Early dispersal of modern humans in Europe and implications for Neanderthal behaviour.

The appearance of anatomically modern humans in Europe and the nature of the transition from the Middle to Upper Palaeolithic are matters of intense debate. Most researchers accept that before the arrival of anatomically modern humans, Neanderthals had adopted several 'transitional' technocomplexes. Two of these, the Uluzzian of southern Europe and the Châtelperronian of western Europe, are key to current interpretations regarding the timing of arrival of anatomically modern humans in the region and their potential interaction with Neanderthal populations. They are also central to current debates regarding the cognitive abilities of Neanderthals and the reasons behind their extinction. However, the actual fossil evidence associated with these assemblages is scant and fragmentary, and recent work has questioned the attribution of the Châtelperronian to Neanderthals on the basis of taphonomic mixing and lithic analysis. Here we reanalyse the deciduous molars from the Grotta del Cavallo (southern Italy), associated with the Uluzzian and originally classified as Neanderthal. Using two independent morphometric methods based on microtomographic data, we show that the Cavallo specimens can be attributed to anatomically modern humans. The secure context of the teeth provides crucial evidence that the makers of the Uluzzian technocomplex were therefore not Neanderthals. In addition, new chronometric data for the Uluzzian layers of Grotta del Cavallo obtained from associated shell beads and included within a Bayesian age model show that the teeth must date to ~45,000-43,000 calendar years before present. The Cavallo human remains are therefore the oldest known European anatomically modern humans, confirming a rapid dispersal of modern humans across the continent before the Aurignacian and the disappearance of Neanderthals.

Vergisson 4: a left-handed Neandertal.

OBJECTIVES: Handedness is an important marker for lateralization of humans in the modern and fossil record. For the most part, Neandertals and their ancestors are strongly right-handed. We describe a single tooth from a Neandertal level at Vergisson 4 (Vg 4-83). This left upper central incisor shows all the features typical of Neandertal incisors. It also exhibits a predominance of left-handed striations. METHODS: Striations on the incisor's labial surface were mapped at 20x magnification using Photoshop. Angulations of the striations were determined from their deviation from the maximum mesio-distal line and were analyzed using NIH's freeware, Image J. RESULTS: Of the 60 labial surface striations, Vg 4-83 shows a strong predominance of left-handed striations (46; 76.7%), which are statistically significantly different (p < .001 with a two-tailed chi2 test) from the small number (3) of right-handed striations. DISCUSSION: The identification of another left-handed Neandertal adds to our understanding about handedness variation in this fossil hominin. Given the high frequency of right-handed Neandertals, the 90: 10 modern ratio is still preserved in this group.

Structural organization and tooth development in a Homo aff. erectus juvenile mandible from the Early Pleistocene site of Garba IV at Melka Kunture, Ethiopian highlands.

OBJECTIVES: The immature partial mandible GAR IVE from the c. 1.7 Ma old Garba IV site at Melka Kunture (Upper Awash Basin, Ethiopia), the earliest human representative from a mountain-like environment, represents one of the oldest early Homo specimens bearing a mixed dentition. Following its first description (Condemi, ), we extended the analytical and comparative record of this specimen by providing unreported details about its inner morphology, tooth maturational pattern and age at death, crown size, and tooth tissue proportions. MATERIALS AND METHODS: The new body of quantitative structural information and virtual imaging derives from a medical CT record performed in 2013. RESULTS: Compared to the extant human condition and to some fossil representatives of comparable individual age, the GAR IVE mandible reveals absolutely and relatively thick cortical bone. Crown size of the permanent lateral incisor and the canine fit the estimates of H. erectus s.l., while the dm2 and the M1 more closely approach those of H. habilis-rudolfensis. Molar crown pulp volumes are lower than reported in other fossil specimens and in extant humans. The mineralization sequence of the permanent tooth elements is represented four times in our reference sample of extant immature individuals (N = 795). CONCLUSIONS: The tooth developmental pattern displayed by the immature individual from Garba IV falls within the range of variation of extant human populations and is also comparable with that of other very young early fossil hominins. Taken together, the evidence presented here for mandibular morphology and dental development suggest GAR IVE is a robust 2.5- to 3.5-year old early Homo specimen.

Venturing out safely: The biogeography of Homo erectus dispersal out of Africa.

