Publications by authors named "Jean-Jacques Hublin"

193 Publications

Initial Upper Palaeolithic humans in Europe had recent Neanderthal ancestry.

Nature 2021 Apr 7;592(7853):253-257. Epub 2021 Apr 7.

Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

Modern humans appeared in Europe by at least 45,000 years ago, but the extent of their interactions with Neanderthals, who disappeared by about 40,000 years ago, and their relationship to the broader expansion of modern humans outside Africa are poorly understood. Here we present genome-wide data from three individuals dated to between 45,930 and 42,580 years ago from Bacho Kiro Cave, Bulgaria. They are the earliest Late Pleistocene modern humans known to have been recovered in Europe so far, and were found in association with an Initial Upper Palaeolithic artefact assemblage. Unlike two previously studied individuals of similar ages from Romania and Siberia who did not contribute detectably to later populations, these individuals are more closely related to present-day and ancient populations in East Asia and the Americas than to later west Eurasian populations. This indicates that they belonged to a modern human migration into Europe that was not previously known from the genetic record, and provides evidence that there was at least some continuity between the earliest modern humans in Europe and later people in Eurasia. Moreover, we find that all three individuals had Neanderthal ancestors a few generations back in their family history, confirming that the first European modern humans mixed with Neanderthals and suggesting that such mixing could have been common.
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http://dx.doi.org/10.1038/s41586-021-03335-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8026394PMC
April 2021

Assessing the status of the KNM-ER 42700 fossil using Homo erectus neurocranial development.

J Hum Evol 2021 May 29;154:102980. Epub 2021 Mar 29.

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

Based on ontogenetic data of endocranial shape, it has been proposed that a younger than previously assumed developmental status of the 1.5-Myr-old KNM-ER 42700 calvaria could explain why the calvaria of this fossil does not conform to the shape of other Homo erectus individuals. Here, we investigate (ecto)neurocranial ontogeny in H. erectus and assess the proposed juvenile status of this fossil using recent Homo sapiens, chimpanzees (Pan troglodytes), and Neanderthals (Homo neanderthalensis) to model and discuss changes in neurocranial shape from the juvenile to adult stages. We show that all four species share common patterns of developmental shape change resulting in a relatively lower cranial vault and expanded supraorbital torus at later developmental stages. This finding suggests that ectoneurocranial data from extant hominids can be used to model the ontogenetic trajectory for H. erectus, for which only one well-preserved very young individual is known. However, our study also reveals differences in the magnitudes and, to a lesser extent, directions of the species-specific trajectories that add to the overall shared pattern of neurocranial shape changes. We demonstrate that the very young H. erectus juvenile from Mojokerto together with subadult and adult H. erectus individuals cannot be accommodated within the pattern of the postnatal neurocranial trajectory for humans. Instead, the chimpanzee pattern might be a better 'fit' for H. erectus despite their more distant phylogenetic relatedness. The data are also compatible with an ontogenetic shape trajectory that is in some regards intermediate between that of recent H. sapiens and chimpanzees, implying a unique trajectory for H. erectus that combines elements of both extant species. Based on this new knowledge, neurocranial shape supports the assessment that KNM-ER 42700 is a young juvenile H. erectus if H. erectus followed an ontogenetic shape trajectory that was more similar to chimpanzees than humans.
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http://dx.doi.org/10.1016/j.jhevol.2021.102980DOI Listing
May 2021

Early ontogeny of humeral trabecular bone in Neandertals and recent modern humans.

J Hum Evol 2021 May 26;154:102968. Epub 2021 Mar 26.

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany; Chaire Internationale de Paléoanthropologie du Collège de France, 11 Place Marcelin Berthelot, 75005 Paris, France.

Trabecular bone ontogeny is well known in modern humans and unknown in Neandertals. Yet the bone developmental pattern is useful for interpreting fossils from evolutionary and functional perspectives. Interestingly, microstructure in early ontogeny is supposedly not influenced by high and specific mechanical loading related to the lifestyle of a human group and consequently does not directly depend on the activities of hunter-gatherers. Here, we specifically explored the early growth trajectories of the trabecular bone structure of the humerus and emphasized in particular how bone fraction (bone volume/total volume [BV/TV]) was built up in Neandertals, given the specific modern human bone loss after birth and the use of BV/TV in functional studies. Six Neandertals and 26 recent modern humans ranging from perinates to adolescents were included in this study. Six trabecular parameters were measured within a cubic region of interest extracted from the proximal metaphysis of the humerus. We found that the microstructural changes in Neandertals during early ontogeny (<1 year) fit with modern human growth trajectories for each parameter. The specific bone loss occurring immediately after birth in modern humans also occurred in Neandertals (but not in chimpanzees). However, the early childhood fossil Ferrassie 6 presented unexpectedly high BV/TV, whereas the high BV/TV in the Crouzade I adolescent was predictable. These results suggest that Neandertals and modern humans shared predetermined early growth trajectories and developmental mechanisms. We assume that the close relationship between skeletal characteristics in early ontogeny and adults in modern humans also existed in Neandertals. However, it was difficult to ensure that the high BV/TV in Neandertal early childhood, represented by only one individual, was at the origin of the high BV/TV observed in adults. Consequently, our study does not challenge the mechanical hypothesis that explains the trabecular gracilization of the humerus during the Holocene.
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http://dx.doi.org/10.1016/j.jhevol.2021.102968DOI Listing
May 2021

Exploring the functional morphology of the Gorilla shoulder through musculoskeletal modelling.

