Evolution of middle-late Pleistocene human cranio-facial form: A 3-D approach

The classification and phylogenetic relationships of the middle Pleistocene human fossil record remains one of the most intractable problems in paleoanthropology. Several authors have noted broad resemblances between European and African fossils from this period, suggesting a single taxon ancestral to both modern humans and Neanderthals. Others point out ‘incipient’ Neanderthal features in the morphology of the European sample and have argued for their inclusion in the Neanderthal lineage exclusively, following a model of accretionary evolution of Neanderthals. We approach these questions using geometric morphometric methods which allow the intuitive visualization and quantification of features previously described qualitatively. We apply these techniques to evaluate proposed cranio-facial ‘incipient’ facial, vault, and basicranial traits in a middle-late Pleistocene European hominin sample when compared to a sample of the same time depth from Africa. Some of the features examined followed the predictions of the accretion model and relate the middle Pleistocene European material to the later Neanderthals. However, although our analysis showed a clear separation between Neanderthals and early/recent modern humans and morphological proximity between European specimens from OIS 7 to 3, it also shows that the European hominins from the first half of the middle Pleistocene still shared most of their cranio-facial architecture with their African contemporaries.     

Mandibular condyle traits in Neanderthals and other Homo: a comparative,correlative, and ontogenetic study

The relationship between the mandibular condyle and the crest of the mandibular notch (CMN) has historically entered into discussions of Neanderthal characteristics and was recently suggested to be autapomorphic in Neanderthals. The Neanderthal CMN has been described as intersecting the condyle in the middle, while the modern human CMN runs to the condyle's lateral end. A large lateral condylar tubercle (LCT) has also been observed in Neanderthals and thought to be related to medial (or less lateral) CMN position. In addition, the presence of a less lateral CMN early in ontogeny, as seen in the Amud 7 infant, has been argued to demonstrate great evolutionary divergence in Neanderthals. Using a scoring system for each trait, this study first examines the expression of CMN position and LCT size in 102 adult modern humans and in samples of Neanderthals and other fossil Homo. Then, CMN position is scored in 208 subadult modern humans to elucidate the ontogeny of this trait. Results show that CMN position is not autapomorphic in Neanderthals, but Neanderthals have significantly more CMNs in the least-lateral score category than does the modern human sample. Large LCTs are found to be strongly predictive of less lateral CMN position, although less lateral CMN position may exist in the absence of a large LCT. The complex ontogenetic pattern of CMN expression observed indicates that features of subadult and adult condylar morphology cannot be constructively compared without first considering subadult morphology on its own functional and developmental terms.     

The Mousterian child from Teshik‐Tash is a Neanderthal: A geometric morphometric study of the frontal bone

In the 1930s subadult hominin remains and Mousterian artifacts were discovered in the Teshik‐Tash cave in South Uzbekistan. Since then, the majority of the scientific community has interpreted Teshik‐Tash as a Neanderthal. However, some have considered aspects of the morphology of the Teshik‐Tash skull to be more similar to fossil modern humans such as those represented at Skhūl and Qafzeh, or to subadult Upper Paleolithic modern humans. Here we present a 3D geometric morphometric analysis of the Teshik‐Tash frontal bone in the context of developmental shape changes in recent modern humans, Neanderthals, and early modern humans. We assess the phenetic affinities of Teshik‐Tash to other subadult fossils, and use developmental simulations to predict possible adult shapes. We find that the morphology of the frontal bone places the Teshik‐Tash child close to other Neanderthal children and that the simulated adult shapes are closest to Neanderthal adults. Taken together with genetic data showing that Teshik‐Tash carried mtDNA of the Neanderthal type, as well as its occipital bun, and its shovel‐shaped upper incisors, these independent lines of evidence firmly place Teshik‐Tash among Neanderthals. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

The ATD6-5 mandibular specimen from Gran Dolina (Atapuerca, Spain). Morphological study and phylogenetic implications.

