Neanderthals and humans interbred in Europe for 5,400 years

A mysterious small human species coexisted with modern man in China until at least 10,500 years ago, scientists have announced, based on an analysis of an anomalous thigh bone found in a cave. The discovery brings the number of human species coexisting until very recently to three: us, this new one and the so-called hobbit (Homo floresiensis) that survived on the Indonesian island of Flores until at least 13,000 years ago.



The thigh bone found in Red Deer Cave in Yunnan Province is about 14,000 years old and is substantially different from a modern man’s, Prof. Darren Curnoe of the University of New South Wales and Prof. Ji Xueping of the Yunnan Institute of Cultural Relics and Archaeology report in PLOS ONE. The bone is more similar to those possessed by Homo habilis and early Homo erectus, which predated man by some 1.5 million years. Like habilis, the scientists say, the Maludong (Red Deer Cave) thigh bone is tiny. And like the hobbit, this hominin was a half-pint, apparently weighing around 50 kilos.



Actually, the Red Deer Cave people had been discovered decades ago. Bones, including a partial skull, had been found at Longlin Cave in the Guangxi Zhuang region in 1979. The thigh bone at Maludong was found in 1989 and has sat in a museum in Yunnan ever since. Eventually a study began on the remains, starting with the skull bits found at Longlin. Thus in 2012 Curnoe, Ji and their team announced the discovery of the mystery “deer people” at Maludong and in Longlin Cave in nearby Guangxi. Then it hit the fan: Was it a new species of archaic human or some sort of hybrid?



One thing that’s sure is that the Red Cave Deerites didn’t look like us. They had flat short faces, no chin and archaic big teeth. Their skulls were thicker than ours but their brains had modern-looking frontal lobes, the team wrote in 2012. As for age, the Longlin skull and bones were dated between 10,500 and 14,300 years old. The Maludong bones were recovered during excavations from a single layer dated between about 14,300 and 13,600 years old, according to radiocarbon analysis of charcoal, Curnoe says, adding: “It is unlikely to be any younger.”



The unusually primitive nature of the bones, coupled with their relatively young age, has raised some startling implications—and this discovery is expected to be controversial because, until now, it had been thought that the youngest pre-modern humans on mainland Eurasia - the Neanderthals of Europe and West Asia, and the 'Denisovans' of southern Siberia - died out about 40,000 years ago, soon after modern humans entered the region. The new find shows that at least one pre-modern species overlapped in time with modern humans in mainland East Asia for tens of thousands of years.



“The Maludong individual might represent a relic, tropically adapted, pre-modern population that survived relatively late in the biogeographically complex region of southwest China,” reported Curnoe, Ji and colleagues. “It is intriguing that such a primitive looking species could have survived at Maludong until near the end of the Ice Age, until about 14,000 years ago. Yunnan Province in southwest China is a remarkable place with a very complex topography resulting from the uplift of the Himalayan Mountains (Qinghai Tibetan Plateau) and the building up of the Indochina block due to plate tectonics. The result is that it has a highly varied and highly unusual set of plant and animal communities and species, with many having persisted in isolation for hundreds of thousands or millions of years……the region around Maludong is also biogeographically on the northern edge of tropical Southeast Asia, and at the time the Maludong cave deposit was formed, it would have been warmer and wetter than today.”** Adds Curnoe: "This is exciting because it shows the bones from Maludong, after 25 years of neglect, still have an incredible story to tell. There seems to have been a diversity of different kinds of human living until very recently in southwest China.”



Curnoe and colleagues are guarded about assigning the finds to a new species at present. “It is certainly possible that the Maludong femur represents a new species,” they report. “The problem at present is that there simply aren’t many pre-modern femora from East Asia with which to compare the Maludong specimen. It may even be that there were different species living on mainland East Asia during the last Ice Age, from what we see in Europe or Africa at the time…..[but] we can’t narrow down just yet which species the Maludong bone belongs to, other than to state that it strongly resembles early pre-modern groups like Homo habilis.”**

Figure 1: Site locations and final boundary age ranges for Mousterian and Neanderthal sites.

European Palaeolithic sites contain the best evidence for the replacement of one human group (Neanderthals) by another (AMHs)1. The nature and process of the replacement, both in cultural and genetic terms, has been the focus of extensive research1, 6, 7. Recent studies of complete Neanderthal and modern human genomic sequences suggest that Neanderthals and AMHs interbred outside Africa7. This resulted in an introgression of 1.5–2.1% of Neanderthal-derived DNA8, or perhaps more9, in all modern non-African human populations. The analysis of three Neanderthal mitochondrial DNA (mtDNA) genomes from Denisova (Russian Altai), Vindija (Croatia) and Mezmaiskaya (Russian North Caucasus) indicates that the greatest amount of gene flow into non-African AMHs occurred after these Neanderthal populations had separated from each other8. At present it is not clear whether interbreeding occurred once or several times outside Africa10, or where it happened. After the interbreeding episode(s), Neanderthals and their distinctive material culture disappeared and were replaced across Eurasia by AMHs, but the precise timing of this has remained difficult to identify in the absence of a reliable chronological framework3.