J Anat 2021 Feb 24. Epub 2021 Feb 24.

Department of Human Evolution, Max-Planck-Institute for Evolutionary Anthropology, Leipzig, Germany.

Musculoskeletal computer models allow us to quantitatively relate morphological features to biomechanical performance. In non-human apes, certain morphological features have long been linked to greater arm abduction potential and increased arm-raising performance, compared to humans. Here, we present the first musculoskeletal model of a western lowland gorilla shoulder to test some of these long-standing proposals. Estimates of moment arms and moments of the glenohumeral abductors (deltoid, supraspinatus and infraspinatus muscles) over arm abduction were conducted for the gorilla model and a previously published human shoulder model. Contrary to previous assumptions, we found that overall glenohumeral abduction potential is similar between Gorilla and Homo. However, gorillas differ by maintaining high abduction moment capacity with the arm raised above horizontal. This difference is linked to a disparity in soft tissue properties, indicating that scapular morphological features like a cranially oriented scapular spine and glenoid do not enhance the abductor function of the gorilla glenohumeral muscles. A functional enhancement due to differences in skeletal morphology was only demonstrated in the gorilla supraspinatus muscle. Contrary to earlier ideas linking a more obliquely oriented scapular spine to greater supraspinatus leverage, our results suggest that increased lateral projection of the greater tubercle of the humerus accounts for the greater biomechanical performance in Gorilla. This study enhances our understanding of the evolution of gorilla locomotion, as well as providing greater insight into the general interaction between anatomy, function and locomotor biomechanics.
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http://dx.doi.org/10.1111/joa.13412DOI Listing
February 2021

How old are the oldest in Far East Asia?

Proc Natl Acad Sci U S A 2021 Mar;118(10)

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig 04103, Germany;

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http://dx.doi.org/10.1073/pnas.2101173118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7958237PMC
March 2021

Reconstructing Late Pleistocene paleoclimate at the scale of human behavior: an example from the Neandertal occupation of La Ferrassie (France).

Sci Rep 2021 Jan 14;11(1):1419. Epub 2021 Jan 14.

Department of Human Evolution, Max-Planck-Institute for Evolutionary Anthropology, Leipzig, Germany.

Exploring the role of changing climates in human evolution is currently impeded by a scarcity of climatic information at the same temporal scale as the human behaviors documented in archaeological sites. This is mainly caused by high uncertainties in the chronometric dates used to correlate long-term climatic records with archaeological deposits. One solution is to generate climatic data directly from archaeological materials representing human behavior. Here we use oxygen isotope measurements of Bos/Bison tooth enamel to reconstruct summer and winter temperatures in the Late Pleistocene when Neandertals were using the site of La Ferrassie. Our results indicate that, despite the generally cold conditions of the broader period and despite direct evidence for cold features in certain sediments at the site, Neandertals used the site predominantly when climatic conditions were mild, similar to conditions in modern day France. We suggest that due to millennial scale climate variability, the periods of human activity and their climatic characteristics may not be representative of average conditions inferred from chronological correlations with long-term climatic records. These results highlight the importance of using direct routes, such as the high-resolution archives in tooth enamel from anthropogenically accumulated faunal assemblages, to establish climatic conditions at a human scale.
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http://dx.doi.org/10.1038/s41598-020-80777-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7809458PMC
January 2021

New hominin teeth from Stajnia Cave, Poland.

J Hum Evol 2021 Feb 5;151:102929. Epub 2021 Jan 5.

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig D-04103, Germany; International Chair of Paleoanthropology, Collège de France, 11 Place Marcelin Berthelot, Paris 75231, France.

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http://dx.doi.org/10.1016/j.jhevol.2020.102929DOI Listing
February 2021

Virtual reconstruction of the Kebara 2 Neanderthal pelvis.

J Hum Evol 2021 Feb 25;151:102922. Epub 2020 Dec 25.

Department of Anthropology, University of California, 1 Shields Avenue, Davis, CA, 95616, USA; Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany.

The paucity of well-preserved pelvises in the hominin fossil record has hindered robust analyses of shifts in critical biological processes throughout human evolution. The Kebara 2 pelvis remains one of the best preserved hominin pelvises, providing a rare opportunity to assess Neanderthal pelvic morphology and function. Here, we present two new reconstructions of the Kebara 2 pelvis created from CT scans of the right hip bone and sacrum. For both reconstructions, we proceeded as follows. First, we virtually reconstructed the right hip bone and the sacrum by repositioning the fragments of the hip bone and sacrum. Then, we created a mirrored copy of the right hip bone to act as the left hip bone. Next, we 3D printed the three bones and physically articulated them. Finally, we used fiducial points collected from the physically articulated models to articulate the hip bones and sacrum in virtual space. Our objectives were to (1) reposition misaligned fragments, particularly the ischiopubic ramus; (2) create a 3D model of a complete pelvis; and (3) assess interobserver reconstruction variation. These new reconstructions show that, in comparison with previous measurements, Kebara 2 possessed a higher shape index (maximum anteroposterior length/maximum mediolateral width) for the pelvic inlet and perhaps the outlet and a more anteriorly positioned sacral promontory and pubic symphysis relative to the acetabula. The latter differences result in a lower ratio between the distances anterior and posterior to the anterior margins of the acetabula. Generally, the new reconstructions tend to accentuate features of the Kebara 2 pelvis--the long superior pubic ramus and anteriorly positioned pelvic inlet--that have already been discussed for Kebara 2 and other Neanderthals.
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http://dx.doi.org/10.1016/j.jhevol.2020.102922DOI Listing
February 2021

Pluridisciplinary evidence for burial for the La Ferrassie 8 Neandertal child.

