Thoracic skeletal morphology and high-altitude hypoxia in Andean prehistory

Living humans from the highland Andes exhibit antero-posteriorly and medio-laterally enlarged chests in response to high-altitude hypoxia. This study hypothesizes that morphological responses to high-altitude hypoxia should also be evident in pre-Contact Andean groups. Thoracic skeletal morphology in four groups of human skeletons (N = 347) are compared: two groups from coastal regions (Ancón, Peru, n = 79 and Arica, Chile, n = 123) and two groups from high altitudes (San Pedro de Atacama, Chile, n = 102 and Machu Picchu and Cuzco, Peru, n = 43). Osteometric variables that represent proportions of chest width and depth include sternal and clavicular lengths and breadths and rib length, curvature, and area. Each variable was measured relative to body size, transformed into logarithmic indices, and compared across sex-specific groups using ANOVA and Tukey multiple comparison tests. Atacama highlanders have the largest sternal and clavicular proportions and ribs with the greatest area and least amount of curvature, features that suggest an antero-posteriorly deep and mediolaterally wide thoracic skeleton. Ancón lowlanders exhibit proportions indicating narrower and shallower chests. Machu Picchu and Cuzco males cluster with the other highland group in rib curvature and area at the superior levels of the thorax, whereas chest proportions in Machu Picchu and Cuzco females resemble those of lowlanders. The variation in Machu Picchu and Cuzco males and females is interpreted as the result of population migrations. The presence of morphological traits indicative of enlarged chests in some highland individuals suggests that high-altitude hypoxia was an environmental stressor shaping the biology of highland Andean groups during the pre-Contact period.     

Revisiting dental fluctuating asymmetry in neandertals and modern humans

Previous studies have suggested that Neandertals experienced greater physiological stress and/or were less capable of mitigating stress than most prehistoric modern human populations. The current study compares estimates of dental fluctuating asymmetry (DFA) for prehistoric Inupiat from Point Hope Alaska, the Late Archaic, and Protohistoric periods from Ohio and West Virginia, and a modern sample from Ohio to Neandertals from Europe and Southwest Asia. DFA results from developmental perturbation during crown formation and is thus an indicator of developmental stress, which previous studies have found to be higher in Neandertals than in several modern human populations. Here, we use recent methodological improvements in the analysis of fluctuating asymmetry suggested by Palmer and Strobeck (Annu Rev Ecol Syst 17 ( 1986 ) 391–421, Developmental instability: causes and consequences ( 2003a ) v.1–v.36, Developmental instability: causes and consequences ( 2003b ) 279–319) and compare the fit of Neandertal DFA Index values with those of modern humans. DFA estimates for each of the modern population samples exceeded measurement error, with the Inupiat exhibiting the highest levels of DFA for most tooth positions. All significant Neandertal z‐scores were positive, exceeding the estimates for each of the modern prehistoric groups. Neandertals exhibited the fewest significant differences from the Inupiat (9.2% of values are significant at P < 0.05), while for the other modern prehistoric groups more than 10% of the Neandertal z‐scores are significant at P < 0.05, more than 90% of these significant scores at P < 0.01. These results suggest that the Inupiat experienced greater developmental stress than the other prehistoric population samples, and that Neandertals were under greater developmental stress than all other prehistoric modern human samples. Am J Phys Anthropol 149:193–204, 2012. © 2012 Wiley Periodicals, Inc.     

The Shanidar 3 Neandertal

The Shanidar 3 Neandertal partial skeleton preserves four teeth, major portions of the thoracic and lumbar vertebrae, sacrum, ribs, clavicles, scapulae, humeri, hand bones, innominate bones, and foot bones, plus fragments of the ulnae, radii, femora, tibiae, and fibulae. Their morphology aligns Shanidar 3 closely with the other Shanidar Neandertals and the European and Near Eastern Neandertals. This is apparent especially in the dentition, scapulae, hand bones, and pubic bones.     

