Annamaria Ronchitelli

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.

The timing and spatiotemporal patterning of Neanderthal disappearance

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 palaeoanthropology. 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 ago. 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), 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 technocomplex, 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.

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. We analyze 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 the earliest modern humans in Europe did not contribute substantially to 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. A ~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 during the Ice Age ~19,000 years ago. During the major warming period after ~14,000 years ago, a new genetic component related to present-day Near Easterners appears in Europe. These results document how population turnover and migration have been recurring themes of European pre-history.

Pleistocene Mitochondrial Genomes Suggest a Single Major Dispersal of Non-Africans and a Late Glacial Population Turnover in Europe

How modern humans dispersed into Eurasia and Australasia, including the number of separate expansions and their timings, is highly debated [1, 2]. Two categories of models are proposed for the dispersal of non-Africans: (1) single dispersal, i.e., a single major diffusion of modern humans across Eurasia and Australasia [3-5]; and (2) multiple dispersal, i.e., additional earlier population expansions that may have contributed to the genetic diversity of some present-day humans outside of Africa [6-9]. Many variants of these models focus largely on Asia and Australasia, neglecting human dispersal into Europe, thus explaining only a subset of the entire colonization process outside of Africa [3-5, 8, 9]. The genetic diversity of the first modern humans who spread into Europe during the Late Pleistocene and the impact of subsequent climatic events on their demography are largely unknown. Here we analyze 55 complete human mitochondrial genomes (mtDNAs) of hunter-gatherers spanning ∼35,000 years of European prehistory. We unexpectedly find mtDNA lineage M in individuals prior to the Last Glacial Maximum (LGM). This lineage is absent in contemporary Europeans, although it is found at high frequency in modern Asians, Australasians, and Native Americans. Dating the most recent common ancestor of each of the modern non-African mtDNA clades reveals their single, late, and rapid dispersal less than 55,000 years ago. Demographic modeling not only indicates an LGM genetic bottleneck, but also provides surprising evidence of a major population turnover in Europe around 14,500 years ago during the Late Glacial, a period of climatic instability at the end of the Pleistocene.

A 28,000 years old Cro-Magnon mtDNA sequence differs from all potentially contaminating modern sequences.

Background DNA sequences from ancient speciments may in fact result from undetected contamination of the ancient specimens by modern DNA, and the problem is particularly challenging in studies of human fossils. Doubts on the authenticity of the available sequences have so far hampered genetic comparisons between anatomically archaic (Neandertal) and early modern (Cro-Magnoid) Europeans. Methodology/Principal Findings We typed the mitochondrial DNA (mtDNA) hypervariable region I in a 28,000 years old Cro-Magnoid individual from the Paglicci cave, in Italy (Paglicci 23) and in all the people who had contact with the sample since its discovery in 2003. The Paglicci 23 sequence, determined through the analysis of 152 clones, is the Cambridge reference sequence, and cannot possibly reflect contamination because it differs from all potentially contaminating modern sequences. Conclusions/Significance: The Paglicci 23 individual carried a mtDNA sequence that is still common in Europe, and which radically differs from those of the almost contemporary Neandertals, demonstrating a genealogical continuity across 28,000 years, from Cro-Magnoid to modern Europeans. Because all potential sources of modern DNA contamination are known, the Paglicci 23 sample will offer a unique opportunity to get insight for the first time into the nuclear genes of early modern Europeans.

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.

Comments on “Human-climate interaction during the Early Upper Paleolithic: Testing the hypothesis of an adaptive shift between the Proto-Aurignacian and the Early Aurignacian” by William E. Banks, Francesco d'Errico, João Zilhão

In this brief comment, we intend to reply to issues arising fromthe recently published article by Banks et al. (2013a). Banks et al.’spaper focuses on the human-climate interaction during the Proto-Aurignacian and the Early Aurignacian and on the technologicaland tempo-spatial relationship between these two techno-complexes. In addition, they briefly examine the European transi-tional complexes, and revisit the current debate regarding theauthorshipof theChâtelperronianandtheUluzzian.Inouropinion,Banks et al. (2013a) are selective in their use of stratigraphic (andradiometric) data, and their practice of unjustifiably discarding‘inconvenient’ data, as Banks et al. (2011) explicitly do, is puzzling.Here, we are mainly interested in clarifying questions raisedabout the stratigraphic and chronometric integrity of Grotta delCavallo (Lecce, Southern Italy). Banks et al. (2013a) define as‘tentative at best’ the attribution to anatomically modern humans(AMH) of the two deciduous teeth recovered at Grotta del Cavallo(Benazzi et al., 2011b), suggesting that there are stratigraphic,chronological and definitional issues with the evidence. Surpris-ingly, they do not elaborate in any detail on these assertions.The attribution of the Cavallo teeth to AMH had an obviousimpact on the debate around Neanderthal ‘modern behaviour,’which the Uluzzian evidence was used to support previously (e.g.,Zilhao, 2007). However, the assumption that the makers of tran-sitional assemblages (or of some of them) were modern humansrather than Neandertals does not automatically mean that ‘com-plex’cognitiveskillswereuniquetoAMHs.Thecruxofthematteristhat the concept of ‘modernity’ at issue is based on a completelyrelative and ‘self-referential’ model because ‘modernity’ and itsevolutionary degree are exclusively defined on Homo sapiens pa-rameters (“This is the ultimate fate of Neandertals: to live on asinexact mirrors of ourselves” from Wynn and Coolidge, 2012: 188).Before discussing the purported ‘issue’ with the stratigraphy ofGrotta del Cavallo, it is worth commenting briefly on the criticismraised by Banks et al. (2013a) on the taxonomic determination ofthe two deciduous molars from the Uluzzian levels of the site(Cavallo B and Cavallo C). The authors reject the attribution of theteeth to AMH, proposed by Benazzi et al. (2011b), and instead cite arecent publication by Trinkaus and Zilhao (2012). However,Trinkaus and Zilhao (2012: 392), referring tothe Cavallo teeth, onlystate that “.their morphology is insufficient to establish that theyare indeed from modern humans instead of Neandertals (cf.Churchill and Smith, 2000; Gambassini et al., 2005; Riel-Salvatore,2009)”. This is at least circular. Banks et al. (2013a) do not supplyany morphological or morphometric evidence to support theirclaims, the latter are simply based on previous observations byother scholars whose aim had not been to classify the teeth (i.e.,Riel-Salvatore, 2009) or who had done so on the basis of insuffi-ciently published data (i.e., Churchill and Smith, 2000; Gambassinietal.,2005).ThestudybyBenazzietal.(2011b)specificallytargetedthe taxonomic determination of the deciduous teeth from Grotta