Sci Rep 2020 12 9;10(1):21230. Epub 2020 Dec 9.

Department Geología, Facultad de Ciencia y Tecnología, Universidad del País Vasco-Euskal Herriko Unibertsitatea (UPV/EHU), Barrio Sarriena s/n, 48940, Leioa, Spain.

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 -C 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 C age of 41.7-40.8 ka cal BP (95%), younger than the C 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.
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http://dx.doi.org/10.1038/s41598-020-77611-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7725784PMC
December 2020

Reply to Haeusler et al.: Internal structure of the femur provides robust evidence for locomotor and taxonomic diversity at Sterkfontein.

Proc Natl Acad Sci U S A 2020 11 20;117(46):28570-28571. Epub 2020 Oct 20.

Skeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Canterbury CT2 7NR, United Kingdom.

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http://dx.doi.org/10.1073/pnas.2016647117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7682416PMC
November 2020

Intraspecific variability in human maxillary bone modeling patterns during ontogeny.

Am J Phys Anthropol 2020 12 8;173(4):655-670. Epub 2020 Oct 8.

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

Objectives: This study compares the ontogenetic bone modeling patterns of the maxilla to the related morphological changes in three human populations to better understand how morphological variability within a species is established during ontogeny at both micro- and macroscopic levels.

Materials And Methods: The maxillary bones of an ontogenetic sample of 145 subadult and adult individuals from Greenland (Inuit), Western Europe (France, Germany, and Portugal), and South Africa (Khoekhoe and San) were analyzed. Bone formation and resorption were quantified using histological methods to visualize the bone modeling patterns. In parallel, semilandmark geometric morphometric techniques were used on 3D models of the same individuals to capture the morphological changes. Multivariate statistics were applied and shape differences between age groups were visualized through heat maps.

Results: The three populations show differences in the degree of shape change acquired during ontogeny, leading to divergences in the developmental trajectories. Only subtle population differences in the bone modeling patterns were found, which were maintained throughout ontogeny. Bone resorption in adults mirrors the pattern found in subadults, but is expressed at lower intensities.

Discussion: Our data demonstrate that maxillary morphological differences observed in three geographically distinct human populations are also reflected at the microscopic scale. However, we suggest that these differences are mostly driven by changes in rates and timings of the cellular activities, as only slight discrepancies in the location of bone resorption could be observed. The shared general bone modeling pattern is likely characteristic of all Homo sapiens, and can be observed throughout ontogeny.
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http://dx.doi.org/10.1002/ajpa.24153DOI Listing
December 2020

New perspectives on Neanderthal dispersal and turnover from Stajnia Cave (Poland).

Sci Rep 2020 09 8;10(1):14778. Epub 2020 Sep 8.

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany.

The Micoquian is the broadest and longest enduring cultural facies of the Late Middle Palaeolithic that spread across the periglacial and boreal environments of Europe between Eastern France, Poland, and Northern Caucasus. Here, we present new data from the archaeological record of Stajnia Cave (Poland) and the paleogenetic analysis of a Neanderthal molar S5000, found in a Micoquian context. Our results demonstrate that the mtDNA genome of Stajnia S5000 dates to MIS 5a making the tooth the oldest Neanderthal specimen from Central-Eastern Europe. Furthermore, S5000 mtDNA has the fewest number of differences to mtDNA of Mezmaiskaya 1 Neanderthal from Northern Caucasus, and is more distant from almost contemporaneous Neanderthals of Scladina and Hohlenstein-Stadel. This observation and the technological affinity between Poland and the Northern Caucasus could be the result of increased mobility of Neanderthals that changed their subsistence strategy for coping with the new low biomass environments and the increased foraging radius of gregarious animals. The Prut and Dniester rivers were probably used as the main corridors of dispersal. The persistence of the Micoquian techno-complex in South-Eastern Europe infers that this axis of mobility was also used at the beginning of MIS 3 when a Neanderthal population turnover occurred in the Northern Caucasus.
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http://dx.doi.org/10.1038/s41598-020-71504-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7479612PMC
September 2020

A late Neanderthal tooth from northeastern Italy.

J Hum Evol 2020 10 2;147:102867. Epub 2020 Sep 2.

Department of Cultural Heritage, University of Bologna, Via Degli Ariani 1, Ravenna, 48121, Italy; Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig, 04103, Germany.

