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Author contributions: Radiocarbon dating of Neanderthal remains recovered from Vindija Cave Croatia initially revealed surprisingly recent results: This implied the remains could represent a late-surviving, refugial Neanderthal population and suggested they could have been responsible for producing some of the early Upper Paleolithic artefacts more usually produced by anatomically modern humans. This article presents revised radiocarbon dates of the human bones from this site obtained using a more robust purification method targeting the amino acid hydroxyproline.

These revised dates change our interpretation of this important site and demonstrate that the Vindija Neanderthals probably did not overlap temporally with early modern humans. Previous dating of the Vi and Vi Neanderthal remains from Vindija Cave Croatia led to the suggestion that Neanderthals survived there as recently as 28,—29, B. We have redated these same specimens using an approach based on the extraction of the amino acid hydroxyproline, using preparative high-performance liquid chromatography Prep-HPLC.

This method is more efficient in eliminating modern contamination in the bone collagen. The revised dates are older than 40, B. We applied zooarchaeology by mass spectrometry ZooMS to find additional hominin remains. We additionally dated animal bone samples from units G 1 and G 1 —G 3. These dates suggest a co-occurrence of early Upper Paleolithic osseous artifacts, particularly split-based points, alongside the remains of Neanderthals is a result of postdepositional mixing, rather than an association between the two groups, although more work is required to show this definitively.

Significant questions still remain regarding the precise nature of this transition, the humans responsible for the various transitional early Upper Paleolithic industries, the degree of overlap between Neanderthals and modern humans, and the timing of the disappearance of the former. The European record for the transition retains its interest because it is the best-documented sequence for the disappearance of a hominin group available 3. The latest data, both radiometric and genetic, suggest Neanderthals and modern humans coexisted or overlapped for up to several thousand years in Europe until Neanderthal disappearance at around 40, cal B.

Ascertaining the spatial attributes of Neanderthal and modern human populations in Europe is an area of active research, and a reliable chronology remains essential. Our understanding of the biocultural processes involved in the transition have been greatly influenced by improved accelerator mass spectrometry AMS dating methods and their application to directly dating the remains of late Neanderthals and early modern humans, as well as artifacts recovered from the sites they occupied.

It has become clear that there have been major problems with dating reliability and accuracy across the Paleolithic in general, with studies highlighting issues with underestimation of the ages of different dated samples from previously analyzed sites 6. At Mezmaiskaya, the AMS dates obtained for the Neanderthal excavated above the previously dated individual were substantially older 9.

This, along with other AMS dates from cut-marked fauna from the same archaeological horizons, suggested the original date of 29, B. At Zafarraya, Wood et al. In both cases, revised radiocarbon dates produced with more robust chemical pretreatment methods have illustrated significant underestimates in the previous dates that cannot be reconciled with a hypothesis of late-surviving refugial Neanderthals. The Neanderthal fossil remains from level G 1 of Vindija Cave in northern Croatia have remained in the literature as potentially late individuals.

Vi is a right posterior mandible and Vi is a parietal fragment, both showing Neanderthal-specific morphology 11 , OxA Higham et al. OxA-X , which indicated the previous dates were indeed too young. The radiocarbon date for this sample could therefore include a higher molecular weight noncollagenous contaminant, possibly cross-linked to the collagen. On the basis of the potential problems associated with the small size of the redated samples and the potential for remaining contaminants, OxA-X was considered to be a minimum age If the dates are even approximately correct, however, it makes them the most recent known Neanderthals.

This would imply a more extensive temporal overlap between Neanderthals and early modern humans in central Europe than has recently been documented 4. In addition to the Neanderthal remains, level G 1 has yielded a small archaeological assemblage that contains techno-typologically Middle and Upper Paleolithic lithic artifacts plus several distinctively early Upper Paleolithic osseous points It has been argued that the mix of Neanderthals, Middle Paleolithic tools, and Upper Paleolithic technology was the result of cryoturbation and Ursus spelaeus activity in level G 1 , with elements mixing into level G 1 from both the Upper Paleolithic unit F above and the Middle Paleolithic level G 3 below 15 , These alternatives are testable by selecting human and organic osseous points, as well as animal bones, for renewed AMS dating.

This is what we have undertaken and describe here. These included three previously dated Neanderthal specimens Vi, Vi, and Vi In addition, to test the reality of the co-occurrence of earlier Upper Paleolithic bone and antler point artifacts with the Neanderthal remains, we selected six osseous points for dating SI Appendix , Fig. This is an indicator of collagen preservation The results show that only one bone point sample Vi had sufficient levels of nitrogen to warrant full sampling for collagen extraction and AMS dating; the remainder failed and therefore were not sampled further SI Appendix , Table S1.

We also included the sample from a split-based bone point Vi that had been analyzed in the laboratory previously, producing only a small collagen yield. We decided to attempt to redate it, using a larger starting mass of bone powder. Unfortunately, there was insufficient collagen remaining from this sample after pretreatment. See SI Appendix , Fig. S1 for images of the bone points included in this study. We used ZooMS to identify potential hominin bone fragments among the unidentified faunal remains from the G 1 and G 3 levels, as well as the stratigraphic unit G 1 —G 3.

The majority of the samples we analyzed yielded poor collagen preservation, which prevented any identification to genus or taxon. This assemblage is dominated by Ursus , and only six of the 27 taxa identified by morphological study of the bones in Miracle et al. We identified a single hominin specimen Fig. The bone was analyzed using ancient DNA techniques to enable a formal species identification.

