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.

Grey wolf genomic history reveals a dual ancestry of dogs.

The grey wolf (Canis lupus) was the first species to give rise to a domestic population, and they remained widespread throughout the last Ice Age when many other large mammal species went extinct. Little is known, however, about the history and possible extinction of past wolf populations or when and where the wolf progenitors of the present-day dog lineage (Canis familiaris) lived1-8. Here we analysed 72 ancient wolf genomes spanning the last 100,000 years from Europe, Siberia and North America. We found that wolf populations were highly connected throughout the Late Pleistocene, with levels of differentiation an order of magnitude lower than they are today. This population connectivity allowed us to detect natural selection across the time series, including rapid fixation of mutations in the gene IFT88 40,000-30,000 years ago. We show that dogs are overall more closely related to ancient wolves from eastern Eurasia than to those from western Eurasia, suggesting a domestication process in the east. However, we also found that dogs in the Near East and Africa derive up to half of their ancestry from a distinct population related to modern southwest Eurasian wolves, reflecting either an independent domestication process or admixture from local wolves. None of the analysed ancient wolf genomes is a direct match for either of these dog ancestries, meaning that the exact progenitor populations remain to be located.

The genomic history of southeastern Europe.

Farming was first introduced to Europe in the mid-seventh millennium bc, and was associated with migrants from Anatolia who settled in the southeast before spreading throughout Europe. Here, to understand the dynamics of this process, we analysed genome-wide ancient DNA data from 225 individuals who lived in southeastern Europe and surrounding regions between 12000 and 500 bc. We document a west-east cline of ancestry in indigenous hunter-gatherers and, in eastern Europe, the early stages in the formation of Bronze Age steppe ancestry. We show that the first farmers of northern and western Europe dispersed through southeastern Europe with limited hunter-gatherer admixture, but that some early groups in the southeast mixed extensively with hunter-gatherers without the sex-biased admixture that prevailed later in the north and west. We also show that southeastern Europe continued to be a nexus between east and west after the arrival of farmers, with intermittent genetic contact with steppe populations occurring up to 2,000 years earlier than the migrations from the steppe that ultimately replaced much of the population of northern Europe.

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.

Stable isotope evidence of human diet in Mediterranean context during the Last Glacial Maximum.

The Final Gravettian in Europe overlapped with the cold and dry climatic event of Heinrich 2 (ca. 27-23.5 kyr cal BP), which caused the contraction of human distribution over refuge regions in the southern peninsulas of Europe. Here, we consider the human subsistence in the northeast Iberian Peninsula, where an extensive range of small to large prey was available. Four human remains from the Serinyà caves were investigated using the stable isotope ratios of carbon, nitrogen, and sulfur of bulk collagen (δ13Ccoll, δ15Ncoll, δ34Scoll) and of phenylalanine and glutamine amino acids (δ15NPhe, δ15NGlu). Direct AMS dating of the human and animal remains from the Final Gravettian levels of Mollet III, Reclau Viver, and Arbreda at Serinyà confirmed their chronological position from 27.5 to 22.6 kyr cal BP and the occurrence of four different human individuals. The δ13Ccoll and δ15Ncoll values showed a large contribution of terrestrial prey to the dietary protein of the individuals. The δ34Scoll values were consistent with a subsistence based on the local continental resources, without detectable contribution of marine resource. The δ15NPhe and δ15NGlu values confirm that freshwater resources were not a substantial component of the diet of the considered individuals. Contrast in the isotopic amounts in bulk collagen could be interpreted as the result of different proportions of terrestrial prey in human diet at Serinyà. Altogether, the isotopic investigation reveals the importance of terrestrial over aquatic resources in the subsistence of the studied Final Gravettian individuals from the Serinyà caves in northeastern Iberia during the Last Glacial Maximum. It would be consistent with a scenario of a productive enough terrestrial ecosystem to sustain hunter-gatherer subsistence in this refuge region.

