technocomplex in Western Europe. A detailed multidisciplinary approach, as presented here, is essential to advance understanding of Neandertal behavior, including funerary practices.

Early development of the Neanderthal ribcage reveals a different body shape at birth compared to modern humans.

Ontogenetic studies provide clues for understanding important paleobiological aspects of extinct species. When compared to that of modern humans, the adult Neanderthal thorax was shorter, deeper, and wider. This is related to the wide Neanderthal body and is consistent with their hypothetical large requirements for energy and oxygen. Whether these differences were already established at birth or appeared later during development is unknown. To delve into this question, we use virtual reconstruction tools and geometric morphometrics to recover the 3D morphology of the ribcages of four Neanderthal individuals from birth to around 3 years old: Mezmaiskaya 1, Le Moustier 2, Dederiyeh 1, and Roc de Marsal. Our results indicate that the comparatively deep and short ribcage of the Neanderthals was already present at birth, as were other skeletal species-specific traits. This morphology possibly represents the plesiomorphic condition shared with Homo erectus, and it is likely linked to large energetic requirements.

Issues of theory and method in the analysis of Paleolithic mortuary behavior: A view from Shanidar Cave.

Mortuary behavior (activities concerning dead conspecifics) is one of many traits that were previously widely considered to have been uniquely human, but on which perspectives have changed markedly in recent years. Theoretical approaches to hominin mortuary activity and its evolution have undergone major revision, and advances in diverse archeological and paleoanthropological methods have brought new ways of identifying behaviors such as intentional burial. Despite these advances, debates concerning the nature of hominin mortuary activity, particularly among the Neanderthals, rely heavily on the rereading of old excavations as new finds are relatively rare, limiting the extent to which such debates can benefit from advances in the field. The recent discovery of in situ articulated Neanderthal remains at Shanidar Cave offers a rare opportunity to take full advantage of these methodological and theoretical developments to understand Neanderthal mortuary activity, making a review of these advances relevant and timely.

Cranial trepanation and healing process in modern patients-Bioarchaeological and anthropological implications.

The diagnosis of cranial trepanation in the archaeological record has always been a big challenge for archaeologists. The identification is first and foremost based on the shape and edges of the opening, and in cases where the individual survived, the shape and edges resulted from both the surgical procedure and the healing process. Because of the lack of reliable data on the osseous remodelling process of the skull, it is difficult to distinguish true trepanations from some pathological or physiological defects called pseudotrepanations. Furthermore, it is challenging to investigate the post-operative survival time. The purpose of this paper was to summarize observations made on a total of 90 archaeological samples of cranial lesions interpreted as 'partially' or 'completely' healed trepanations, and compare them with 14 modern case studies. Observations made on monitoring post-operative scans of modern patients, at varying times after craniotomy, provided a preliminary timetable for the successive post-surgery bony changes in the skull, and confirmed that the process of osseous remodelling does lead to smooth and rounded edges of the profile of the opening. However, contrary to what has been observed in several archaeological case studies, none of the cases shows a complete closure of the cranial vault. The sharp vertical edges of the opening become bevelled at late stages of healing, which has to be taken into consideration when interpreting the procedures and methods in past population. By bridging bioarchaeology and medical sciences, this study adds to previous discussions on the diagnosis of healed trepanation in the archaeological record, by providing detailed descriptions of morphological changes at various healing stages, that may help archaeologists to identify ancient trepanations more accurately.

Cervical ribs in human early life: morphological variability and first identification as a morbidity criterion in a past population.

Despite the medical literature on supernumerary cervical ribs in extant adult samples, little is known about their development and occurrence in early infancy. The documentation of cervical ribs in modern samples of fetuses and neonates is indeed affected by ethical as well as technical limitations. The aim of the present study was to investigate their frequencies and morphological variability in the first known archaeological collection of very young children with this anatomical variant. The study sample comes from the 8B-51 necropolis on the Saï island (Sudan) and dates to the Classic Kerma Period (XVIIIe-XVIe centuries BC). It consists of 64 individuals deceased between 24 weeks of amenorrhoea and 2 years of age. Bilateral or unilateral cervical ribs were found in 27 individuals. A total of 43 cervical ribs were identified, 38 of which are fully preserved. According to these observations, at least 42% of the individuals have unilateral or bilateral cervical ribs, with an average maximum length of < 1 cm. This frequency is very high compared to those observed in contemporary adult samples (up to 3%). First, the comparison of our results with biological and genetic research demonstrating the link between the occurrence of cervical ribs and a reduced chance of survival during infancy allows the first identification of this trait as an indicator of morbidity in an archaeological collection, a morbidity to which a genetic homogeneity or even endogamy could contribute. Second, the number of ribs studied makes it possible to propose a morphological classification based on the general shape and the shape of the articular facets, classification that can be used tos refine the analyses of the trait in future samples.

The Neanderthal teeth from Marillac (Charente, Southwestern France): Morphology, comparisons and paleobiology.