Size variation in early human mandibles and molars from Klasies River,South Africa: Comparison with other middle and late Pleistocene assemblages and with modern humans

Previous studies of the Middle Stone Age human remains from Klasies River have concluded that they exhibited more sexual dimorphism than extant populations, but these claims have not been assessed statistically. We evaluate these claims by comparing size variation in the best‐represented elements at the site, namely the mandibular corpora and M₂s, to that in samples from three recent human populations using resampling methods. We also examine size variation in these same elements from seven additional middle and late Pleistocene sites: Skhūl, Dolní Věstonice, Sima de los Huesos, Arago, Krapina, Shanidar, and Vindija. Our results demonstrate that size variation in the Klasies assemblage was greater than in recent humans, consistent with arguments that the Klasies people were more dimorphic than living humans. Variation in the Skhūl, Dolní Věstonice, and Sima de los Huesos mandibular samples is also higher than in the recent human samples, indicating that the Klasies sample was not unusual among middle and late Pleistocene hominins. In contrast, the Neandertal samples (Krapina, Shanidar, and Vindija) do not evince relatively high mandibular and molar variation, which may indicate that the level of dimorphism in Neandertals was similar to that observed in extant humans. These results suggest that the reduced levels of dimorphism in Neandertals and living humans may have developed independently, though larger fossil samples are needed to test this hypothesis. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

No evidence of Neandertal mtDNA contribution to early modern humans

The retrieval of mitochondrial DNA (mtDNA) sequences from four Neandertal fossils from Germany, Russia, and Croatia has demonstrated that these individuals carried closely related mtDNAs that are not found among current humans. However, these results do not definitively resolve the question of a possible Neandertal contribution to the gene pool of modern humans since such a contribution might have been erased by genetic drift or by the continuous influx of modern human DNA into the Neandertal gene pool. A further concern is that if some Neandertals carried mtDNA sequences similar to contemporaneous humans, such sequences may be erroneously regarded as modern contaminations when retrieved from fossils. Here we address these issues by the analysis of 24 Neandertal and 40 early modern human remains. The biomolecular preservation of four Neandertals and of five early modern humans was good enough to suggest the preservation of DNA. All four Neandertals yielded mtDNA sequences similar to those previously determined from Neandertal individuals, whereas none of the five early modern humans contained such mtDNA sequences. In combination with current mtDNA data, this excludes any large genetic contribution by Neandertals to early modern humans, but does not rule out the possibility of a smaller contribution.     

No evidence of Neandertal admixture in the mitochondrial genomes of early European modern humans and contemporary Europeans

Neandertals, the archaic human form documented in Eurasia until 29,000 years ago, share no mitochondrial haplotype with modern Europeans. Whether this means that the two groups were reproductively isolated is controversial, and indeed nuclear data have been interpreted as suggesting that they admixed. We explored the range of demographic parameters that may have generated the observed mitochondrial diversity, simulating 3.0 million genealogies under six models differing as for the relationships among contemporary Europeans, Neandertals, and Upper Palaeolithic European early modern humans (EEMH), who coexisted with Neandertals for millennia. We compared by Approximate Bayesian Computations the simulation results with mitochondrial diversity in 7 Neandertals, 3 EEMH, and 150 opportunely chosen modern Europeans. A model of genealogical continuity between EEMH and contemporary Europeans, with no Neandertal contribution, received overwhelming support from the analyses. The maximum degree of Neandertal admixture, under the model of gene flow supported by nuclear data, was estimated at 1.5%, but this model proved 20-32 times less likely than a model without any gene flow. Nuclear and mitochondrial evidence might be reconciled if smaller population sizes led to faster lineage sorting for mitochondrial DNA, and Neandertals shared a longer period of common ancestry with the non-African's than with the African's ancestors.     

What molars contribute to an emerging understanding of lateral enamel formation in Neandertals vs. modern humans

Two hypotheses, based on previous work on Neandertal anterior and premolar teeth, are investigated here: (1) that estimated molar lateral enamel formation times in Neandertals are likely to fall within the range of modern human population variation, and (2) that perikymata (lateral enamel growth increments) are distributed across cervical and occlusal halves of the crown differently in Neandertals than they are in modern humans. To investigate these hypotheses, total perikymata numbers and the distribution of perikymata across deciles of crown height were compared for Neandertal, northern European, and southern African upper molar mesiobuccal (mb) cusps, lower molar mesiobuccal cusps, and the lower first molar distobuccal (db) cusp. Sample sizes range from five (Neandertal M(1)db) to 29 (southern African M(1)mb). Neandertal mean perikymata numbers were found to differ significantly from those of both modern human samples (with the Neandertal mean higher) only for the M(2)mb. Regression analysis suggests that, with the exception of the M(2)mb, the hypothesis of equivalence between Neandertal and modern human lateral enamel formation time cannot be rejected. For the M(2)mb, regression analysis strongly suggests that this cusp took longer to form in the Neandertal sample than it did in the southern African sample. Plots of perikymata numbers across deciles of crown height demonstrate that Neandertal perikymata are distributed more evenly across the cervical and occlusal halves of molar crowns than they are in the modern human samples. These results are integrated into a discussion of Neandertal and modern human lateral enamel formation across the dentition, with reference to issues of life history and enamel growth processes.     