The dispersal of Homo erectus out of Africa at some 1.9 million years ago is one of the most important, crucial, and yet controversial events in human evolution. Current opinions about this episode expose the contrast between those who see H. erectus as a highly social, cooperative species seeking out new ecological opportunities to exploit, and those preferring a passive, climate driven explanation for such an event. By using geostatistics techniques and probabilistic models, we characterised the ecological context of H. erectus dispersal, from its East African origin to the colonization of Eurasia, taking into account both the presence of other large mammals and the physical characteristics of the landscape as potential factors. Our model indicated that H. erectus followed almost passively the large herbivore fauna during its dispersal. In Africa, the dispersal was statistically associated with the presence of large freshwater bodies (Rift Valley Lakes). In Eurasia, the presence of H. erectus was associated with the occurrence of geological outcrops likely yielding unconsolidated flint. During the early phase of dispersal, our model indicated that H. erectus actively avoided areas densely populated by large carnivores. This pattern weakened as H. erectus dispersed over Europe, possibly because of the decreasing presence of carnivores there plus the later acquisition of Acheulean technology. During this later phase, H. erectus was associated with limestone and shaley marl, and seems to have been selecting for high-elevation sites. While our results do not directly contradict the idea that H. erectus may have been an active hunter, they clearly point to the fact that predator avoidance may have conditioned its long-distance diffusion as it moved outside Africa. The modelled dispersal route suggests that H. erectus remained preferentially associated with low/middle latitude (i.e., comparatively warm) sites throughout its colonization history.

A pathological Neandertal thumb phalanx from Moula-Guercy (France).

OBJECTIVE: To discuss a Neandertal pathological adult first pollical proximal phalanx (I2-104) from the Baume de Moula-Guercy (Ardèche, France) and evaluate the possible causes of this pathology. METHODS: Macroscopic analyses of external features, as well as CT imaging, were used in the analysis RESULTS: The presence of asymmetric eburnation on the distal epiphysis associated with an osteophyte on the palmar surface, as well as the absence of periosteal bone reaction visible on CT images, is consistent with osteoarthritis. CONCLUSION: Osteoarthritis (OA) can have different origins and the cause is difficult to identify. The pathology of the Moula-Guercy I2-104 phalanx may be due to a genetic predisposition for OA known in Neandertals and associated with short limb bones. The OA could have been aggravated by the age of this individual and by an inflammatory reaction caused by repeated movements and intense vibrations provoked by high-frequency knapping or by other use of the hands SIGNIFICANCE: The I2-104 phalanx is the first Neandertal pollical phalanx known to display OA, although joints of this bone are frequently affected by this pathology in modern humans. Thus, greater insight into the presence and consequences of Neandertal behaviors is offered LIMITATION: It is impossible to give a definitive conclusion on the cause(s) of the OA in this case. SUGGESTIONS FOR FURTHER RESEARCH: More data is needed concerning OA within Neandertals and its relationship with behavior and genetics.

Cervical and crown outline analysis of worn Neanderthal and modern human lower second deciduous molars.

Despite the general increase in digital techniques for dental morphometric analyses, only a few methods are available to study worn teeth. Moreover, permanent dentitions are studied much more frequently than deciduous teeth. In this study, we address both issues by providing a taxonomic classification of Neanderthal and modern human (MH) lower second deciduous molars (dm(2) s) through the analysis of crown and cervical outlines. Crown and cervical outlines were obtained from a three-dimensional (3D) digital sample of uniformly oriented dm(2) s. Both outlines were centered on the centroid of their area and represented by 16 pseudolandmarks obtained by equiangularly spaced radial vectors out of the centroid. We removed size information from the oriented and centered outlines with a uniform scaling of the pseudolandmark configurations to unit Centroid Size. Group shape variation was evaluated separately for the dm(2) crown and cervical outlines through a shape-space principal component (PC) analysis. Finally, quadratic discriminant analysis of a subset of PCs was used to classify the specimens. Our results demonstrate that both outlines successfully separate the two groups. Neanderthals showed a buccodistal expansion and convex lingual outline shape, whilst MHs have buccodistal reduction and straight lingual outline shape. Therefore, we confirmed that the cervical outline represents an effective parameter for distinguishing between the two taxa when dealing with worn or damaged dm(2) s.