Few European sites have yielded human dental remains safely dated to the end of MIS 4/beginning of MIS 3. One of those sites is Marillac (Southwestern France), a collapsed karstic cave where archeological excavations (1967-1980) conducted by B. Vandermeersch unearthed numerous faunal and human remains, as well as a few Mousterian Quina tools. The Marillac sinkhole was occasionally used by humans to process the carcasses of different prey, but there is no evidence for a residential use of the site, nor have any hearths been found. Rare carnivore bones were also discovered, demonstrating that the sinkhole was seasonally used, not only by Neanderthals, but also by predators across several millennia. The lithostratigraphic units containing the human remains were dated to ∼60 kyr. The fossils consisted of numerous fragments of skulls and jaws, isolated teeth and several post-cranial bones, many of them with traces of perimortem manipulations. For those already published, their morphological characteristics and chronostratigraphic context allowed their attribution to Neanderthals. This paper analyzes sixteen unpublished human teeth (fourteen permanent and two deciduous) by investigating the external morphology and metrical variation with respect to other Neanderthal remains and a sample from modern populations. We also investigate their enamel thickness distribution in 2D and 3D, the enamel-dentine junction morphology (using geometric morphometrics) of one molar and two premolars, the roots and the possible expression of taurodontism, as well as pathologies and developmental defects. The anterior tooth use and paramasticatory activities are also discussed. Morphological and structural alterations were found on several teeth, and interpreted in light of human behavior (tooth-pick) and carnivores' actions (partial digestion). The data are interpreted in the context of the available information for the Eurasian Neanderthals.

A case of marked bilateral asymmetry in the sacral alae of the Neandertal specimen Regourdou 1 (Périgord, France).

OBJECTIVES: A marked asymmetry was previously reported in the sacral alae and S1-L5 facets orientation of the Neandertal individual Regourdou 1. Here, we provide a detailed description and quantification of the morphology and degree of asymmetry of this sacrum. MATERIAL AND METHODS: Regourdou 1 was compared to a modern human sample composed of 24 females and 17 males, and to other Neandertal individuals. Both traditional and geometric morphometric analyses were used in order to quantify the degree of sacral asymmetry of Regourdou 1. RESULTS: The asymmetry of both sacral alae and facets orientation substantially exceeds directional and absolute asymmetry of the healthy modern sample. Regourdou 1 shows a considerably shorter right ala, which is absolutely and relatively outside of the modern and Neandertal variations. CONCLUSION: Regourdou 1 shows marked sacral asymmetry that probably originated in early ontogenetic development. An asymmetric sacrum reflects asymmetric load dissipation and could relate to other morphological abnormalities observed in the skeleton, especially the mild scoliosis of the spine and the asymmetry of the femoral diaphyses. Further investigation is necessary to elucidate the relationship between those morphologies as well as a potential impact on the life of the individual.

Morphology of the Denisovan phalanx closer to modern humans than to Neanderthals.

A fully sequenced high-quality genome has revealed in 2010 the existence of a human population in Asia, the Denisovans, related to and contemporaneous with Neanderthals. Only five skeletal remains are known from Denisovans, mostly molars; the proximal fragment of a fifth finger phalanx used to generate the genome, however, was too incomplete to yield useful morphological information. Here, we demonstrate through ancient DNA analysis that a distal fragment of a fifth finger phalanx from the Denisova Cave is the larger, missing part of this phalanx. Our morphometric analysis shows that its dimensions and shape are within the variability of Homo sapiens and distinct from the Neanderthal fifth finger phalanges. Thus, unlike Denisovan molars, which display archaic characteristics not found in modern humans, the only morphologically informative Denisovan postcranial bone identified to date is suggested here to be plesiomorphic and shared between Denisovans and modern humans.

Neandertal foot remains from Regourdou 1 (Montignac-sur-Vézère, Dordogne, France).

Regourdou is a well-known Middle Paleolithic site which has yielded the fossil remains of a minimum of two Neandertal individuals. The first individual (Regourdou 1) is represented by a partial skeleton while the second one is represented by a calcaneus. The foot remains of Regourdou 1 have been used in a number of comparative studies, but to date a full description and comparison of all the foot remains from the Regourdou 1 Neandertal, coming from the old excavations and from the recent reanalysis of the faunal remains, does not exist. Here, we describe and comparatively assess the Regourdou 1 tarsals, metatarsals and phalanges. They display traits observed in other Neandertal feet, which are different from some traits of the Sima de los Huesos (Atapuerca) hominins and of Middle Paleolithic, Upper Paleolithic and recent modern humans. These Neandertal features are: a rectangular talar trochlea with a large lateral malleolar facet, a broad talar head, a broad calcaneus with a projecting sustentaculum tali, a wide and wedged navicular with a projecting medial tubercle, large and wide bases of the lateral metatarsals, and mediolaterally expanded and robust phalanges that also show hallux valgus in a strongly built hallux.