The site of Riparo Broion (Vicenza, northeastern Italy) preserves a stratigraphic sequence documenting the Middle-to-Upper Paleolithic transition, in particular the final Mousterian and the Uluzzian cultures. In 2018, a human tooth was retrieved from a late Mousterian level, representing the first human remain ever found from this rock shelter (Riparo Broion 1). Here, we provide the morphological description and taxonomic assessment of Riparo Broion 1 with the support of classic and virtual morphology, 2D and 3D analysis of the topography of enamel thickness, and DNA analysis. The tooth is an exfoliated right upper deciduous canine, and its general morphology and enamel thickness distribution support attribution to a Neanderthal child. Correspondingly, the mitochondrial DNA sequence from Riparo Broion 1 falls within the known genetic variation of Late Pleistocene Neanderthals, in accordance with newly obtained radiocarbon dates that point to approximately 48 ka cal BP as the most likely minimum age for this specimen. The present work describes novel and direct evidence of the late Neanderthal occupation in northern Italy that preceded the marked cultural and technological shift documented by the Uluzzian layers in the archaeological sequence at Riparo Broion. Here, we provide a new full morphological, morphometric, and taxonomic analysis of Riparo Broion 1, in addition to generating the wider reference sample of Neanderthal and modern human upper deciduous canines. This research contributes to increasing the sample of fossil remains from Italy, as well as the number of currently available upper deciduous canines, which are presently poorly documented in the scientific literature.
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http://dx.doi.org/10.1016/j.jhevol.2020.102867DOI Listing
October 2020

A wolf from Gravettian site Pavlov I, Czech Republic: Approach to skull pathology.

Int J Paleopathol 2020 12 28;31:7-13. Epub 2020 Aug 28.

Czech Academy of Sciences, Institute of Archeology, Brno, Center for Paleolithic and Paleoanthropology Dolní Věstonice, Čechyňská 19, CZ - 602 00 Brno, Czech Republic; Masaryk University, Faculty of Science, Department of Anthropology, Kotlářská 2, CZ - 611 37 Brno, Czech Republic. Electronic address:

Objective: Describe pathological features on internal and external aspects of the skull of an ancient grey wolf.

Materials: Wolf remains that were found at the southwestern settlement Area A of Gravettian site Pavlov I.

Methods: Visual observation and description; microcomputed tomography; porosity and fragmentation indices for internal and external skull features; histological section of the fourth upper premolar tooth.

Results: Dorsally, the sagittal crest revealed bone healing and remodeling. The sagittal lesion differential diagnosis was blunt trauma with or without fracture. Ventrally, otic region pathology included severe proliferation and lysis (osteomyelitis). The pathology was not resolvable among differential (microbial) causes of osteomyelitis, although other potential etiologies were ruled out.

Conclusions: Probable first report of otic region osteomyelitis in an ancient grey wolf.

Significance: The proximity of the wolf remains to human-related findings, and presence of red ochre and shells, suggest human involvement in the burial.

Limitations: This is a single specimen with differential diagnoses that were not resolvable to a single definitive diagnosis.

Suggestions For Further Research: Further investigation of the possible anthropological significance of the burial circumstances.
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http://dx.doi.org/10.1016/j.ijpp.2020.07.001DOI Listing
December 2020

Enamel thickness variation in the deciduous dentition of extant large-bodied hominoids.

Am J Phys Anthropol 2020 11 7;173(3):500-513. Epub 2020 Aug 7.

Institute of Human Origins, School of Human Evolution and Social Change, Arizona State University, Tempe, Arizona, USA.

Objectives: Enamel thickness features prominently in hominoid evolutionary studies. To date, however, studies of enamel thickness in humans, great apes, and their fossil relatives have focused on the permanent molar row. Comparatively little research effort has been devoted to tissue proportions within deciduous teeth. Here we attempt to fill this gap by documenting enamel thickness variation in the deciduous dentition of extant large-bodied hominoids.

Materials And Methods: We used microcomputed tomography to image dental tissues in 80 maxillary and 78 mandibular deciduous premolars of Homo sapiens, Pan troglodytes, Gorilla, and Pongo. Two-dimensional virtual sections were created from the image volumes to quantify average (AET) and relative (RET) enamel thickness, as well as its distribution across the crown.

Results: Our results reveal no significant differences in enamel thickness among the great apes. Unlike the pattern present in permanent molars, Pongo does not stand out as having relatively thicker-enameled deciduous premolars than P. troglodytes and Gorilla. Humans, on the other hand, possess significantly thicker deciduous premolar enamel in comparison to great apes. Following expectations from masticatory biomechanics, we also find that the "functional" side (protocone, protoconid) of deciduous premolars generally possesses thicker enamel than the "nonfunctional" side.

Discussion: Our study lends empirical support to anecdotal observations that patterns of AET and RET observed for permanent molars of large-bodied apes do not apply to deciduous premolars. By documenting enamel thickness variation in hominoid deciduous teeth, this study provides the comparative context to interpret rates and patterns of wear of deciduous teeth and their utility in life history reconstructions.
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http://dx.doi.org/10.1002/ajpa.24106DOI Listing
November 2020

Distinct mandibular premolar crown morphology in Homo naledi and its implications for the evolution of Homo species in southern Africa.

Sci Rep 2020 08 6;10(1):13196. Epub 2020 Aug 6.

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany.