Metric and shape features of the Lower Pleistocene mandibular specimen ATD605 from the level 6 of Gran Dolina site (Atapuerca, Spain) are compared with a large sample of fossil hominid mandibles. The analysis shows that ATD6-5 displays a generalized morphology largely shared with both African and European Lower and Middle Pleistocene samples. However, distinctive African traits, such as corpus robustness and strong alveolar prominence, are absent in the Gran Dolina specimen. At the same time, none of the apomorphic features that characterize Middle and early Upper Pleistocene European hominids can be recognized in ATD6-5. Finally, the Gran Dolina specimen displays a remarkable position of the mylohyoid groove, only comparable to that found in immature specimens of Homo ergaster, and very rarely in adult H. sapiens. The morphology of ATD6-5 supports the hypothesis of an African origin for the first Europeans with subsequent phylogenetic continuity with Middle Pleistocene populations in Europe. These findings are consistent with H. antecessor being the last common ancestor of Neandertals and H. sapiens.     

New foot remains from the Gran Dolina-TD6 Early Pleistocene site (Sierra de Atapuerca, Burgos, Spain)

This paper presents and describes new foot fossils from the species Homo antecessor, found in level TD6 of the site of Gran Dolina (Sierra de Atapuerca, Burgos, Spain). These new fossils consist of an almost complete left talus (ATD6-95) and the proximal three-quarters of a right fourth metatarsal (ATD6-124). The talus ATD6-95 is tentatively assigned to Hominin 10 of the TD6 sample, an adult male specimen with which the second metatarsal ATD6-70+107 (already published) is also tentatively associated. Analysis of these fossils and other postcranial remains has made possible to estimate a stature similar to those of the specimens from the Middle Pleistocene site of Sima de los Huesos (Sierra de Atapuerca, Burgos, Spain). The morphology of the TD6 metatarsals does not differ significantly from that of modern humans, Neanderthals and the specimens from Sima de los Huesos. Talus ATD6-95, however, differs from the rest of the comparative samples in being long and high, having a long and wide trochlea, and displaying a proportionally short neck.     

The human cranial remains from Gran Dolina Lower Pleistocene site (Sierra de Atapuerca, Spain).

In this article we study the cranial remains of the late Lower Pleistocene human fossils from Gran Dolina (Sierra de Atapuerca, Spain), assigned to the new species Homo antecessor. The cranial remains belong to at least five individuals, both juveniles and adults. The most outstanding feature is the totally modern human morphology of the very complete face ATD6-69, representing the earliest occurrence of the modern face in the fossil record. The Gran Dolina fossils show in the face a suite of modern human apomorphies not found in earlier hominids nor in contemporary or earlier Homo erectus fossils. There are also traits in the Gran Dolina fossils shared with both Neandertals and modern humans, which reinforce the hypothesis that Neandertals and modern humans form a clade, and that the Gran Dolina fossils are a common ancestor to both lineages.     

Facial Morphogenesis of the Earliest Europeans

The modern human face differs from that of our early ancestors in that the facial profile is relatively retracted (orthognathic). This change in facial profile is associated with a characteristic spatial distribution of bone deposition and resorption: growth remodeling. For humans, surface resorption commonly dominates on anteriorly-facing areas of the subnasal region of the maxilla and mandible during development. We mapped the distribution of facial growth remodeling activities on the 900–800 ky maxilla ATD6-69 assigned to H. antecessor, and on the 1.5 My cranium KNM-WT 15000, part of an associated skeleton assigned to African H. erectus. We show that, as in H. sapiens, H. antecessor shows bone resorption over most of the subnasal region. This pattern contrasts with that seen in KNM-WT 15000 where evidence of bone deposition, not resorption, was identified. KNM-WT 15000 is similar to Australopithecus and the extant African apes in this localized area of bone deposition. These new data point to diversity of patterns of facial growth in fossil Homo. The similarities in facial growth in H. antecessor and H. sapiens suggest that one key developmental change responsible for the characteristic facial morphology of modern humans can be traced back at least to H. antecessor.     

