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.

Ancient West African foragers in the context of African population history.

Our knowledge of ancient human population structure in sub-Saharan Africa, particularly prior to the advent of food production, remains limited. Here we report genome-wide DNA data from four children-two of whom were buried approximately 8,000 years ago and two 3,000 years ago-from Shum Laka (Cameroon), one of the earliest known archaeological sites within the probable homeland of the Bantu language group1-11. One individual carried the deeply divergent Y chromosome haplogroup A00, which today is found almost exclusively in the same region12,13. However, the genome-wide ancestry profiles of all four individuals are most similar to those of present-day hunter-gatherers from western Central Africa, which implies that populations in western Cameroon today-as well as speakers of Bantu languages from across the continent-are not descended substantially from the population represented by these four people. We infer an Africa-wide phylogeny that features widespread admixture and three prominent radiations, including one that gave rise to at least four major lineages deep in the history of modern humans.

Reconstructing the genetic history of late Neanderthals.

Although it has previously been shown that Neanderthals contributed DNA to modern humans, not much is known about the genetic diversity of Neanderthals or the relationship between late Neanderthal populations at the time at which their last interactions with early modern humans occurred and before they eventually disappeared. Our ability to retrieve DNA from a larger number of Neanderthal individuals has been limited by poor preservation of endogenous DNA and contamination of Neanderthal skeletal remains by large amounts of microbial and present-day human DNA. Here we use hypochlorite treatment of as little as 9 mg of bone or tooth powder to generate between 1- and 2.7-fold genomic coverage of five Neanderthals who lived around 39,000 to 47,000 years ago (that is, late Neanderthals), thereby doubling the number of Neanderthals for which genome sequences are available. Genetic similarity among late Neanderthals is well predicted by their geographical location, and comparison to the genome of an older Neanderthal from the Caucasus indicates that a population turnover is likely to have occurred, either in the Caucasus or throughout Europe, towards the end of Neanderthal history. We find that the bulk of Neanderthal gene flow into early modern humans originated from one or more source populations that diverged from the Neanderthals that were studied here at least 70,000 years ago, but after they split from a previously sequenced Neanderthal from Siberia around 150,000 years ago. Although four of the Neanderthals studied here post-date the putative arrival of early modern humans into Europe, we do not detect any recent gene flow from early modern humans in their ancestry.

The evolution and changing ecology of the African hominid oral microbiome.

The oral microbiome plays key roles in human biology, health, and disease, but little is known about the global diversity, variation, or evolution of this microbial community. To better understand the evolution and changing ecology of the human oral microbiome, we analyzed 124 dental biofilm metagenomes from humans, including Neanderthals and Late Pleistocene to present-day modern humans, chimpanzees, and gorillas, as well as New World howler monkeys for comparison. We find that a core microbiome of primarily biofilm structural taxa has been maintained throughout African hominid evolution, and these microbial groups are also shared with howler monkeys, suggesting that they have been important oral members since before the catarrhine-platyrrhine split ca. 40 Mya. However, community structure and individual microbial phylogenies do not closely reflect host relationships, and the dental biofilms of Homo and chimpanzees are distinguished by major taxonomic and functional differences. Reconstructing oral metagenomes from up to 100 thousand years ago, we show that the microbial profiles of both Neanderthals and modern humans are highly similar, sharing functional adaptations in nutrient metabolism. These include an apparent Homo-specific acquisition of salivary amylase-binding capability by oral streptococci, suggesting microbial coadaptation with host diet. We additionally find evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that is not observed in later modern human populations. Differences in the oral microbiomes of African hominids provide insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.

The genetic history of Ice Age Europe.

Modern humans arrived in Europe ~45,000 years ago, but little is known about their genetic composition before the start of farming ~8,500 years ago. Here we analyse genome-wide data from 51 Eurasians from ~45,000-7,000 years ago. Over this time, the proportion of Neanderthal DNA decreased from 3-6% to around 2%, consistent with natural selection against Neanderthal variants in modern humans. Whereas there is no evidence of the earliest modern humans in Europe contributing to the genetic composition of present-day Europeans, all individuals between ~37,000 and ~14,000 years ago descended from a single founder population which forms part of the ancestry of present-day Europeans. An ~35,000-year-old individual from northwest Europe represents an early branch of this founder population which was then displaced across a broad region, before reappearing in southwest Europe at the height of the last Ice Age ~19,000 years ago. During the major warming period after ~14,000 years ago, a genetic component related to present-day Near Easterners became widespread in Europe. These results document how population turnover and migration have been recurring themes of European prehistory.