Homo naledi displays a combination of features across the skeleton not found in any other hominin taxon, which has hindered attempts to determine its placement within the hominin clade. Using geometric morphometrics, we assess the morphology of the mandibular premolars of the species at the enamel-dentine junction (EDJ). Comparing with specimens of Paranthropus, Australopithecus and Homo (n = 97), we find that the H. naledi premolars from the Dinaledi chamber consistently display a suite of traits (e.g., tall crown, well-developed P and P metaconid, strongly developed P mesial marginal ridge, and a P > P size relationship) that distinguish them from known hominin groups. Premolars from a second locality, the Lesedi Chamber, are consistent with this morphology. We also find that two specimens from South Africa, SK 96 (usually attributed to Paranthropus) and Stw 80 (Homo sp.), show similarities to the species, and we discuss a potential evolutionary link between H. naledi and hominins from Sterkfontein and Swartkrans.
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http://dx.doi.org/10.1038/s41598-020-69993-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7413389PMC
August 2020

Multi-protease analysis of Pleistocene bone proteomes.

J Proteomics 2020 09 9;228:103889. Epub 2020 Jul 9.

Evolutionary Genomics Section, Globe Institute, University of Copenhagen, Copenhagen, Denmark; Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany. Electronic address:

Ancient protein analysis is providing new insights into the evolutionary relationships between hominin fossils across the Pleistocene. Protein identification commonly relies on the proteolysis of a protein extract using a single protease, trypsin. As with modern proteome studies, alternative or additional proteases have the potential to increase both proteome size and protein sequence recovery. This could enhance the recovery of phylogenetic information from ancient proteomes. Here we identify 18 novel hominin bone specimens from the Kleine Feldhofer Grotte using MALDI-TOF MS peptide mass fingerprinting of collagen type I. Next, we use one of these hominin bone specimens and three Late Pleistocene Equidae specimens identified in a similar manner and present a comparison of the bone proteome size and protein sequence recovery obtained after using nanoLC-MS/MS and parallel proteolysis using six different proteases, including trypsin. We observe that the majority of the preserved bone proteome is inaccessible to trypsin. We also observe that for proteins recovered consistently across several proteases, protein sequence coverage can be increased significantly by combining peptide identifications from two or more proteases. Our results thereby demonstrate that the proteolysis of Pleistocene proteomes by several proteases has clear advantages when addressing evolutionary questions in palaeoproteomics. SIGNIFICANCE: Maximizing proteome and protein sequence recovery of ancient skeletal proteomes is important when analyzing unique hominin fossils. As with modern proteome studies, palaeoproteomic analysis of Pleistocene bone and dentine samples has almost exclusively used trypsin as its only protease, despite the demonstrated advantages of alternative proteases to increase proteome recovery in modern proteome studies. We demonstrate that Pleistocene bone proteomes can be significantly expanded by using additional proteases beside trypsin, and that this also improves sequence coverage of individual proteins. The use of several alternative proteases beside trypsin therefore has major benefits to maximize the phylogenetic information retrieved from ancient skeletal proteomes.
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http://dx.doi.org/10.1016/j.jprot.2020.103889DOI Listing
September 2020

Initial Upper Palaeolithic Homo sapiens from Bacho Kiro Cave, Bulgaria.

Nature 2020 05 11;581(7808):299-302. Epub 2020 May 11.

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

The Middle to Upper Palaeolithic transition in Europe witnessed the replacement and partial absorption of local Neanderthal populations by Homo sapiens populations of African origin. However, this process probably varied across regions and its details remain largely unknown. In particular, the duration of chronological overlap between the two groups is much debated, as are the implications of this overlap for the nature of the biological and cultural interactions between Neanderthals and H. sapiens. Here we report the discovery and direct dating of human remains found in association with Initial Upper Palaeolithic artefacts, from excavations at Bacho Kiro Cave (Bulgaria). Morphological analysis of a tooth and mitochondrial DNA from several hominin bone fragments, identified through proteomic screening, assign these finds to H. sapiens and link the expansion of Initial Upper Palaeolithic technologies with the spread of H. sapiens into the mid-latitudes of Eurasia before 45 thousand years ago. The excavations yielded a wealth of bone artefacts, including pendants manufactured from cave bear teeth that are reminiscent of those later produced by the last Neanderthals of western Europe. These finds are consistent with models based on the arrival of multiple waves of H. sapiens into Europe coming into contact with declining Neanderthal populations.
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http://dx.doi.org/10.1038/s41586-020-2259-zDOI Listing
May 2020

The position of Australopithecus sediba within fossil hominin hand use diversity.

Nat Ecol Evol 2020 07 18;4(7):911-918. Epub 2020 May 18.

Skeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Canterbury, UK.

The human lineage is marked by a transition in hand use, from locomotion towards increasingly dexterous manipulation, concomitant with bipedalism. The forceful precision grips used by modern humans probably evolved in the context of tool manufacture and use, but when and how many times hominin hands became principally manipulative remains unresolved. We analyse metacarpal trabecular and cortical bone, which provide insight into behaviour during an individual's life, to demonstrate previously unrecognized diversity in hominin hand use. The metacarpals of the palm in Australopithecus sediba have trabecular morphology most like orangutans and consistent with locomotor power-grasping with the fingers, while that of the thumb is consistent with human-like manipulation. This internal morphology is the first record of behaviour consistent with a hominin that used its hand for both arboreal locomotion and human-like manipulation. This hand use is distinct from other fossil hominins in this study, including A. afarensis and A. africanus.
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http://dx.doi.org/10.1038/s41559-020-1207-5DOI Listing
July 2020

A C chronology for the Middle to Upper Palaeolithic transition at Bacho Kiro Cave, Bulgaria.