Unconstrained cranial evolution in Neandertals and modern humans compared to common chimpanzees

A variety of lines of evidence support the idea that neutral evolutionary processes (genetic drift, mutation) have been important in generating cranial differences between Neandertals and modern humans. But how do Neandertals and modern humans compare with other species? And how do these comparisons illuminate the evolutionary processes underlying cranial diversification? To address these questions, we used 27 standard cranial measurements collected on 2524 recent modern humans, 20 Neandertals and 237 common chimpanzees to estimate split times between Neandertals and modern humans, and between Pan troglodytes verus and two other subspecies of common chimpanzee. Consistent with a neutral divergence, the Neandertal versus modern human split-time estimates based on cranial measurements are similar to those based on DNA sequences. By contrast, the common chimpanzee cranial estimates are much lower than DNA-sequence estimates. Apparently, cranial evolution has been unconstrained in Neandertals and modern humans compared with common chimpanzees. Based on these and additional analyses, it appears that cranial differentiation in common chimpanzees has been restricted by stabilizing natural selection. Alternatively, this restriction could be due to genetic and/or developmental constraints on the amount of within-group variance (relative to effective population size) available for genetic drift to act on.     

Lumbar anomalies in the Shanidar 3 Neandertal

Recent examination of the Shanidar 3 remains revealed the presence of anomalous bilateral arthroses in the lumbar region. This paper describes this developmental anomaly, as well as several degenerative changes and offers potential etiologies.The Shanidar 3 remains represent an adult male Neandertal, approximately 35–50 years of age, dating to the Last Glacial. Although the partial skeleton is fragmentary, preserved elements include an almost complete set of ribs, portions of all thoracic vertebrae, all lumbar vertebrae, and the sacrum. Vertebral articulations from S1–T1 can be confidently assigned. The vertebra designated L1 is well preserved but lacks transverse processes. Instead, well defined bilateral articular surfaces, rather than transverse processes, are located on the pedicles. The skeletal elements associated with the anomalous L1 articulations were not recovered.The most likely interpretation is that the arthroses in question represent the facets for a 13th pair of ribs, a rare condition in modern hominid populations. Such lumbar developmental anomalies are an infrequent expression of a larger complex of cranial-caudal border shifting seen in the vertebral column. These shifts result in a change in the usual boundaries between the distinctive vertebral regions and are responsible for the majority of variability present in the vertebral column.     

Did the lateral enamel of Neandertal anterior teeth grow differently from that of modern humans?

The formation of lateral enamel in Neandertal anterior teeth has been the subject of recent studies. When compared to the anterior teeth of modern humans from diverse regions (Point Hope, Alaska; Newcastle upon Tyne, England; southern Africa), Neandertal anterior teeth appear to fall within the modern human range of variation for lateral enamel formation time. However, the lateral enamel growth curves of Neandertals are more linear than those of these modern human samples. Other researchers have found that the lateral enamel growth curves of Neandertals are more linear than those of Upper Paleolithic and Mesolithic modern humans as well. The statistical significance of this apparent difference between Neandertal and modern human lateral enamel growth curves is analyzed here. The more linear Neandertal enamel growth curves result from the smaller percentage of total perikymata located in the cervical halves of their teeth. The percentage of total perikymata in the cervical halves of teeth is therefore compared between the Neandertal sample (n=56 teeth) and each modern human population sample: Inuit (n=65 teeth), southern African (n=114 teeth), and northern European (n=115 teeth). There are 18 such comparisons (6 tooth types, Neandertals vs. each of the three modern human populations). Eighteen additional comparisons are made among the modern human population samples. Statistically significant differences are found for 16 of the 18 Neandertal vs. modern human comparisons but for only two of the 18 modern human comparisons. Statistical analyses repeated for subsamples of less worn teeth show a similar pattern. Because surface curvature is thought to affect perikymata spacing, we also conducted measurements to assess surface curvature in thirty teeth. Our analysis shows that surface curvature is not a factor in this lateral enamel growth difference between Neandertals and modern humans.     