Blood groups of Neandertals and Denisova decrypted.

Blood group systems were the first phenotypic markers used in anthropology to decipher the origin of populations, their migratory movements, and their admixture. The recent emergence of new technologies based on the decoding of nucleic acids from an individual's entire genome has relegated them to their primary application, blood transfusion. Thus, despite the finer mapping of the modern human genome in relation to Neanderthal and Denisova populations, little is known about red cell blood groups in these archaic populations. Here we analyze the available high-quality sequences of three Neanderthals and one Denisovan individuals for 7 blood group systems that are used today in transfusion (ABO including H/Se, Rh (Rhesus), Kell, Duffy, Kidd, MNS, Diego). We show that Neanderthal and Denisova were polymorphic for ABO and shared blood group alleles recurrent in modern Sub-Saharan populations. Furthermore, we found ABO-related alleles currently preventing from viral gut infection and Neanderthal RHD and RHCE alleles nowadays associated with a high risk of hemolytic disease of the fetus and newborn. Such a common blood group pattern across time and space is coherent with a Neanderthal population of low genetic diversity exposed to low reproductive success and with their inevitable demise. Lastly, we connect a Neanderthal RHD allele to two present-day Aboriginal Australian and Papuan, suggesting that a segment of archaic genome was introgressed in this gene in non-Eurasian populations. While contributing to both the origin and late evolutionary history of Neanderthal and Denisova, our results further illustrate that blood group systems are a relevant piece of the puzzle helping to decipher it.

Funerary practices of the Iberomaurusian population of Taforalt (Tafoughalt, Morocco, 11-12,000 BP): the case of Grave XII.

The Iberomaurusian necropolis of Taforalt (Morocco, 11-12000 BP), excavated by Roche in the 1950s, contains 28 multiple graves. The funerary practices of the Taforalt population have been the focus of a previous work (Mariotti et al., 2009). In the absence of the excavation records of the necropolis, these funerary practices were investigated through the analysis of the contents of each grave and the distribution of intentionally modified specimens (ochre-dyeing, cut marks). Previous research has drawn particular attention to Grave XII (containing three male adults and two juveniles), where many intentionally modified specimens were identified. The present study focused specifically on the human remains recovered from Grave XII. Analysis of these remains has provided evidence of interventions, such as dismemberment and defleshing of the cadaver, and the use of ochre to colour the bones. Furthermore, the presence of lesions on two skulls suggests the possibility of intentional killing and cannibalism among the Taforalt population. This study further supports our previous impression of the complex and diversified funerary practices, characterising the social life of the Iberomaurusian population of Taforalt.

Is Homo heidelbergensis a distinct species? New insight on the Mauer mandible.

The discovery of new fossils in Africa, Asia, and Europe, and the recognition of a greater diversity in the middle Pleistocene fossil record, has led to a reconsideration of the species Homo heidelbergensis. This nomen, formulated by Schoetensack in 1908 to describe the Mauer jaw (Germany), was almost forgotten during most of the past century. Numerous fossils have been attributed to it but no consensus has arisen concerning their classification. The holotype anatomical traits are still poorly understood, and numerous fossils with no mandibular remains have been placed in the taxon. Some researchers propose H. heidelbergensis as an Afro-European taxon that is ancestral to both modern humans and Neandertals whereas others think it is a strictly European species that is part of the Neandertal lineage. We focus on the validity of H. heidelbergensis, using the traditional basis of species recognition: anatomical description. We provide a comparative morphological analysis using 47 anatomical traits of 36 Pleistocene fossils from Africa, Asia, and Europe and 35 extant human mandibles. We re-examine the mandibular features of Mauer and discuss the specimen's inclusion in H. heidelbergensis, as well as alternative evolutionary theories. To lend objectivity to specimen grouping, we use multiple correspondence analysis associated with hierarchical classification that creates clusters corresponding to phenetic similarities between jaws. Our phenetic and comparative morphological analyses support the validity of H. heidelbergensis as a taxon. A set of morphological features can be statistically identified for the definition of the species. Some traits can be used to delimit H. heidelbergensis in an evolutionary framework (e.g., foramina mentale posteriorly positioned, horizontal retromolar surface). Those traits are also present on African (e.g., Tighenif) and European (e.g., Sima de los Huesos) specimens that show a close relationship with the Mauer mandible. Therefore, the definition of H. heidelbergensis is more precise and mainly supports the theory of an Afro-European taxon, which is the last common ancestor of H. neanderthalensis and H. sapiens. However, the results of this study fail to entirely discount the hypothesis that considers H. heidelbergensis as a chronospecies leading to the Neandertals.