Multistep food plant processing at Grotta Paglicci (Southern Italy) around 32,600 cal B.P.

Significance The Early Gravettian inhabitants of Grotta Paglicci (sublayer 23 A) are currently the most ancient hunter–gatherers able to process plants to obtain flour. They also developed targeted technologies for complex processing of the plant portions before grinding. The present study testifies for the first time, to our knowledge, the performance of a thermal pretreatment that could have been crucial in a period characterized by a climate colder than the current one. The starch record on the Paglicci grinding stone is currently the most ancient evidence of the processing of Avena (oat). Residue analyses on a grinding tool recovered at Grotta Paglicci sublayer 23A [32,614 ± 429 calibrated (cal) B.P.], Southern Italy, have demonstrated that early modern humans collected and processed various plants. The recording of starch grains attributable to Avena (oat) caryopses expands our information about the food plants used for producing flour in Europe during the Paleolithic and about the origins of a food tradition persisting up to the present in the Mediterranean basin. The quantitative distribution of the starch grains on the surface of the grinding stone furnished information about the tool handling, confirming its use as a pestle-grinder, as suggested by the wear-trace analysis. The particular state of preservation of the starch grains suggests the use of a thermal treatment before grinding, possibly to accelerate drying of the plants, making the following process easier and faster. The study clearly indicates that the exploitation of plant resources was very important for hunter–gatherer populations, to the point that the Early Gravettian inhabitants of Paglicci were able to process food plants and already possessed a wealth of knowledge that was to become widespread after the dawn of agriculture.

I ciottoli decorati di Paglicci : raffigurazioni e utilizzo

In this paper we analyze nine pebbles (two of which are unpublished) coming from the mobiliary art assemblage of Paglicci cave (Foggia - Italy). The principals aims of the study are: - To understand the production process of artistic incisions on the pebbles, through the study of the engravings, as the starting point for deciphering their symbolic and cognitive value. Every engraved stroke has in fact retained, at a microscopic level, important technological information and by means of experimental replication of the engravings, it has been possible to retrieve microscopic indexes which allow one to re-create the link between the result of the engraving, the tools used and the action performed. The importance of re-enacting the sequence of actions which led to the creation of the artistic object is given not only by the possibility to understand in depth the technique employed during such events, but, more importantly, by the possibility to test their cultural significance. - To assess the cultural value of the artistic production, also through functional analysis. Engravings, different from cave art which has solely a symbolic value, are in this case carried out on artefacts used in every-day life. The identification of use-wear traces on such objects, or at least on those which possess the necessary characteristics to suggest their likely utilization, is undertaken in an attempt to find out whether such objects were used before and/or after they were engraved. Within the technological study of engravings and the functional analysis of pebbles, the interpretation of the archaeological data has been possible thanks to the comparison with the data obtained through replication under controlled parameters. Technological analysis of the incisions has underlined the employment of various engraving tools, or at least various active edges of the same tool. Strokes are generally redone several times to make them readable. Use-wear analysis has highlighted that the majority of pebbles has been used as retouchers or hammer stones (active percussion). Three pieces show use-wear far from the edges denoting a function of these pebbles as anvil (passive percussion) or mallet (indirect percussion). In two cases the surface has been abraded after utilization and before the engravings. All pebbles have been used before being engraved. This observation may suggest that pebbles, at a certain moment, lost a functional value for a different one. The care employed in preparing and engraving pebbles after utilization denotes the will of using no longer these objects, even though their life continues, as polish following the incisions show.

A spotted hyaena den in the Middle Palaeolithic of Grotta Paglicci (Gargano promontory, Apulia, Southern Italy)

The Palaeolithic sequence of Grotta Paglicci (Gargano promontory, Apulia, Southern Italy) is one of the most important in the Mediterranean area: It comprises the whole Upper Palaeolithic cultural sequence known for the region, as well as Early Middle Palaeolithic and Lower Palaeolithic levels. These earlier phases are best represented in a collapsed room located outside the present-day cave (the so called “external rock shelter”). In this area, a new excavation, started in 2004, brought to light Middle Palaeolithic animal remains associated with evidence of spotted hyaena (SU 64 and 53). The spatial distribution analysis of remains from SU 53 revealed the presence of a bone accumulation area and a wider dispersal of hyaena coprolites. Three main ungulate species (aurochs, fallow deer and red deer) as well as carnivores (spotted hyaena, wolf, fox, wild cat and lynx) and lagomorphs have been identified. The majority of aurochs remains are located in the main accumulation; among these specimens, a complete metatarsal connected with three tarsal bones has been found; a talus and a complete tibia, probably belonging to the same limb, have also been identified. The multidisciplinary study carried out in this paper highlights a specific bone accumulation and scattering pattern in a spotted hyaena (Crocuta crocuta) den. In addition, taphonomy of lagomorph remains indicates the presence of other depositional agents.