Early Pleistocene human humeri from the Gran Dolina-TD6 site (Sierra de Atapuerca, Spain)

In this report, we present a morphometric comparative study of two Early Pleistocene humeri recovered from the TD6 level of the Gran Dolina cave site in Sierra de Atapuerca, northern Spain. ATD6-121 belongs to a child between 4 and 6 years old, whereas ATD6-148 corresponds to an adult. ATD6-148 exhibits the typical pattern of the genus Homo, but it also shows a large olecranon fossa and very thin medial and lateral pillars (also present in ATD6-121), sharing these features with European Middle Pleistocene hominins, Neandertals, and the Bodo Middle Pleistocene humerus. The morphology of the distal epiphysis, together with a few dental traits, suggests a phylogenetic relationship between the TD6 hominins and the Neandertal lineage. Given the older geochronological age of these hominins (ca. 900 ka), which is far from the age estimated by palaeogenetic studies for the population divergence of modern humans and Neandertals (ca. 400 ka), we suggest that this suite of derived "Neandertal" features appeared early in the evolution of the genus Homo. Thus, these features are not "Neandertal" apomorphies but traits which appeared in an ancestral and polymorphic population during the Early Pleistocene.     

Tooth wear, Neanderthal facial morphology and the anterior dental loading hypothesis

The Anterior Dental Loading Hypothesis states that the unique Neanderthal facial and dental anatomy was an adaptive response to the regular application of heavy forces resulting from both the masticatory and cultural use of the anterior teeth. Heavy anterior tooth wear frequently observed in Neanderthal specimens is cited as a main source of evidence for heavy forces being applied to these teeth. From this, it might be predicted that the wear shown on the anterior teeth of Neanderthals would greatly exceed that of the posterior teeth and that this differential would be greater than in other hominins with different facial morphologies.In this paper, a new method of examining tooth wear patterns is used to test these predictions in a large assemblage of Late Pleistocene hominins and a group of recent hunter-gatherers from Igloolik, Canada. The results show that all Late Pleistocene hominins, including Neanderthals, had heavily worn anterior teeth relative to their posterior teeth but, contrary to expectations, this was more pronounced in the modern humans than in the Neanderthals. The Igloolik Inuit showed heavier anterior tooth wear relative to their posterior teeth than any Late Pleistocene hominins. There was, however, a characteristic Neanderthal pattern in which wear was more evenly spread between anterior teeth than in modern humans. Overall, the evidence presented here suggests that all Late Pleistocene hominins habitually applied heavy forces between their anterior teeth and that Neanderthals were not exceptional in this regard. These results therefore does not support the Anterior Dental Loading Hypothesis.     

The human chin revisited: what is it and who has it?

Although the presence of a "chin" has long been recognized as unique to Homo sapiens among mammals, both the ontogeny and the morphological details of this structure have been largely overlooked. Here we point out the essential features of symphyseal morphology in H. sapiens, which are present and well-defined in the fetus at least as early as the fifth gestational month. Differences among adults in expression of these structures, particularly in the prominence of the mental tuberosity, are developmental epiphenomena and serve to emphasize the importance of studying this region in juveniles whenever possible. A survey of various middle to late Pleistocene fossil hominids for which juveniles are known reveals that these features are present in some late Pleistocene specimens assigned to H. sapiens, but not in all of the presumed anatomically modern H. sapiens (i.e., Qafzeh 8, 9, and 11). The adult specimens from Skhūl, as well as the adult Qafzeh 7 specimen, are similarly distinctive in symphyseal morphology. Neanderthals are quite variable in their own right, and they as well as other middle to late Pleistocene fossils lack the symphyseal features of H. sapiens. Some of the latter are, however, seen in the Tighenif (Ternifine) mandibles.     