Funerary practices of the Iberomaurusian population of Taforalt (Tafoughalt; Morocco, 11-12,000BP): new hypotheses based on a grave by grave skeletal inventory and evidence of deliberate human modification of the remains.

The Iberomaurusian necropolis of Taforalt (Morocco, 11-12,000BP), excavated by Roche in the 1950s, contains 28 multiple graves. The osteological collection has been the focus of many anthropological studies and has been used as a comparative sample for other paleoanthropological investigations. The presence of particular sepulchral structures and the use of ochre testify to complex funerary practices, which have not been adequately investigated thus far. Unfortunately, neither the excavation records nor detailed descriptions of the graves are available today. The aim of this study is to investigate the funerary practices of the population based on examination of the human osteological collection (Institut de Paléontologie Humaine, Paris). The bones of adolescents and adults were inventoried to analyse the contents of each grave and the distribution of intentionally modified specimens (ochre-dyeing, cutmarks). The minimum number of individuals was also calculated. The results suggest that the necropolis is a group of primary and secondary burials, even within the same "grave," of about 40 adolescents and adults. The previous estimate of 86 individuals by Ferembach in 1962 appears to be an overestimation. The presence of red ochre and cutmarks on some bones suggests various rituals, which denote a certain profundity of thinking about life and death. It is possible that the Taforalt cave was a special, perhaps sacred, place where particular rituals were celebrated or where more occasional social or religious events took place. Comparison with other Iberomaurusian and Capsian sites provides evidence of cultural continuity in North Africa for a long period of time. The present study demonstrates that re-examination of human osteological collections deriving from ancient excavations, for which a lack of adequate documentation of the context of the specimens is fairly common, can also provide information about aspects like funerary practices, which are usually investigated on the basis of other sources.

Living on the edge: Was demographic weakness the cause of Neanderthal demise?

The causes of disappearance of the Neanderthals, the only human population living in Europe before the arrival of Homo sapiens, have been debated for decades by the scientific community. Different hypotheses have been advanced to explain this demise, such as cognitive, adaptive and cultural inferiority of Neanderthals. Here, we investigate the disappearance of Neanderthals by examining the extent of demographic changes needed over a period of 10,000 years (yrs) to lead to their extinction. In regard to such fossil populations, we inferred demographic parameters from present day and past hunter-gatherer populations, and from bio-anthropological rules. We used demographic modeling and simulations to identify the set of plausible demographic parameters of the Neanderthal population compatible with the observed dynamics, and to explore the circumstances under which they might have led to the disappearance of Neanderthals. A slight (<4%) but continuous decrease in the fertility rate of younger Neanderthal women could have had a significant impact on these dynamics, and could have precipitated their demise. Our results open the way to non-catastrophic events as plausible explanations for Neanderthal extinction.

Sub-adult aging method selection (SAMS): A decisional tool for selecting and evaluating sub-adult age estimation methods based on standardized methodological parameters.

OBJECTIVES: A decisional tool was developed to select sub-adult age estimation methods referenced in a centralized database. Through a freely accessible webpage interface, this tool allows users to evaluate how much the sampling and statistical protocols of these referenced methods comply with methodological recommendations published for building and applying methods in forensic anthropology. MATERIALS AND METHODS: 261 publications on sub-adult age estimation were collected. Three search parameters describing the anatomical element(s) and the indicators used to obtain age estimates are chosen by the user to filter the database and present the publications that best correspond to the user's selection. A simple algorithm was created to score age estimation methods according to their relevance and validity. "Relevance" and "Validity" parameters indicate how much a publication complies with user queries and published methodological recommendations, respectively; "Score" is a combination of "Relevance" and "Validity". The closer these parameters are to 1, the better the method complies with the user's choice and standardized protocols. RESULTS: The publications resulting from the user's query appear as search results alphabetically. They are characterized by their "Relevance", "Validity" and "Score" values and descriptors relating to their methodology, sampling and statistical protocols. The reference of the publications and an URL to access them online are also provided. CONCLUSIONS: SAMS is a decisional tool based on a centralized database for selecting, accessing and evaluating sub-adult age estimation methods based on published methodological recommendations. Protocol validity can be easily and fully accessed to provide the necessary information for method evaluation. The database will be gradually updated and implemented as new sub-adult age estimation methods are made available online.