Nat Ecol Evol 2020 06 11;4(6):794-801. Epub 2020 May 11.

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

The stratigraphy at Bacho Kiro Cave, Bulgaria, spans the Middle to Upper Palaeolithic transition, including an Initial Upper Palaeolithic (IUP) assemblage argued to represent the earliest arrival of Upper Palaeolithic Homo sapiens in Europe. We applied the latest techniques in C dating to an extensive dataset of newly excavated animal and human bones to produce a robust, high-precision radiocarbon chronology for the site. At the base of the stratigraphy, the Middle Palaeolithic (MP) occupation dates to >51,000 yr BP. A chronological gap of over 3,000 years separates the MP occupation from the occupation of the cave by H. sapiens, which extends to 34,000 cal BP. The extensive IUP assemblage, now associated with directly dated H. sapiens fossils at this site, securely dates to 45,820-43,650 cal BP (95.4% probability), probably beginning from 46,940 cal BP (95.4% probability). The results provide chronological context for the early occupation of Europe by Upper Palaeolithic H. sapiens.
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http://dx.doi.org/10.1038/s41559-020-1136-3DOI Listing
June 2020

Evidence for habitual climbing in a Pleistocene hominin in South Africa.

Proc Natl Acad Sci U S A 2020 04 30;117(15):8416-8423. Epub 2020 Mar 30.

Skeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Canterbury CT2 7NR, United Kingdom.

Bipedalism is a defining trait of the hominin lineage, associated with a transition from a more arboreal to a more terrestrial environment. While there is debate about when modern human-like bipedalism first appeared in hominins, all known South African hominins show morphological adaptations to bipedalism, suggesting that this was their predominant mode of locomotion. Here we present evidence that hominins preserved in the Sterkfontein Caves practiced two different locomotor repertoires. The trabecular structure of a proximal femur (StW 522) attributed to exhibits a modern human-like bipedal locomotor pattern, while that of a geologically younger specimen (StW 311) attributed to either sp. or exhibits a pattern more similar to nonhuman apes, potentially suggesting regular bouts of both climbing and terrestrial bipedalism. Our results demonstrate distinct morphological differences, linked to behavioral differences between and later hominins in South Africa and contribute to the increasing evidence of locomotor diversity within the hominin clade.
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http://dx.doi.org/10.1073/pnas.1914481117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7165455PMC
April 2020

Maxillary molar enamel thickness of Plio-Pleistocene hominins.

J Hum Evol 2020 05 19;142:102731. Epub 2020 Mar 19.

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, 04103, Germany; School of Anthropology and Conservation, University of Kent, Canterbury, CT2 7NR, United Kingdom; Evolutionary Studies Institute, University of Witwatersrand, Johannesburg, South Africa. Electronic address:

Enamel thickness remains an important morphological character in hominin systematics and is regularly incorporated into dietary reconstructions in hominin species. We expand upon a previous study of enamel thickness in mandibular molars by examining a large maxillary molar sample of Plio-Pleistocene hominins (n = 62) and a comparative sample of extant nonhuman apes (n = 48) and modern humans (n = 29). 2D mesial planes of section were generated through microtomography, and standard dental tissue variables were measured to calculate average enamel thickness (AET) and relative enamel thickness (RET). AET was also examined across the lingual, occlusal, and buccal regions of the crown. This study confirms previous findings of increasing enamel thickness throughout the Plio-Pleistocene, being thinnest in Australopithecus anamensis and peaking in Australopithecus boisei, with early Homo specimens, exhibiting intermediate enamel thickness. Agreeing with previous findings, 2D plane of section enamel thickness is found to be a poor taxonomic discriminator, with no statistically significant differences observed between fossil hominins. For fossil hominins, modern humans, and Pongo, the occlusal region of enamel was the thickest, and the lingual enamel thickness was greater than buccal. Pan and Gorilla present the opposite pattern with enamel being thinnest occlusally. Comparison at each molar position between the maxilla and mandible revealed very few significant differences in fossil hominins but some evidence of significantly thicker maxillary enamel (AET) in modern humans and thinner maxillary enamel in Pan (RET).
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http://dx.doi.org/10.1016/j.jhevol.2019.102731DOI Listing
May 2020

Earliest African evidence of carcass processing and consumption in cave at 700 ka, Casablanca, Morocco.

Sci Rep 2020 03 16;10(1):4761. Epub 2020 Mar 16.

Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany.