Adapt or die-Response of large herbivores to environmental changes in Europe during the Holocene.

Climate warming and human landscape transformation during the Holocene resulted in environmental changes for wild animals. The last remnants of the European Pleistocene megafauna that survived into the Holocene were particularly vulnerable to changes in habitat. To track the response of habitat use and foraging of large herbivores to natural and anthropogenic changes in environmental conditions during the Holocene, we investigated carbon (δ13 C) and nitrogen (δ15 N) stable isotope composition in bone collagen of moose (Alces alces), European bison (Bison bonasus) and aurochs (Bos primigenius) in Central and Eastern Europe. We found strong variations in isotope compositions in the studied species throughout the Holocene and diverse responses to changing environmental conditions. All three species showed significant changes in their δ13 C values reflecting a shift of foraging habitats from more open in the Early and pre-Neolithic Holocene to more forest during the Neolithic and Late Holocene. This shift was strongest in European bison, suggesting higher plasticity, more limited in moose, and the least in aurochs. Significant increases of δ15 N values in European bison and moose are evidence of a diet change towards more grazing, but may also reflect increased nitrogen in soils following deglaciation and global temperature increases. Among the factors explaining the observed isotope variations were time (age of samples), longitude and elevation in European bison, and time, longitude and forest cover in aurochs. None of the analysed factors explained isotope variations in moose. Our results demonstrate the strong influence of natural (forest expansion) and anthropogenic (deforestation and human pressure) changes on the foraging ecology of large herbivores, with forests playing a major role as a refugial habitat since the Neolithic, particularly for European bison and aurochs. We propose that high flexibility in foraging strategy was the key for survival of large herbivores in the changing environmental conditions of the Holocene.

Prey-to-fox isotopic enrichment of 34 S in bone collagen: Implications for paleoecological studies.

RATIONALE: The trophic enrichment factor (TEF) is a parameter reflecting the difference in isotopic ratio between a consumer's tissues and diet, used in isotopic ecology and paleoecology to track dietary habits. The TEF of sulfur is believed to be low, but was, until now, only documented in a limited number of taxa. In this study we use a subfossil accumulation of bones from a red fox (Vulpes vulpes) den to verify the TEF for sulfur in fox bone collagen. METHODS: Collagen was extracted from 30 samples of subfossil bones, including foxes and their prey. The δ34 S values of the bone collagen samples were measured with an elemental analyzer connected to an isotope ratio mass spectrometer. The TEF was calculated as [Δ34 S = (mean δ34 S in predator) - (mean δ34 S in prey)], using taphonomic indices to estimate the mean diet, and calculated separately for different age classes of the predator. RESULTS: We modeled 12 variants of TEF for different estimations of the diet composition and for three fox age classes (adult, subadult, and juvenile). The estimated TEF values range from -0.54 to +0.03‰ and are similar to TEFs known for other mammals. Absolute TEF values are nearly equal to or lower than the analytical error, which is ±0.4‰. CONCLUSIONS: For the first time, we present direct δ34 S data for the bone collagen of a free-living predator and its naturally selected prey. Our results indicate very low or even slightly negative TEF values for sulfur. Furthermore, according to our results, the δ34 S value should not be considered a reliable indicator of trophic position in terrestrial food webs but rather, it should be used to disentangle different food webs based on different primary producers.

Ecological niche of Neanderthals from Spy Cave revealed by nitrogen isotopes of individual amino acids in collagen.