Integrating Growth Variability of the Ilium, Fifth Lumbar Vertebra, and Clavicle with Multivariate Adaptive Regression Splines Models for Subadult Age Estimation.

Subadult age estimation should rely on sampling and statistical protocols capturing development variability for more accurate age estimates. In this perspective, measurements were taken on the fifth lumbar vertebrae and/or clavicles of 534 French males and females aged 0-19 years and the ilia of 244 males and females aged 0-12 years. These variables were fitted in nonparametric multivariate adaptive regression splines (MARS) models with 95% prediction intervals (PIs) of age. The models were tested on two independent samples from Marseille and the Luis Lopes reference collection from Lisbon. Models using ilium width and module, maximum clavicle length, and lateral vertebral body heights were more than 92% accurate. Precision was lower for postpubertal individuals. Integrating punctual nonlinearities of the relationship between age and the variables and dynamic prediction intervals incorporated the normal increase in interindividual growth variability (heteroscedasticity of variance) with age for more biologically accurate predictions.

A critical review of sub-adult age estimation in biological anthropology: Do methods comply with published recommendations?

The diversity of approaches and the high number of publications on sub-adult age estimation is a testament to the relevance of this particular area of forensic anthropological research. However, a downside of this diversity is the many methodological, sampling and statistical discrepancies between publications, which can lead to difficulties in method definition, application and comparison. Several authors have published recommendations highlighting standardized methodological parameters that should be respected and clearly appear in the original publications for anthropological methods to be valid. This study aims to objectively evaluate a corpus of 269 publications on dental and skeletal postnatal sub-adult age estimation using these recommendations translated into descriptors. These descriptors cover five sampling and five statistical parameters that can be considered valid or invalid according to published methodological recommendations. Parameter and descriptor distributions are shown in frequency tables and graphs, illustrating the general invalidity of the sampling and/or statistical protocols. Provided our corpus of methods is an accurate representation of available publications, the extrapolation of these results leads to conclude that most sub-adult age estimates are at worst invalid, at best questionable, and almost certainly method-dependent. In view of this study, rigorous and standardized sampling and statistical approaches should be preferred when applying and building sub-adult age estimation methods.

A New Approach of Juvenile Age Estimation using Measurements of the Ilium and Multivariate Adaptive Regression Splines (MARS) Models for Better Age Prediction.

Juvenile age estimation methods used in forensic anthropology generally lack methodological consistency and/or statistical validity. Considering this, a standard approach using nonparametric Multivariate Adaptive Regression Splines (MARS) models were tested to predict age from iliac biometric variables of male and female juveniles from Marseilles, France, aged 0-12 years. Models using unidimensional (length and width) and bidimensional iliac data (module and surface) were constructed on a training sample of 176 individuals and validated on an independent test sample of 68 individuals. Results show that MARS prediction models using iliac width, module and area give overall better and statistically valid age estimates. These models integrate punctual nonlinearities of the relationship between age and osteometric variables. By constructing valid prediction intervals whose size increases with age, MARS models take into account the normal increase of individual variability. MARS models can qualify as a practical and standardized approach for juvenile age estimation.

Possible interbreeding in late Italian Neanderthals? New data from the Mezzena jaw (Monti Lessini, Verona, Italy).