Archaic and modern human distal humeral morphology

The morphology of the proximal ulna has been shown to effectively differentiate archaic or premodern humans (such as Homo heidelbergensis and H. neanderthalensis) from modern humans (H. sapiens). Accordingly, the morphology of adjacent, articulating elements should be able to distinguish these two broad groups as well. Here we test the taxonomic utility of another portion of the elbow, the distal humerus, as a discriminator of archaic and modern humans. Principal components analysis was employed on a suite of log-raw and log-shape distal humeral measures to examine differences between Neandertal and modern human distal humeri. In addition, the morphological affinities of Broken Hill (Kabwe) E.898, an archaic human distal humeral fragment from the middle Pleistocene of Zambia, and five Pliocene and early Pleistocene australopith humeri were assessed. The morphometric analyses effectively differentiated the Neandertals from the other groups, while the Broken Hill humerus appears morphologically similar to modern human distal humeri. Thus, an archaic/modern human dichotomy-as previously reported for proximal ulnar morphology-is not supported with respect to distal humeral morphology. Relative to australopiths and modern humans, Neandertal humeri are characterized by large olecranon fossae and small distodorsal medial and lateral pillars. The seeming disparity in morphological affinities of proximal ulnae (in which all archaic human groups appear distinct from modern humans) and distal humeri (in which Neandertals appear distinct from modern humans, but other archaic humans do not) is probably indicative of a highly variable, possibly transitional population of which our knowledge is hampered by sample-size limitations imposed by the scarcity of middle-to-late Pleistocene premodern human fossils outside of Europe.     

The derived FOXP2 variant of modern humans was shared with Neandertals

Although many animals communicate vocally, no extant creature rivals modern humans in language ability. Therefore, knowing when and under what evolutionary pressures our capacity for language evolved is of great interest. Here, we find that our closest extinct relatives, the Neandertals, share with modern humans two evolutionary changes in FOXP2, a gene that has been implicated in the development of speech and language. We furthermore find that in Neandertals, these changes lie on the common modern human haplotype, which previously was shown to have been subject to a selective sweep. These results suggest that these genetic changes and the selective sweep predate the common ancestor (which existed about 300,000-400,000 years ago) of modern human and Neandertal populations. This is in contrast to more recent age estimates of the selective sweep based on extant human diversity data. Thus, these results illustrate the usefulness of retrieving direct genetic information from ancient remains for understanding recent human evolution.     

Dental remains from the Grotte du Renne at Arcy-sur-Cure (Yonne)

Human remains associated with the earliest Upper Paleolithic industries are sparse. What is preserved is often fragmentary, making it difficult to accurately assign them to a particular species. For some time it has been generally accepted that Neandertals were responsible for the Chatelperronian and anatomically modern humans for the early Aurignacian industries. However, the recent re-dating of several of the more-complete modern human fossils associated with the early Aurignacian (e.g., Vogelherd) has led some to question the identity of the makers and the context of these early Upper Paleolithic industries. The Grotte du Renne at Arcy-sur-Cure, France has yielded many hominin remains, from Mousterian, Chatelperronian, Aurignacian, and Gravettian layers. Previously, a child's temporal bone from the Chatelperronian Layer Xb was recognized as belonging to a Neandertal; however, most of the teeth from Chatelperronian layers VIII-X remain unpublished. We describe the dental remains from the Chatelperronian layers, place them in a comparative (Mousterian Neandertal and Upper Paleolithic modern human) context, and evaluate their taxonomic status. The teeth (n = 29) represent a minimum of six individuals aged from birth to adult. The permanent dental sample (n = 15) from the Chatelperronian layers of Arcy-sur-Cure exhibits traits (e.g., lower molar mid-trigonid crest) that occur more frequently in Neandertals than in Upper Paleolithic modern humans. Furthermore, several teeth show trait combinations, including Cusp 6/mid-trigonid crest/anterior fovea in the lower second molar, that are rare or absent in Upper Paleolithic modern humans. The deciduous teeth (n = 14) significantly increase the sample of known deciduous hominin teeth and are more similar to Mousterian Neandertals from Europe and Asia than to Upper Paleolithic modern humans. Thus, the preponderance of dental evidence from the Grotte du Renne strongly supports that Neandertals were responsible for the Chatelperronian industry at Arcy-sur-Cure.     

Ontogenetic migration of the mental foramen in Neandertals and modern humans

Since the nineteenth century, researchers have noted that Neandertal and modern human adults differ in mental foramen position, although the ontogenetic changes in the position of this feature have only recently come under the scrutiny of paleoanthropologists. Research on mental foramen position has focused on whether this feature is inferior to a particular tooth. However, tooth position may not be a reliable indicator of mental foramen position because of variability in tooth size within and between taxa and during eruption events. As opposed to observing the mental foramen with respect to the postcanine teeth, we examined linear distances from the mental foramen to other mandibular landmarks. Modern human adults may appear truncated, or paedomorphic, in mental foramen position with respect to Neandertal adults. However, infants of the two taxa differ substantially in anterior mandibular form. The initial differences in the shape of the mental region may be related to the embryological position of the mental foramen in modern humans and its role in the development of the mental trigone. The shape changes that accrue thereafter, possibly from faster mandibular growth rates in Neandertals, further distinguish the adults from one another. Although mandibular shape differences exist from early infancy onwards, adults of the two taxa are broadly similar in bi-mental foramen breadth with respect to mandibular size. For this reason, qualitative assessments of mental foramen position may provide less taxonomic information than previously thought.     