We obtained 196 AMS radiocarbon measurements and used them to build high-precision age models using Bayesian statistics on the OxCal20 platform. This allows us to incorporate stratigraphic and other relative age information, along with the calibrated likelihoods for each site. Probability distribution functions (PDFs) corresponding with the temporal boundaries of the latest Mousterian occupations were generated (Fig. 1b and Supplementary Methods). The results show that the Mousterian end boundary PDFs all fall before 40,000 calibrated years (cal) BP (all probability ranges are expressed at 95.4%) (Fig. 1b). When placed into a single phase Bayesian model, the PDFs result in an overall end boundary ranging from 41,030–39,260 cal BP (Fig. 1c and Supplementary Methods). This PDF represents the age of the latest European Mousterian on the basis of our data.


Figure 2: Transitional site locations and Bayesian age ranges for the start and end of the Châtelperronian and Uluzzian technocomplexes.

The temporal range of the ‘transitional’ technocomplexes was also examined. With regard to the Châtelperronian, it is apparent on stratigraphic grounds that the Mousterian precedes it at all sites where both occur. However, our results show that the Châtelperronian at some sites (for example, Arcy-sur-Cure) starts statistically significantly before the end of the Mousterian at other sites in Europe such as Abric Romaní and Geissenklösterle (Germany). If Neanderthals were responsible for both Mousterian and Châtelperronian, the implication is that there was considerable regional variation in their behaviour and adaptation strategies during this transition period. Assuming that the Châtelperronian is associated with Neanderthals, we combined the end boundaries for both into a single-phase Bayesian model and obtained a final ‘Neanderthal’ end PDF of 40,890–39,220 cal BP. The result is indistinguishable from the final Mousterian PDF, showing that uncertainty over the authorship of the Châtelperronian does not affect the age estimated for the last Neanderthals; they did not survive after ~41,000–39,000 cal BP (Fig. 2b).

By comparing the final Neanderthal PDF with those obtained for the start of the Uluzzian at the Cavallo site23, we can quantify the temporal overlap between Neanderthals and the earliest western European AMHs (Fig. 2b). The difference is significant and ranges from 2,600 to 5,400 years at 95.4% probability. Coexistence has been linked previously with the possibility of cultural transmission from AMHs to Neanderthals, termed ‘acculturation’24, as a means of accounting for late Neanderthal technical and behavioural development. The early presence of AMHs in Mediterranean Europe by ~45,000–43,000 cal BP (ref. 23) and the potential overlapping time may have acted as a stimulus for putative Neanderthal innovative and symbolic behaviour in the millennia before their disappearance. When we compare the start and end boundary PDFs for both Uluzzian and Châtelperronian sites we observe that they are very similar (Fig. 2b). This may provide further support for an acculturation model. Alternatively, this similarity in the start dates of the two industries might be seen as reflecting an AMH authorship for both. If this were the case, then the distribution of early modern humans would be wider than expected. Since the physical evidence linking these industries to different human groups is scarce, these interpretations are potentially prone to change with new excavation data.


Figure 3: Time slices for western Europe between 45,000 and 40,000 cal BP showing the distribution of the Mousterian, Châtelperronian and Uluzzian modelled ages.

High-precision chronometric data and Bayesian modelling allows us to map the spatiotemporal relationship between the three technocomplexes during the period ~45,000–41,000 cal BP as a series of time slices (Fig. 3 and Supplementary Methods). Since there is little to no robust evidence for interstratification of the transitional industries within Mousterian archaeological layers, we conclude that the chronological overlap observed must have also involved a degree of spatial separation between the two populations, regardless of whether Neanderthals were responsible for the Châtelperronian or not. In turn, this suggests that the dispersal of early AMHs was initially geographically circumscribed, proceeding step-wise, with the Uluzzian first and the Aurignacian following a few millennia later. The transitional industries, including those not analysed here, may be broadly contemporaneous technocomplexes that remained spatially distinct from one another. Rather than a rapid model of replacement of autochthonous European Neanderthals by incoming AMHs, our results support a more complex picture, one characterized by a biological and cultural mosaic that lasted for several thousand years.

The timing of Neanderthal disappearance and the extent to which they overlapped with the earliest incoming anatomically modern humans (AMHs) in Eurasia are key questions in palaeoanthropology1, 2. Determining the spatiotemporal relationship between the two populations is crucial if we are to understand the processes, timing and reasons leading to the disappearance of Neanderthals and the likelihood of cultural and genetic exchange. Serious technical challenges, however, have hindered reliable dating of the period, as the radiocarbon method reaches its limit at ~50,000 years ago3. Here we apply improved accelerator mass spectrometry 14C techniques to construct robust chronologies from 40 key Mousterian and Neanderthal archaeological sites, ranging from Russia to Spain. Bayesian age modelling was used to generate probability distribution functions to determine the latest appearance date. We show that the Mousterian ended by 41,030–39,260 calibrated years BP (at 95.4% probability) across Europe. We also demonstrate that succeeding ‘transitional’ archaeological industries, one of which has been linked with Neanderthals (Châtelperronian)4, end at a similar time. Our data indicate that the disappearance of Neanderthals occurred at different times in different regions. Comparing the data with results obtained from the earliest dated AMH sites in Europe, associated with the Uluzzian technocomplex5, allows us to quantify the temporal overlap between the two human groups. The results reveal a significant overlap of 2,600–5,400 years (at 95.4% probability). This has important implications for models seeking to explain the cultural, technological and biological elements involved in the replacement of Neanderthals by AMHs. A mosaic of populations in Europe during the Middle to Upper Palaeolithic transition suggests that there was ample time for the transmission of cultural and symbolic behaviours, as well as possible genetic exchanges, between the two groups.

Nature 512, 306–309 (21 August 2014) doi:10.1038/nature13621