Biocultural diversity in Late Pleistocene/Early Holocene Africa: Olduvai Hominid 1 (Tanzania) biological affinity and intentional body modification.

OBJECTIVES: The dentition of Olduvai Hominid 1 (OH1) exhibits an anomalous pattern of dental wear that was originally attributed to either intentional cultural modification (filing) or plant processing behaviors. A differential diagnosis of the wear and assessment of the biological affinity of OH1 is presented. MATERIALS AND METHODS: Macroscopic and microscopic observations of all labial and buccal tooth surfaces were undertaken to assess wear patterns. A multivariate analysis of mandibular morphology of OH1 compared to other Late Pleistocene, Holocene, and recent modern humans was used to ascertain biological affinity. RESULTS: The morphological variation of the OH1 mandible is closely aligned with variation in penecontemporaneous fossils from Africa and outside that of recent humans. The concave wear facets exposing dentin on the labial surfaces of all three preserved mandibular incisors is confirmed. Substantial loss of labial/buccal surfaces was documented on the surfaces of all in situ maxillary and mandibular canines, premolars, and molars ranging from distinct facets with well-defined edges, to blunting or "polishing" around areas of maximum buccal curvature. The wear on both the anterior and postcanine teeth closely resemble that caused by adornments ("labrets") worn in lower-lip and buccal facial piercings known from bioarchaeological and ethnographic contexts. The wear pattern suggests that the OH1 wore three facial piercings-two buccal/lateral and a medial one in the lower lip. DISCUSSION: Our findings suggest that the expression of social identities through intentional body modification is more diverse than previously documented elsewhere in Africa during the Late Pleistocene (i.e., ablation) and Early Holocene (i.e., ablation, chipping, and filing).

Late Pleistocene age and archaeological context for the hominin calvaria from GvJm-22 (Lukenya Hill, Kenya).

Kenya National Museums Lukenya Hill Hominid 1 (KNM-LH 1) is a Homo sapiens partial calvaria from site GvJm-22 at Lukenya Hill, Kenya, associated with Later Stone Age (LSA) archaeological deposits. KNM-LH 1 is securely dated to the Late Pleistocene, and samples a time and region important for understanding the origins of modern human diversity. A revised chronology based on 26 accelerator mass spectrometry radiocarbon dates on ostrich eggshells indicates an age range of 23,576-22,887 y B.P. for KNM-LH 1, confirming prior attribution to the Last Glacial Maximum. Additional dates extend the maximum age for archaeological deposits at GvJm-22 to >46,000 y B.P. (>46 kya). These dates are consistent with new analyses identifying both Middle Stone Age and LSA lithic technologies at the site, making GvJm-22 a rare eastern African record of major human behavioral shifts during the Late Pleistocene. Comparative morphometric analyses of the KNM-LH 1 cranium document the temporal and spatial complexity of early modern human morphological variability. Features of cranial shape distinguish KNM-LH 1 and other Middle and Late Pleistocene African fossils from crania of recent Africans and samples from Holocene LSA and European Upper Paleolithic sites.

Temporal labyrinths of eastern Eurasian Pleistocene humans.

One of the morphological features that has been identified as uniquely derived for the western Eurasian Neandertals concerns the relative sizes and positions of their semicircular canals. In particular, they exhibit a relatively small anterior canal, a relatively larger lateral one, and a more inferior position of the posterior one relative to the lateral one. These discussions have not included full paleontological data on eastern Eurasian Pleistocene human temporal labyrinths, which have the potential to provide a broader context for assessing Pleistocene Homo trait polarities. We present the temporal labyrinths of four eastern Eurasian Pleistocene Homo, one each of Early (Lantian 1), Middle (Hexian 1), and Late (Xujiayao 15) Pleistocene archaic humans and one early modern human (Liujiang 1). The labyrinths of the two earlier specimens and the most recent one conform to the proportions seen among western early and recent modern humans, reinforcing the modern human pattern as generally ancestral for the genus Homo. The labyrinth of Xujiayao 15 is in the middle of the Neandertal variation and separate from the other samples. This eastern Eurasian labyrinthine dichotomy occurs in the context of none of the distinctive Neandertal external temporal or other cranial features. As such, it raises questions regarding possible cranial and postcranial morphological correlates of Homo labyrinthine variation, the use of individual "Neandertal" features for documenting population affinities, and the nature of late archaic human variation across Eurasia.