To date, in Africa, evidence for animal processing and consumption in caves routinely used as living spaces is only documented in the late Middle Pleistocene of the North and South of the continent and postdates the Middle Pleistocene in East Africa. Here we report the earliest evidence in a North-African cave (Grotte des Rhinocéros at Casablanca, Morocco) of cut, percussion and human gnawing marks on faunal remains directly associated with lithic knapping activities in the same space and in a well-documented stratified context. Ages for this Acheulean site are provided by the dating of herbivorous teeth to 690-720 ka and 520-550 ka (lower and upper sets) by combined Electron Spin Resonance (ESR) and U-series techniques. Traces of butchery on gazelle, alcelaphin, and zebra bones demonstrate that hominins had primary access to herbivore carcasses. Hominins brought and consumed meat in the cave, as documented by herbivore bones bearing human tooth marks concentrated in a circumscribed area of the excavation. In Africa, this site provides the earliest evidence for in situ carcass processing and meat-eating in cave, directly associated with lithic production and demonstrates the recurrent use by early Middle Pleistocene hominins of a North African cave site 400 000 years before that by Homo sapiens at Jebel Irhoud (Morocco).
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http://dx.doi.org/10.1038/s41598-020-61580-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7075909PMC
March 2020

Evolution of brain lateralization: A shared hominid pattern of endocranial asymmetry is much more variable in humans than in great apes.

Sci Adv 2020 02 14;6(7):eaax9935. Epub 2020 Feb 14.

Department of Evolutionary Biology, University of Vienna, Vienna, Austria.

Brain lateralization is commonly interpreted as crucial for human brain function and cognition. However, as comparative studies among primates are rare, it is not known which aspects of lateralization are really uniquely human. Here, we quantify both pattern and magnitude of brain shape asymmetry based on endocranial imprints of the braincase in humans, chimpanzees, gorillas, and orangutans. Like previous studies, we found that humans were more asymmetric than chimpanzees, however so were gorillas and orangutans, highlighting the need to broaden the comparative framework for interpretation. We found that the average spatial asymmetry pattern, previously considered to be uniquely human, was shared among humans and apes. In humans, however, it was less directed, and different local asymmetries were less correlated. We, thus, found human asymmetry to be much more variable compared with that of apes. These findings likely reflect increased functional and developmental modularization of the human brain.
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http://dx.doi.org/10.1126/sciadv.aax9935DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7021492PMC
February 2020

Zinc isotopes in Late Pleistocene fossil teeth from a Southeast Asian cave setting preserve paleodietary information.

Proc Natl Acad Sci U S A 2020 03 18;117(9):4675-4681. Epub 2020 Feb 18.

Institut für Geowissenschaften, Arbeitsgruppe für Angewandte und Analytische Paläontologie, Johannes Gutenberg-Universität Mainz, 55099 Mainz, Germany.

Stable carbon and nitrogen isotope ratios of collagen from bone and dentin have frequently been used for dietary reconstruction, but this method is limited by protein preservation. Isotopes of the trace element zinc (Zn) in bioapatite constitute a promising proxy to infer dietary information from extant and extinct vertebrates. The Zn/Zn ratio (expressed as δZn value) shows an enrichment of the heavy isotope in mammals along each trophic step. However, preservation of diet-related δZn values in fossil teeth has not been assessed yet. Here, we analyzed enamel of fossil teeth from the Late Pleistocene (38.4-13.5 ka) mammalian assemblage of the Tam Hay Marklot (THM) cave in northeastern Laos, to reconstruct the food web and assess the preservation of original δZn values. Distinct enamel δZn values of the fossil taxa (δZn < δZn < δZn) according to their expected feeding habits were observed, with a trophic carnivore-herbivore spacing of +0.60‰ and omnivores having intermediate values. Zn and trace element concentration profiles similar to those of modern teeth also indicate minimal impact of diagenesis on the enamel. While further work is needed to explore preservation for settings with different taphonomic conditions, the diet-related δZn values in fossil enamel from THM cave suggest an excellent long-term preservation potential, even under tropical conditions that are well known to be adverse for collagen preservation. Zinc isotopes could thus provide a new tool to assess the diet of fossil hominins and associated fauna, as well as trophic relationships in past food webs.
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http://dx.doi.org/10.1073/pnas.1911744117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7060694PMC
March 2020

Reply to Scott et al: A closer look at the 3-rooted lower second molar of an archaic human from Xiahe.

Proc Natl Acad Sci U S A 2020 01 17;117(1):39-40. Epub 2019 Dec 17.

Center for the Study of Human Origins, New York University, New York, NY 10003.

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http://dx.doi.org/10.1073/pnas.1918959116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6955358PMC
January 2020

Corrigendum to "Endostructural morphology in hominoid mandibular third premolars: Geometric morphometric analysis of dentine crown shape" [Journal of Human Evolution 133 (2019) 198-213].

J Hum Evol 2020 Jan 9;138:102692. Epub 2019 Dec 9.

School of Anthropology and Conservation, University of Kent, Canterbury, CT2 7NZ, UK; Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany; Evolutionary Studies Institute, University of the Witwatersrand, 1 Jan Smuts Avenue, Braamfontein, 2000, Johannesburg, South Africa.

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http://dx.doi.org/10.1016/j.jhevol.2019.102692DOI Listing
January 2020

Anterior tooth-use behaviors among early modern humans and Neandertals.

PLoS One 2019 27;14(11):e0224573. Epub 2019 Nov 27.

Department of Evolutionary Biology, Ecology and Environmental Sciences, Universitat de Barcelona, Barcelona, Spain.