The Neanderthal "chignon": variation, integration, and homology

The occipital bun ("chignon") is cited widely as a Neanderthal derived trait. It encompasses the posterior projection/convexity of the occipital squama and is associated with lambdoid flattening on the parietal. A 'hemibun' in some Upper Paleolithic Europeans is thought by some authors to indicate interbreeding between Neanderthals and early modern Europeans. However, 'bunning' is difficult to measure, and the term has been applied to a range of morphological patterns. Furthermore, its usefulness in phylogenetic reconstruction and its homologous status across modern and fossil humans have been disputed. We present a geometric morphometric study that quantitatively evaluates the chignon, assesses its usefulness in separating Neanderthals from modern humans, and its degree of similarity to Upper Paleolithic 'hemibuns.' We measured the three-dimensional coordinates of closely spaced points along the midsagittal plane from bregma to inion and of anatomical landmarks in a large series of recent human crania and several Middle and Late Pleistocene European and African fossils. These coordinate data were processed using the techniques of geometric morphometrics and analyzed with relative warps, canonical variates, and singular warps. Our results show no separation between Neanderthals and modern humans, including early modern Europeans, when the shape of the occipital plane midsagittal-profile is considered alone. On the other hand, Neanderthals are well separated from both recent and fossil modern humans when information about the occipital's relative position and relative size are also included. Furthermore, the occurrence of a highly convex and posteriorly projecting midline occipital profile (interpreted as the occipital bun) is highly correlated (>0.8) with a flat parietal midsagittal profile and with antero-superiorly positioned temporal bones across both our recent and our fossil human samples. We conclude that the shape of the occipital profile alone should not be considered an independent trait, as it is very tightly integrated with braincase shape. Our analysis does not support differences in integration of the posterior midsagittal profile and the cranial base in Pleistocene and recent humans.     

Neanderthals

Neanderthals are a group of fossil humans that inhabited Western Eurasia from approximately 300 to 30,000 years ago (ka). They vanished from the fossil record a few millennia after the first modern humans appeared in Europe (ca. 40 ka BP). They are characterized by a unique combination of distinctive anatomical features, and are found with stone tools of the Mousterian stone tool industry. Current consensus views them as a distinct Eurasian human lineage isolated from the rest of the Old World and sharing a common ancestor with modern humans sometime in the early Middle Pleistocene. The extreme cold of the European Ice Ages is considered at least partly responsible for the evolution of some of the distinctive Neanderthal anatomy, although other factors (functional demands, effects of chance in small populations) were probably also important. The causes for the Neanderthal extinction are not well understood. Worsening climate and competition with modern humans are implicated. Neanderthals were our sister species, much more closely related to us than the chimpanzees, our closest living relatives are today.     

Étude analytique d’une clavicule complète de subadulte d’Homo antecessor (site de Gran Dolina, Sierra d’Atapuerca, Burgos, Espagne)

This study reports on the skeletal remains of an infant clavicle - specimen ATD6-37 - belonging to the Homo antecessor species, unearthed at Lower Pleistocene level TD6 of the Gran Dolina site (Sierra de Atapuerca). Studied alongside a further adult specimen - ATD6-50 -, they provide us with significant information on two key paleobiological aspects of these early humans: body shape and development. Based on the analytical results, the paper proposes a more accurate proportional method for determining age at death is applied to the fossilized infant clavicle under study. It goes on to hypothesize on postcranial growth and body shape and discusses morphological patterns and age at death of these early humans through comparisons with a wide range of infant dental samples and clavicular specimens in early and modern humans.     

The Vindija Neanderthal scapular glenoid fossa: comparative shape analysis suggests evo-devo changes among Neanderthals

Although the shape of the scapular glenoid fossa (SGF) may be influenced by epigenetic and developmental factors, there appears to be strong genetic control over its overall form, such that variation within and between hominin taxa in SGF shape may contain information about their evolutionary histories. Here we present the results of a geometric morphometric study of the SGF of the Neanderthal Vi-209 from Vindjia Cave (Croatia), relative to samples of Plio-Pleistocene, later Pleistocene, and recent hominins. Variation in overall SGF shape follows a chronological trend from the plesiomorphic condition seen in Australopithecus to modern humans, with pre-modern species of the genus Homo exhibiting intermediate morphologies. Change in body size across this temporal series is not linearly directional, which argues against static allometry as an explanation. However, life history and developmental rates change directionally across the series, suggesting an ontogenetic effect on the observed changes in shape (ontogenetic allometry). Within this framework, the morphospace occupied by the Neanderthals exhibits a discontinuous distribution. The Vindija SGF and those of the later Near Eastern Neanderthals (Kebara and Shanidar) approach the modern condition and are somewhat segregated from both northwestern European (Neandertal and La Ferrassie) and early Mediterranean Neanderthals (Krapina and Tabun). Although more than one scenario may account for the pattern seen in the Neanderthals, the data is consistent with palaeogenetic evidence suggesting low levels of gene flow between Neanderthals and modern humans in the Near East after ca. 120-100 ka (thousands of years ago) (with subsequent introgression of modern human alleles into eastern and central Europe). Thus, in keeping with previous analyses that document some modern human features in the Vindija Neanderthals, the Vindija G₃ sample should not be seen as representative of ‘classic’ - that is, unadmixed, pre-contact - Neanderthal morphology.     