Evidence supporting an intentional Neandertal burial at La Chapelle-aux-Saints.

The bouffia Bonneval at La Chapelle-aux-Saints is well known for the discovery of the first secure Neandertal burial in the early 20th century. However, the intentionality of the burial remains an issue of some debate. Here, we present the results of a 12-y fieldwork project, along with a taphonomic analysis of the human remains, designed to assess the funerary context of the La Chapelle-aux-Saints Neandertal. We have established the anthropogenic nature of the burial pit and underlined the taphonomic evidence of a rapid burial of the body. These multiple lines of evidence support the hypothesis of an intentional burial. Finally, the discovery of skeletal elements belonging to the original La Chapelle aux Saints 1 individual, two additional young individuals, and a second adult in the bouffia Bonneval highlights a more complex site-formation history than previously proposed.

La Ferrassie 8 Neandertal child reloaded: New remains and re-assessment of the original collection.

The first evidence of the partial infant Neandertal skeleton La Ferrassie 8 (LF8) was discovered in 1970, although most of the remains were found in 1973 as part of the 1968-1973 work at the site by H. Delporte. This individual and the other Neandertal children from La Ferrassie were published in the early 1980s by J.-L. Heim, and since then LF8 has been regarded as coming from a poorly documented excavation. The recent rediscovery of the box that contained the hominin bones given by Delporte to Heim in the Muséum national d'Histoire naturelle (MNHN) collection provided new fossils and helped to locate LF8 in the site: level M2 in square 1. Two visits to the Musée d'Archéologie nationale et Domaine national de Saint-Germain-en-Laye (MAN) yielded additional fossil remains from both the 1970 and 1973 excavations and resulted in the discovery of all of the notes from the excavation of H. Delporte between 1968 and 1973. Here the new fossil remains (47 after performing all possible refits), representing significant portions of the cranium, mandible, and vertebral column together with fragmentary hand and costal remains, are described. Unsurprisingly, the morphology of the bony labyrinth and of a complete stapes from the nearly complete left temporal show clear Neandertal affinities. Additionally, a complete reassessment of the original LF8 collection has resulted in the identification of several errors in the anatomical determination. Despite the significant increase in the anatomical representation of LF8, the skeletal remains are still limited to the head, thorax, pelvis, and four hand phalanges, with some very fragile elements relatively well preserved. Different hypotheses are proposed to explain this anatomical representation, which can be tested during future fieldwork.

Frontal sinus size in South African Later Stone Age Holocene Khoe-San.

Frontal size variation is comparatively poorly sampled among sub-Saharan African populations. This study assessed frontal sinus size in a sample of Khoe-San skeletal remains from South African Later Stone Age contexts. Volumes were determined from CT scans of 102 adult crania; individual sex could be estimated in 82 cases. Sinus volume is not sexually dimorphic in this sample. The lack of frontal sinus aplasia is concordant with the low incidences recorded for other sub-Saharan African and most other global populations save those that inhabit high latitudes. There is considerable variation in frontal sinus size among global populations, and the Khoe-San possess among the smallest. The Khoe-San have rather diminutive sinuses compared to sub-Saharan Bantu-speaking populations but resemble a northern African (Sudanese) population. Genetic studies indicate the earliest population divergence within Homo sapiens to have been between the Khoe-San and all other living groups, and that this likely occurred in Africa during the span of Marine Isotope Stages 8-6. There is scant information on frontal sinus development among Late Quaternary African fossils that are likely either closely related or attributable to Homo sapiens. Among these, the MIS 3 cranium from Hofmeyr, South Africa, exhibits distinct Khoe-San cranial affinities and despite its large size has a very small frontal sinus. This raises the possibility that the small frontal sinuses of the Holocene South African Khoe-San might be a feature retained from an earlier MIS 3 population.

From hunter-gatherers to food producers: New dental insights into the Nile Valley population history (Late Paleolithic-Neolithic).