This study provides a refined view on the diet and ecological niche of Neanderthals. The traditional view is that Neanderthals obtained most of their dietary protein from terrestrial animals, especially from large herbivores that roamed the open landscapes. Evidence based on the conventional carbon and nitrogen isotopic composition of bulk collagen has supported this view, although recent findings based on plant remains in the tooth calculus, microwear analyses, and small game and marine animal remains from archaeological sites have raised some questions regarding this assumption. However, the lack of a protein source other than meat in the Neanderthal diet may be due to methodological difficulties in defining the isotopic composition of plants. Based on the nitrogen isotopic composition of glutamic acid and phenylalanine in collagen for Neanderthals from Spy Cave (Belgium), we show that i) there was an inter-individual dietary heterogeneity even within one archaeological site that has not been evident in bulk collagen isotopic compositions, ii) they occupied an ecological niche different from those of hyenas, and iii) they could rely on plants for up to ∼20% of their protein source. These results are consistent with the evidence found of plant consumption by the Spy Neanderthals, suggesting a broader subsistence strategy than previously considered.

Carbon and nitrogen stable isotopes of well-preserved Middle Pleistocene bone collagen from Schöningen (Germany) and their paleoecological implications.

Carbon and nitrogen stable isotopes in bone collagen can provide valuable information about the diet and habitat of mammal species. However, bone collagen degrades in normal circumstances very rapidly, and isotope analyses are therefore usually restricted to fossil material with a Late Pleistocene or Holocene age. The Middle Pleistocene site of Schöningen, dated to around 300,000 years ago, yielded bones and teeth with an exceptionally good state of collagen preservation. This allowed us to measure reliable biogenic carbon and nitrogen stable isotope ratios for different herbivorous taxa from the families Elephantidae, Rhinocerotidae, Equidae, Cervidae, and Bovidae. The results provide insights regarding the paleoenvironmental setting in which Middle Pleistocene hominins operated. The vegetation consumed by the herbivores from the famous spear horizon originates from open environments. During the climatic Reinsdorf Interglacial optimum, the landscape seems to have been relatively open as well, but certainly included parts that were forested. The results also indicate some niche partitioning; different herbivore species used different plant resources. For instance, the horses seem to have been predominantly browsers, while the straight-tusked elephants were feeding chiefly on grass.

Investigation of equid paleodiet from Schöningen 13 II-4 through dental wear and isotopic analyses: Archaeological implications.

The paleodietary traits of the equid population from Schöningen 13 II-4 were investigated through tooth mesowear and microwear analyses, as well as stable isotopic analyses. The mesowear pattern observed on the upper teeth indicates a low abrasion diet with a significant amount of browse in the diet of the horses. The tooth microwear analysis and the isotopic data confirm that the horses from Schöningen 13 II-4 were mixed feeders, like many populations from other Pleistocene localities in Northern and Eastern Europe. Microwear also provides information on seasonal changes in the diet of the horses and offers the possibility to test hypotheses about the presence of one or several horse populations. Our analysis determined that the assemblage of horse remains from Schöningen 13 II-4 resulted from multiple accumulation events, which took place at different periods of time.

Evidence for a (15)N positive excursion in terrestrial foodwebs at the Middle to Upper Palaeolithic transition in south-western France: Implications for early modern human palaeodiet and palaeoenvironment.

The Middle to Upper Palaeolithic transition around 35,000 years ago coincides with the replacement of Neanderthals by anatomically modern humans in Europe. Several hypotheses have been suggested to explain this replacement, one of them being the ability of anatomically modern humans to broaden their dietary spectrum beyond the large ungulate prey that Neanderthals consumed exclusively. This scenario is notably based on higher nitrogen-15 amounts in early Upper Palaeolithic anatomically modern human bone collagen compared with late Neanderthals. In this paper, we document a clear increase of nitrogen-15 in bone collagen of terrestrial herbivores during the early Aurignacian associated with anatomically modern humans compared with the stratigraphically older Châtelperronian and late Mousterian fauna associated with Neanderthals. Carnivores such as wolves also exhibit a significant increase in nitrogen-15, which is similar to that documented for early anatomically modern humans compared with Neanderthals in Europe. A shift in nitrogen-15 at the base of the terrestrial foodweb is responsible for such a pattern, with a preserved foodweb structure before and after the Middle to Upper Palaeolithic transition in south-western France. Such an isotopic shift in the terrestrial ecosystem may be due to an increase in aridity during the time of deposition of the early Aurignacian layers. If it occurred across Europe, such a shift in nitrogen-15 in terrestrial foodwebs would be enough to explain the observed isotopic trend between late Neanderthals and early anatomically modern humans, without any significant change in the diet composition at the Middle to Upper Palaeolithic transition.