In this article we examine the mandible of Riparo Mezzena a Middle Paleolithic rockshelter in the Monti Lessini (NE Italy, Verona) found in 1957 in association with Charentian Mousterian lithic assemblages. Mitochondrial DNA analysis performed on this jaw and on other cranial fragments found at the same stratigraphic level has led to the identification of the only genetically typed Neanderthal of the Italian peninsula and has confirmed through direct dating that it belongs to a late Neanderthal. Our aim here is to re-evaluate the taxonomic affinities of the Mezzena mandible in a wide comparative framework using both comparative morphology and geometric morphometrics. The comparative sample includes mid-Pleistocene fossils, Neanderthals and anatomically modern humans. This study of the Mezzena jaw shows that the chin region is similar to that of other late Neanderthals which display a much more modern morphology with an incipient mental trigone (e.g. Spy 1, La Ferrassie, Saint-Césaire). In our view, this change in morphology among late Neanderthals supports the hypothesis of anatomical change of late Neanderthals and the hypothesis of a certain degree of interbreeding with AMHs that, as the dating shows, was already present in the European territory. Our observations on the chin of the Mezzena mandible lead us to support a non abrupt phylogenetic transition for this period in Europe.

The stem species of our species: a place for the archaic human cranium from Ceprano, Italy.

One of the present challenges in the study of human evolution is to recognize the hominin taxon that was ancestral to Homo sapiens. Some researchers regard H. heidelbergensis as the stem species involved in the evolutionary divergence leading to the emergence of H. sapiens in Africa, and to the evolution of the Neandertals in Europe. Nevertheless, the diagnosis and hypodigm of H. heidelbergensis still remain to be clarified. Here we evaluate the morphology of the incomplete cranium (calvarium) known as Ceprano whose age has been recently revised to the mid of the Middle Pleistocene, so as to test whether this specimen may be included in H. heidelbergensis. The analyses were performed according to a phenetic routine including geometric morphometrics and the evaluation of diagnostic discrete traits. The results strongly support the uniqueness of H. heidelbergensis on a wide geographical horizon, including both Eurasia and Africa. In this framework, the Ceprano calvarium--with its peculiar combination of archaic and derived traits--may represent, better than other penecontemporaneous specimens, an appropriate ancestral stock of this species, preceding the appearance of regional autapomorphic features.

Neanderthals versus Modern Humans: Evidence for Resource Competition from Isotopic Modelling.

During later MOIS3, in Europe two populations were present, autochthonous Neanderthals and modern humans. Ecological competition between these two populations has often been evoked but never demonstrated. Our aim is to establish whether resource competition occurred. In this paper, in order to examine the possibility of ecological competition between these two populations, 599 isotopic data were subjected to rigorous statistical treatment and analysis through mixing models. The aim of this paper was to compare dietary strategies of Neanderthals and modern humans over time. Our conclusions suggest that Neanderthals and modern humans shared dietary habits in the particular environmental context of MOIS3 characterised in Europe by climatic deterioration. In this environmental context, the resource competition between Neanderthals and modern humans may have accelerated the disappearance of the Neanderthal population.

The microcephalin ancestral allele in a Neanderthal individual.

BACKGROUND: The high frequency (around 0.70 worldwide) and the relatively young age (between 14,000 and 62,000 years) of a derived group of haplotypes, haplogroup D, at the microcephalin (MCPH1) locus led to the proposal that haplogroup D originated in a human lineage that separated from modern humans >1 million years ago, evolved under strong positive selection, and passed into the human gene pool by an episode of admixture circa 37,000 years ago. The geographic distribution of haplogroup D, with marked differences between Africa and Eurasia, suggested that the archaic human form admixing with anatomically modern humans might have been Neanderthal. METHODOLOGY/PRINCIPAL FINDINGS: Here we report the first PCR amplification and high-throughput sequencing of nuclear DNA at the microcephalin (MCPH1) locus from Neanderthal individual from Mezzena Rockshelter (Monti Lessini, Italy). We show that a well-preserved Neanderthal fossil dated at approximately 50,000 years B.P., was homozygous for the ancestral, non-D, allele. The high yield of Neanderthal mtDNA sequences of the studied specimen, the pattern of nucleotide misincorporation among sequences consistent with post-mortem DNA damage and an accurate control of the MCPH1 alleles in all personnel that manipulated the sample, make it extremely unlikely that this result might reflect modern DNA contamination. CONCLUSIONS/SIGNIFICANCE: The MCPH1 genotype of the Monti Lessini (MLS) Neanderthal does not prove that there was no interbreeding between anatomically archaic and modern humans in Europe, but certainly shows that speculations on a possible Neanderthal origin of what is now the most common MCPH1 haplogroup are not supported by empirical evidence from ancient DNA.