The place of Neandertals in the evolution of hominid patterns of growth and development

This study uses the two developmental fields of dental maturation and femoral growth to determine if the pattern of growth and development in Neandertals (archaic Homo sapiens) was intermediate between that of Homo erectus and recent modern humans. Specimens used in the analysis included Neandertals and Upper Palaeolithic early modern Homo sapiens from Europe and individuals from two recent modern human populations. Ontogenetic data for the H. erectus adolescent KNM-WT 15000 and for Gorilla gorilla were included for comparison. Previous reports have indicated that H. erectus demonstrates a pattern of ontogeny characterized by earlier and more rapid linear growth than in modern humans. Results reported here demonstrate that Upper Paleolithic early modern Homo sapiens display a growth trajectory indistinguishable from that of recent modern humans. The pattern of Neandertal ontogeny is not intermediate between the pattern displayed in H. erectus and the derived pattern seen in the modern reference samples and the early modern H. sapiens sample. The Neandertal growth trajectory is consistent with either slow linear growth or advanced dental development.     

Diagnostic differences in mandibular P4 shape between Neandertals and anatomically modern humans

This study uses elliptical Fourier analysis to quantify shape differences observed in the P(4) crown of Neandertals and anatomically modern humans. Previously, P(4) shape was assessed qualitatively, and results suggested marked differences between Neandertals and anatomically modern humans (Bailey [2002] New Anat. 269:148-156). The goal of this study was to investigate the P(4) shape in more detail, quantifying it in order to determine its utility for taxonomic classification and phylogenetic analysis. A comparison of mean shapes confirms that the mesiolingual portion of the P(4) is truncated in Neandertals, and that this produces a distinctively asymmetrical P(4). A randomization test confirms that the shape difference between Neandertals and anatomically modern humans is significant. Principal component and discriminant function analyses indicate that the relative size of the lingual portion of the tooth also affects tooth shape, with the lingual portion of the Neandertal P(4) being narrower than that of anatomically modern humans. Classification of P(4) crown shapes using discriminant functions analysis is far from perfect. While 86.4% of the teeth were correctly classified, classification was much better for anatomically modern humans (98.1%) than it was for Neandertals (65%). Fortunately, crown shape is but one of several diagnostic characters of the P(4) crown. P(4) crown asymmetry can be added to the growing list of dental morphological characters distinguishing Neandertals from anatomically modern humans. Moreover, based on a comparison of mean tooth shapes in fossil and recent humans, symmetry, rather than asymmetry, appears to be the primitive state, and the high frequency of P(4) asymmetry is likely derived in Neandertals.     

The premaxilla in Neandertal and early modern children: ontogeny and morphology.

This comparative study of maxillae in Neandertals, Qafzeh, and extant children examines two specific traits: the premaxillary suture (sutura incisiva) and the interincisive sinuses, proposing a new hypothesis about some features of the Neandertal mid-face. Morphologic study of the premaxillary suture at its different borders (i.e. the nasal aspect of the frontal process, nasal and palatal aspects of the palatal process of the maxilla) indicates a persistence of the suture among very young Neandertal children in comparison to the condition in extant ones. This suggests a longer independence of some parts of the premaxilla in Neandertals. To further examine this possibility, CT scans of two Neandertal children were analyzed: Roc de Marsal, estimated to be about 3 years, and Engis 2, estimated to be about 5-6 years. The results are quite different between the fossils. In the older, the premaxillary suture is represented only by a deep groove. In the younger it extends deep to the surface of the nasal process reaching the Parinaud's canal. Synostosis of the premaxillary suture was found to occur later in Neandertal children than in modern ones. Moreover, we observed the existence of two interincisive sinuses in the fossil children, whereas this is rare in modern children (present on only 2% of our sample of 0-6 year-old infants, n = 247).Persistence of an open premaxillary suture represents the potential for an extended period of growth of the Neandertal mid-face. Although no trace of the premaxillary suture remains in adult Neandertals, Neandertals present many features classically considered as consequences of this persistence. The two interincisive sinuses could be a consequence of the labio-lingual diameter of the incisors. The results presented here can be further investigated by additional studies on the cranial sutural system and by precise morphologic observations and CT scans of the mid-face of a larger sample of fossil children.