OBJECTIVES: This study presents biological affinities between the last hunter-fisher-gatherers and first food-producing societies from the Nile Valley. We investigate odontometric and dental tissue proportion changes between these populations from the Middle Nile Valley and acknowledge the biological processes behind them. MATERIALS AND METHODS: Dental remains of 329 individuals from Nubia and Central Sudan that date from the Late Pleistocene to the mid-Holocene are studied. Using 3D imaging techniques, we investigated outer and inner metric aspects of upper central incisors, and first and second upper molars. RESULTS: Late Paleolithic and Mesolithic foragers display homogeneous crown dimensions, dental tissue proportions, and enamel thickness distribution. This contrasts with Neolithic trends for significant differences from earlier samples on inner and outer aspects. Finally, within the Neolithic sample differences are found between Nubian and Central Sudanese sites. DISCUSSION: Substantial dental variation appears to have occurred around 6000 bce in the Nile Valley, coinciding with the emergence of food-producing societies in the region. Archeological and biological records suggest little differences in dietary habits and dental health during this transition. Furthermore, the substantial variations identified here would have happened in an extremely short time, a few centuries at most. This does not support in situ diet-related adaptation. Rather, we suggest these data are consistent with some level of population discontinuity between the Mesolithic and Neolithic samples considered here. Complex settlement processes could also explain the differences between Nubia and Central Sudan, and with previous results based on nonmetric traits.

A double-blind comparison of morphological and collagen fingerprinting (ZooMS) methods of skeletal identifications from Paleolithic contexts.

Modeling the subsistence strategies of prehistoric groups depends on the accuracy of the faunal identifications that provide the basis for these models. However, our knowledge remains limited about the reproducibility of published taxonomic identifications and how they accurately reflect the range of species deposited in the archaeological record. This study compares taxonomic identifications at three Paleolithic sites (Saint-Césaire and Le Piage in France, Crvena Stijena in Montenegro) characterized by high levels of fragmentation. Identifications at these sites were derived using two methods: morphological identification and collagen fingerprinting, the latter a peptide-based approach known as ZooMS. Using a double-blind experimental design, we show that the two methods give taxonomic profiles that are statistically indistinguishable at all three sites. However, rare species and parts difficult to identify such as ribs seem more frequently associated with errors of identification. Comparisons with the indeterminate fraction indicate that large game is over-represented in the ZooMS sample at two of the three sites. These differences possibly signal differential fragmentation of elements from large species. Collagen fingerprinting can produce critical insights on the range distribution of animal prey in the past while also contributing to improved models of taphonomic processes and subsistence behavior.

New insights on interpersonal violence in the Late Pleistocene based on the Nile valley cemetery of Jebel Sahaba.

The remains of 61 individuals buried in the cemetery of Jebel Sahaba (site 117) offer unique and substantial evidence to the emergence of violence in the Nile Valley at the end of the Late Pleistocene. Excavated and assessed in the 1960s, some of the original findings and interpretations are disputed. A full reanalysis of the timing, nature and extent of the violence was conducted through the microscopic characterization of the nature of each osseous lesion, and the reassessment of the archaeological data. Over 100 previously undocumented healed and unhealed lesions were identified on both new and/or previously identified victims, including several embedded lithic artefacts. Most trauma appears to be the result of projectile weapons and new analyses confirm for the first time the repetitive nature of the interpersonal acts of violence. Indeed, a quarter of the skeletons with lesions exhibit both healed and unhealed trauma. We dismiss the hypothesis that Jebel Sahaba reflects a single warfare event, with the new data supporting sporadic and recurrent episodes of inter-personal violence, probably triggered by major climatic and environmental changes. At least 13.4 ka old, Jebel Sahaba is one of the earliest sites displaying interpersonal violence in the world.

Characterisation of charred organic matter in micromorphological thin sections by means of Raman spectroscopy.

Burned or charred organic matter in anthropogenic combustion features may provide important clues about past human activities related to fire. To interpret archaeological hearths, a correct identification of the organic source material is key. In the present work, Raman spectroscopy is applied to characterise the structural properties of char produced in laboratory heating- and open-fire experiments. This reference data set is compared to analyses of three different archaeological sites with Middle Palaeolithic combustion contexts. The results show that it is possible to determine whether a charred fragment is the product of burning animal-derived matter (e.g. meat) or plant-derived matter (e.g. wood) by plotting a few Raman spectral parameters (i.e. position of G and D bands, and intensity ratios H D/H G and H V/H G) against one another. The most effective parameters for discriminating animal- from plant-derived matter are the position of the G band and the H V/H G intensity ratio. This method can be applied on raw sample material and on uncovered micromorphological thin sections. The latter greatly compliments micromorphology by providing information about char fragments without any clear morphological characteristics. This study is the first of its kind and may provide archaeologists with a robust new method to distinguish animal- from plant-derived char in thin sections. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s12520-020-01263-3.