A refined proposal for the origin of dogs: the case study of Gnirshöhle, a Magdalenian cave site.

Dogs are known to be the oldest animals domesticated by humans. Although many studies have examined wolf domestication, the geographic and temporal origin of this process is still being debated. To address this issue, our study sheds new light on the early stages of wolf domestication during the Magdalenian period (16-14 ka cal BP) in the Hegau Jura region (Southwestern Germany and Switzerland). By combining morphology, genetics, and isotopes, our multidisciplinary approach helps to evaluate alternate processes driving the early phases of domestication. The isotope analysis uncovered a restricted, low δ15N protein diet for all analyzed Gnirshöhle specimens, while morphological examinations and phylogenetic relationships did not unequivocally assign them to one or the other canid lineage. Intriguingly, the newly generated mitochondrial canid genomes span the entire genetic diversity of modern dogs and wolves. Such high mitochondrial diversity could imply that Magdalenian people tamed and reared animals originating from different wolf lineages. We discuss our results in light of three ecological hypotheses and conclude that both domestication and the existence of a specialized wolf ecomorph are highly probable. However, due to their proximity to humans and a restricted diet, we propose domestication as the most likely scenario explaining the patterns observed herein.

Ancient DNA sequences point to a large loss of mitochondrial genetic diversity in the saiga antelope (Saiga tatarica) since the Pleistocene.

Prior to the Holocene, the range of the saiga antelope (Saiga tatarica) spanned from France to the Northwest Territories of Canada. Although its distribution subsequently contracted to the steppes of Central Asia, historical records indicate that it remained extremely abundant until the end of the Soviet Union, after which its populations were reduced by over 95%. We have analysed the mitochondrial control region sequence variation of 27 ancient and 38 modern specimens, to assay how the species' genetic diversity has changed since the Pleistocene. Phylogenetic analyses reveal the existence of two well-supported, and clearly distinct, clades of saiga. The first, spanning a time range from >49,500 (14) C ybp to the present, comprises all the modern specimens and ancient samples from the Northern Urals, Middle Urals and Northeast Yakutia. The second clade is exclusive to the Northern Urals and includes samples dating from between 40,400 to 10,250 (14) C ybp. Current genetic diversity is much lower than that present during the Pleistocene, an observation that data modelling using serial coalescent indicates cannot be explained by genetic drift in a population of constant size. Approximate Bayesian Computation analyses show the observed data is more compatible with a drastic population size reduction (c. 66-77%) following either a demographic bottleneck in the course of the Holocene or late Pleistocene, or a geographic fragmentation (followed by local extinction of one subpopulation) at the Holocene/Pleistocene transition.

Fox dietary ecology as a tracer of human impact on Pleistocene ecosystems.

Nowadays, opportunistic small predators, such as foxes (Vulpes vulpes and Vulpes lagopus), are well known to be very adaptable to human modified ecosystems. However, the timing of the start of this phenomenon in terms of human impact on ecosystems and of the implications for foxes has hardly been studied. We hypothesize that foxes can be used as an indicator of past human impact on ecosystems, as a reflection of population densities and consequently to track back the influence of humans on the Pleistocene environment. To test this hypothesis, we used stable isotope analysis (δ13C, δ15N) of bone collagen extracted from faunal remains from several archaeological sites located in the Swabian Jura (southwest Germany) and covering a time range over three important cultural periods, namely the Middle Palaeolithic (older than 42,000 years ago) attributed to Neanderthals, and the early Upper Palaeolithic periods Aurignacian and Gravettian (42,000 to 30,000 years ago) attributed to modern humans. We then ran Bayesian statistic systems (SIBER, mixSIAR) to reconstruct the trophic niches and diets of Pleistocene foxes. We observed that during the Middle Palaeolithic period, when Neanderthals sparsely populated the Swabian Jura, the niches occupied by foxes suggest a natural trophic behavior. In contrast, during the early Upper Palaeolithic periods, a new trophic fox niche appeared, characterized by a restricted diet on reindeer. This trophic niche could be due to the consumption of human subsidies related to a higher human population density and the resulting higher impact on the Pleistocene environment by modern humans compared to Neanderthals. Furthermore, our study suggests that, a synanthropic commensal behavior of foxes started already in the Aurignacian, around 42,000 years ago.