The bone yields evidence for a probable cut and gauge marks right upper part of the bone. The picture was taken after the bone had undergone sampling for ZooMS and before sampling for aDNA, radiocarbon, and stable isotope analysis. All tagged peaks A, B, C, D, and F denote sequence-matched peptides observed in human collagen 27 , Genomic analysis based on mitochondrial DNA revealed that all four human specimens fall into Neanderthal mitochondrial variation.

Both Vi As previously published, Vi Because of lower endogenous DNA content in Vi, a full mitochondrial genome could not be reconstructed for the sample. However, from the limited amounts of mitochondrial sequences, we were able to trace most of the observed variants to variations found in previously sequenced Neanderthal mitochondrial genomes SI Appendix , Fig. Nine of the samples selected produced enough collagen or hydroxyproline to be dated by AMS. We also list the dates obtained on two other hominin samples: The different sample pretreatments are also indicated in Table 2.

Radiocarbon dates of the Vindija Neanderthal remains. CRA is conventional radiocarbon age, expressed in years B. PCode refers to pretreatment code; AG is gelatinized filtered collagen, AF is ultrafiltered collagen, XB denotes collagen extracted at a different laboratory than the ORAU, and HYP denotes the extraction of hydroxyproline from hydrolyzed bone collagen 51 , Collagen yield represents the weight of gelatin or ultrafiltered gelatin in milligrams.

When further purification AF or HYP was performed on previously extracted collagen, the yields are not reported. The background carbon derived from the HPLC separation has been accounted for by using a correction where appropriate details can be found in the SI Appendix. Slash indicates data not available. These ages are significantly older than any of the dates obtained previously for these specimens using the AG gelatinized filtered collagen and AF ultrafiltered collagen procedures, and this strongly suggests that noncollagenous high molecular weight contaminants, probably crosslinked to the collagen, were still present in the sample previously dated.

It is only by hydrolyzing the collagen and selecting the hydroxyproline that we were able to successfully remove these contaminants. The error weighted mean is 0. This shows that the results obtained on the three Neanderthal bones from level G 1 are statistically in agreement. The fact that the two dates overlap suggests no significant contamination in this bone. Taken together, these dates show a significantly older occupation of the site by Neanderthals, suggesting the site cannot be considered to be a refugium for late-surviving Neanderthals Fig.

The two other dates obtained on samples Vi The model is a simple phase model in OxCal 4. The calibration curve of Reimer et al. Details can be found in the SI Appendix. Less than mg bone was available, so we applied an AG gelatin treatment to maximize the collagen yield. To test possible perturbation in level G 1 , we also dated four faunal samples identified as originating from levels G 1 and G 1 —G 3 , using ultrafiltration AF.

These samples produced dates that were all greater than or very close to the radiocarbon limit Table 3. These samples are less likely to have been treated with conservation materials than the human bones, and therefore were not prepared using the HPLC method. Three of these faunal bones are from level G 1 Table 1. This shows there is bone of variable radiocarbon age in the G 1 level and suggests the possibility of postdepositional mixing and movement of material.

In consequence, the bone tools cannot be associated with the Neanderthal remains unless further direct radiocarbon dating using the HYP approach is undertaken. Clearly, the low collagen content of the points appears to preclude this at this time. Radiocarbon determinations and analytical data from Vindija faunal remains and bone point. Single-amino acid AMS dating of the Vindija Neanderthals has yielded results that are substantially older than the previous ages that were initially obtained.

The results suggest this group was not a late-surviving refugial Neanderthal population, as previously thought, and means the group almost certainly did not overlap with early anatomically modern humans in this part of Europe. Despite our best attempts, we were not able to date the bone industry associated with the archaeology of level G 1. The one date we obtained from a later stratigraphic unit was younger than 30, B.

The dating of other faunal materials from level G 1 highlighted a significant range in age, which could indicate a perturbation of the general sequence. The question, then, of whether some of the points could have been produced by Neanderthals remains open; however, it is parsimonious to conclude that the split-based point at least must have a maximum age of 32,—34, B. Our perception of the biological transition between Neanderthals and modern humans has changed radically during the last decade.

On the basis of our hydroxyproline dates and the DNA results, the Vindija Neanderthals date before the period when the first modern humans arrived into Europe and interbred with Neanderthals. We used collagen peptide mass fingerprinting or ZooMS to analyze preserved type 1 collagen COL1 from small unidentified bone fragments from the Vindija site.

COL1 is characterized by three polypeptide alpha chains, and within these chains there are small differences in the amino acid sequences among different species. These offer the possibility of identification of species-specific amino acid markers. By comparing these values with a library of known fauna, we identified bones to genus or species in some instance 27 — We used two different methods to prepare the samples for AMS dating.

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Author contributions: Radiocarbon dating of Neanderthal remains recovered from Vindija Cave Croatia initially revealed surprisingly recent results: This implied the remains could represent a late-surviving, refugial Neanderthal population and suggested they could have been responsible for producing some of the early Upper Paleolithic artefacts more usually produced by anatomically modern humans. This article presents revised radiocarbon dates of the human bones from this site obtained using a more robust purification method targeting the amino acid hydroxyproline. These revised dates change our interpretation of this important site and demonstrate that the Vindija Neanderthals probably did not overlap temporally with early modern humans.

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Thank you for visiting nature. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer. In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript. A Nature Research Journal. Current protocols for ancient DNA and radiocarbon analysis of ancient bones and teeth call for multiple destructive samplings of a given specimen, thereby increasing the extent of undesirable damage to precious archaeological material.

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