Using genetic evidence to evaluate four palaeoanthropological hypotheses for the timing of Neanderthal and modern human origins

A better understanding of the evolutionary relationship between modern humans and Neanderthals is essential for improving the resolution of hominin phylogenetic hypotheses. Currently, four distinct chronologies for the timing of population divergence are available, ranging from the late Middle Pleistocene to the late Early Pleistocene, each based on different interpretations of hominin taxonomy. Genetic data can present an independent estimate of the evolutionary timescale involved, making it possible to distinguish between these competing models of hominin evolution. We analysed five dated Neanderthal mitochondrial genomes, together with those of 54 modern humans, and inferred a genetic chronology using multiple age calibrations. Our mean date estimates are consistent with a process of genetic divergence within an ancestral population, commencing approximately 410-440 ka. These results suggest that a reappraisal of key elements in the Pleistocene hominin fossil record may now be required.     

The Olduvai Hominid 8 foot: Adult or subadult?

Olduvai Hominid 8 (OH 8), an articulating set of fossil hominin tarsal and metatarsal bones, is critical to interpretations of the evolution of hominin pedal morphology and bipedal locomotion. It has been suggested that OH 8 may represent the foot of a subadult and may be associated with the OH 7 mandible, the type specimen of Homo habilis. This assertion is based on the presence of what may be unfused distal metatarsal epiphyses. Accurately assessing the skeletal maturity of the OH 8 foot is important for interpretations of the functional morphology and locomotor behavior of Plio-Pleistocene hominins. In this study, we compare metatarsal fusion patterns and internal bone morphology of the lateral metatarsals among subadult hominines (85 modern humans, 48 Pan, and 25 Gorilla) to assess the likelihood that OH 8 belonged to either an adult or subadult hominin. Our results suggest that if OH 8 is indeed from a subadult, then it displays a metatarsal developmental pattern that is unobserved in our comparative sample. In OH 8, the fully fused base of the first metatarsal and the presence of trabecular bone at the distal ends of the second and third metatarsal shafts make it highly improbable that it belonged to a subadult, let alone a subadult that matches the developmental age of the OH 7 mandible. In total, the results of this study suggest that the OH 8 foot most likely belonged to an adult hominin.     

A fossil hominoid proximal femur from Kikorongo Crater, southwestern Uganda

The external morphology of a fragmentary right proximal femur from southwestern Uganda is described here. Discovered in the Kikorongo Crater of Queen Elizabeth National Park in 1961, this specimen was informally assigned to Homo sapiens (although never described) and tentatively dated to the late Pleistocene. However, because aspects of the external morphology of the femur align the fossil with the African great apes, we suggest that the Kikorongo femur may be the first postcranial fossil of the genus Pan. Like the African apes, the Kikorongo specimen lacks both an obturator externus groove and an intertrochanteric line. It has a short femoral neck with a circular cross section, and a narrow and deep superior notch. Using resampling statistics and discriminant function analysis, the Kikorongo femur clustered with the genus Pan, as opposed to Gorilla or Homo. However, if the specimen is from Pan, it would be large for this taxon. Furthermore, features that clearly distinguish the external morphology of Plio-Pleistocene hominin proximal femora from African ape femora, such as the shape of the femoral neck in cross section and femoral neck length, have converged in Holocene humans and African apes. Unfortunately, the internal morphology of the femoral neck of the Kikorongo fossil was not discernable. Although we hypothesize that the Kikorongo femur is from the genus Pan, there is such variability in the proximal femora of modern humans that, although it would be an unusual human, it remains possible that this fossil represents H. sapiens.