The Spy VI child: a newly discovered Neandertal infant.

Spy cave (Jemeppe-sur-Sambre, Belgium) is reputed for the two adult Neandertal individuals discovered in situ in 1886. Recent reassessment of the Spy collections has allowed direct radiocarbon dating of these individuals. The sorting of all of the faunal collections has also led to the discovery of the remains of a Neandertal child, Spy VI. This individual is represented by two mandibular corpus fragments. The left fragment is the most complete and both sides preserve the mental foramen. Four deciduous teeth are associated with these mandibular remains: three incisors and one canine. The lower left canine (Spy 645a) conjoins with the corresponding alveolar socket in the left part of the mandible. Following extant standards, the developmental stage of the preserved teeth indicate an age at death of about one and a half years. In addition to performing a classical morphometric comparative study of the mandible and teeth, we have evaluated the dental tissue proportions using high-resolution microtomographic techniques. Our results show that Spy VI generally falls within the Neandertal range of variation. However, this specimen also exhibits particular traits, notably in the dental internal structural organization, which reveals that variation in the immature Neandertal variation is larger than what was variation currently represented by the available fossil record. These observations demonstrate the need for investigating the frequency and expression of immature Neandertal traits in fossil anterior teeth, as well as their temporal and geographic variation. Direct radiocarbon dating of the Spy VI specimen has been conducted in two different laboratories. The results of Spy VI confirm the age previously determined for the two adults, making the Spy Neandertal remains the youngest ever directly dated in northwest Europe.

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.

The evolutionary history of Neanderthal and Denisovan Y chromosomes.

Ancient DNA has provided new insights into many aspects of human history. However, we lack comprehensive studies of the Y chromosomes of Denisovans and Neanderthals because the majority of specimens that have been sequenced to sufficient coverage are female. Sequencing Y chromosomes from two Denisovans and three Neanderthals shows that the Y chromosomes of Denisovans split around 700 thousand years ago from a lineage shared by Neanderthals and modern human Y chromosomes, which diverged from each other around 370 thousand years ago. The phylogenetic relationships of archaic and modern human Y chromosomes differ from the population relationships inferred from the autosomal genomes and mirror mitochondrial DNA phylogenies, indicating replacement of both the mitochondrial and Y chromosomal gene pools in late Neanderthals. This replacement is plausible if the low effective population size of Neanderthals resulted in an increased genetic load in Neanderthals relative to modern humans.

Modern human cranial diversity in the Late Pleistocene of Africa and Eurasia: evidence from Nazlet Khater, Pestera cu Oase, and Hofmeyr.

The origin and evolutionary history of modern humans is of considerable interest to paleoanthropologists and geneticists alike. Paleontological evidence suggests that recent humans originated and expanded from an African lineage that may have undergone demographic crises in the Late Pleistocene according to archaeological and genetic data. This would suggest that extant human populations derive from, and perhaps sample a restricted part of the genetic and morphological variation that was present in the Late Pleistocene. Crania that date to Marine Isotope Stage 3 should yield information pertaining to the level of Late Pleistocene human phenotypic diversity and its evolution in modern humans. The Nazlet Khater (NK) and Hofmeyr (HOF) crania from Egypt and South Africa, together with penecontemporaneous specimens from the Pestera cu Oase in Romania, permit preliminary assessment of variation among modern humans from geographically disparate regions at this time. Morphometric and morphological comparisons with other Late Pleistocene modern human specimens, and with 23 recent human population samples, reveal that elevated levels of variation are present throughout the Late Pleistocene. Comparison of Holocene and Late Pleistocene craniometric variation through resampling analyses supports hypotheses derived from genetic data suggesting that present phenotypic variation may represent only a restricted part of Late Pleistocene human diversity. The Nazlet Khater, Hofmeyr, and Oase specimens provide a unique glimpse of that diversity.