Early modern humans (EMH) are often touted as behaviorally advanced to Neandertals, with more sophisticated technologies, expanded resource exploitation, and more complex clothing production. However, recent analyses have indicated that Neandertals were more nuanced in their behavioral adaptations, with the production of the Châtelperronian technocomplex, the processing and cooking of plant foods, and differences in behavioral adaptations according to habitat. This study adds to this debate by addressing the behavioral strategies of EMH (n = 30) within the context of non-dietary anterior tooth-use behaviors to glean possible differences between them and their Neandertal (n = 45) counterparts. High-resolution casts of permanent anterior teeth were used to collect microwear textures of fossil and comparative bioarchaeological samples using a Sensofar white-light confocal profiler with a 100x objective lens. Labial surfaces were scanned, totaling a work envelope of 204 x 276 μm for each individual. The microwear textures were examined for post-mortem damage and uploaded to SSFA software packages for surface characterization. Statistical analyses were performed to examine differences in central tendencies and distributions of anisotropy and textural fill volume variables among the EMH sample itself by habitat, location, and time interval, and between the EMH and Neandertal samples by habitat and location. Descriptive statistics for the EMH sample were compared to seven bioarchaeological samples (n = 156) that utilized different tooth-use behaviors to better elucidate specific activities that may have been performed by EMH. Results show no significant differences between the means within the EMH sample by habitat, location, or time interval. Furthermore, there are no significant differences found here between EMH and Neandertals. Comparisons to the bioarchaeological samples suggest both fossil groups participated in clamping and grasping activities. These results indicate that EMH and Neandertals were similar in their non-dietary anterior tooth-use behaviors and provide additional evidence for overlapping behavioral strategies employed by these two hominins.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0224573PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6880970PMC
April 2020

The Neanderthal teeth from Marillac (Charente, Southwestern France): Morphology, comparisons and paleobiology.

J Hum Evol 2020 01 22;138:102683. Epub 2019 Nov 22.

UMR5199 PACEA: de la préhistoire à l'actuel: culture, environnement et anthropologie, Université de Bordeaux, bât. B8. Allée Geoffroy Saint-Hilaire - CS 50023, 33615 Pessac, France.

Few European sites have yielded human dental remains safely dated to the end of MIS 4/beginning of MIS 3. One of those sites is Marillac (Southwestern France), a collapsed karstic cave where archeological excavations (1967-1980) conducted by B. Vandermeersch unearthed numerous faunal and human remains, as well as a few Mousterian Quina tools. The Marillac sinkhole was occasionally used by humans to process the carcasses of different prey, but there is no evidence for a residential use of the site, nor have any hearths been found. Rare carnivore bones were also discovered, demonstrating that the sinkhole was seasonally used, not only by Neanderthals, but also by predators across several millennia. The lithostratigraphic units containing the human remains were dated to ∼60 kyr. The fossils consisted of numerous fragments of skulls and jaws, isolated teeth and several post-cranial bones, many of them with traces of perimortem manipulations. For those already published, their morphological characteristics and chronostratigraphic context allowed their attribution to Neanderthals. This paper analyzes sixteen unpublished human teeth (fourteen permanent and two deciduous) by investigating the external morphology and metrical variation with respect to other Neanderthal remains and a sample from modern populations. We also investigate their enamel thickness distribution in 2D and 3D, the enamel-dentine junction morphology (using geometric morphometrics) of one molar and two premolars, the roots and the possible expression of taurodontism, as well as pathologies and developmental defects. The anterior tooth use and paramasticatory activities are also discussed. Morphological and structural alterations were found on several teeth, and interpreted in light of human behavior (tooth-pick) and carnivores' actions (partial digestion). The data are interpreted in the context of the available information for the Eurasian Neanderthals.
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http://dx.doi.org/10.1016/j.jhevol.2019.102683DOI Listing
January 2020

Skull reconstruction of the late Miocene ape Rudapithecus hungaricus from Rudabánya, Hungary.

J Hum Evol 2020 01 20;138:102687. Epub 2019 Nov 20.

Department of Anthropology, University of Toronto, Toronto, ON M5S 2S2, Canada.

We report on a computer-based reconstruction of a well-preserved ape skull from late Miocene deposits in Rudabánya, Hungary. Based on micro-computed tomographic scans of the original Rudapithecus hungaricus partial cranium RUD 200 and the associated mandible RUD 212 we realign displaced bone fragments, and reconstruct the shape of the upper and lower jaws guided by occlusal fingerprint analysis of dental wear patterns. We apply geometric morphometric methods based on several hundred landmarks and sliding semilandmarks to estimate missing data, and create multiple reconstructions of the specimen. We then compare the reconstructed overall cranial shape, as well as the volume and shape of the endocast, with extant primates. Multiple reconstructions of RUD 200 yield an average endocranial volume of 234 cc (S.D.: 9 cc; range: 221-247 cc). RUD 200 is most similar to African apes in overall cranial shape, but in a statistical analysis of endocranial shape the specimen falls closest to extant hylobatids. Our data suggest that R. hungaricus from the late Miocene in Europe displays aspects of the overall cranial geometry typical of extant African great apes, but it does not show an evolutionary reorganization of the brain evident in Pan, Gorilla, and Pongo.
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http://dx.doi.org/10.1016/j.jhevol.2019.102687DOI Listing
January 2020