Author Correction: Heavy reliance on plants for Romanian cave bears evidenced by amino acid nitrogen isotope analysis.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Heavy reliance on plants for Romanian cave bears evidenced by amino acid nitrogen isotope analysis.

Heavy reliance on plants is rare in Carnivora and mostly limited to relatively small species in subtropical settings. The feeding behaviors of extinct cave bears living during Pleistocene cold periods at middle latitudes have been intensely studied using various approaches including isotopic analyses of fossil collagen. In contrast to cave bears from all other regions in Europe, some individuals from Romania show exceptionally high δ15N values that might be indicative of meat consumption. Herbivory on plants with high δ15N values cannot be ruled out based on this method, however. Here we apply an approach using the δ15N values of individual amino acids from collagen that offsets the baseline δ15N variation among environments. The analysis yielded strong signals of reliance on plants for Romanian cave bears based on the δ15N values of glutamate and phenylalanine. These results could suggest that the high variability in bulk collagen δ15N values observed among cave bears in Romania reflects niche partitioning but in a general trophic context of herbivory.

Out of Africa by spontaneous migration waves.

Hominin evolution is characterized by progressive regional differentiation, as well as migration waves, leading to anatomically modern humans that are assumed to have emerged in Africa and spread over the whole world. Why or whether Africa was the source region of modern humans and what caused their spread remains subject of ongoing debate. We present a spatially explicit, stochastic numerical model that includes ongoing mutations, demic diffusion, assortative mating and migration waves. Diffusion and assortative mating alone result in a structured population with relatively homogeneous regions bound by sharp clines. The addition of migration waves results in a power-law distribution of wave areas: for every large wave, many more small waves are expected to occur. This suggests that one or more out-of-Africa migrations would probably have been accompanied by numerous smaller migration waves across the world. The migration waves are considered "spontaneous", as the current model excludes environmental or other extrinsic factors. Large waves preferentially emanate from the central areas of large, compact inhabited areas. During the Pleistocene, Africa was the largest such area most of the time, making Africa the statistically most likely origin of anatomically modern humans, without a need to invoke additional environmental or ecological drivers.

Stable isotopes reveal patterns of diet and mobility in the last Neandertals and first modern humans in Europe.

Correlating cultural, technological and ecological aspects of both Upper Pleistocene modern humans (UPMHs) and Neandertals provides a useful approach for achieving robust predictions about what makes us human. Here we present ecological information for a period of special relevance in human evolution, the time of replacement of Neandertals by modern humans during the Late Pleistocene in Europe. Using the stable isotopic approach, we shed light on aspects of diet and mobility of the late Neandertals and UPMHs from the cave sites of the Troisième caverne of Goyet and Spy in Belgium. We demonstrate that their diet was essentially similar, relying on the same terrestrial herbivores, whereas mobility strategies indicate considerable differences between Neandertal groups, as well as in comparison to UPMHs. Our results indicate that UPMHs exploited their environment to a greater extent than Neandertals and support the hypothesis that UPMHs had a substantial impact not only on the population dynamics of large mammals but also on the whole structure of the ecosystem since their initial arrival in Europe.