Late archaic and modern Homo sapiens from Europe, Africa, and Southwest Asia: Craniometric comparisons and phylogenetic implications

The craniometric affinities among Neandertals. Upper Palcolithic Europeans, early anatomically modern Southwest Asians, and archaic and modern Africans are investigated using univariate and multivariate methods. For the first time, it is possible to analyse the North African finds Dar-es-Soltane 5, Nazlet Khater, and Wadi Kubbaniya. It was not possible to include the Neandertals from Central Europe due to their poor state of preservation. The results point to, first, a basic distinction between Neandertals on the one hand and modern humans from all geographic regions on the other, and, secondly, to great similarities between modern African and European populations. Late archaic sapiens specimens from Africa were more similar to Upper Paleolithic Europeans than were the Neandertals. The results do not support the hypothesis that a regional evolution giving rise to modern humans took place in Europe. The results are, however, consistent with the hypothesis that modern populations originated in Africa and spread to Europe from there.     

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.     

Modern humans did not admix with Neanderthals during their range expansion into Europe

The process by which the Neanderthals were replaced by modern humans between 42,000 and 30,000 before present is still intriguing. Although no Neanderthal mitochondrial DNA (mtDNA) lineage is found to date among several thousands of Europeans and in seven early modern Europeans, interbreeding rates as high as 25% could not be excluded between the two subspecies. In this study, we introduce a realistic model of the range expansion of early modern humans into Europe, and of their competition and potential admixture with local Neanderthals. Under this scenario, which explicitly models the dynamics of Neanderthals' replacement, we estimate that maximum interbreeding rates between the two populations should have been smaller than 0.1%. We indeed show that the absence of Neanderthal mtDNA sequences in Europe is compatible with at most 120 admixture events between the two populations despite a likely cohabitation time of more than 12,000 y. This extremely low number strongly suggests an almost complete sterility between Neanderthal females and modern human males, implying that the two populations were probably distinct biological species.     

Complex History of Admixture between Modern Humans and Neandertals

Recent analyses have found that a substantial amount of the Neandertal genome persists in the genomes of contemporary non-African individuals. East Asians have, on average, higher levels of Neandertal ancestry than do Europeans, which might be due to differences in the efficiency of purifying selection, an additional pulse of introgression into East Asians, or other unexplored scenarios. To better define the scope of plausible models of archaic admixture between Neandertals and anatomically modern humans, we analyzed patterns of introgressed sequence in whole-genome data of 379 Europeans and 286 East Asians. We found that inferences of demographic history restricted to neutrally evolving genomic regions allowed a simple one-pulse model to be robustly rejected, suggesting that differences in selection cannot explain the differences in Neandertal ancestry. We show that two additional demographic models, involving either a second pulse of Neandertal gene flow into the ancestors of East Asians or a dilution of Neandertal lineages in Europeans by admixture with an unknown ancestral population, are consistent with the data. Thus, the history of admixture between modern humans and Neandertals is most likely more complex than previously thought.     

Throwing in the Middle and Upper Paleolithic: inferences from an analysis of humeral retroversion

When in evolutionary history did long-range projectile weapons become an important component of hunting toolkits? The archeological evidence for the development of projectile weaponry is complex and generally indirect, and has led to different conclusions about the origin and spread of this technology. Lithic evidence from the Middle Stone Age (MSA) has led some researchers to suggest that true long- range projectile weaponry developed in Africa perhaps as early as 80,000 years ago, and was part of the subsistence toolkit carried by modern humans who expanded out of Africa after 50,000 years ago. Alternatively, temporal patterns in the morphology of pointed lithics has led others to posit an independent, convergent origin of projectile weaponry in Africa, the Near East, and Europe during the interval between 50,000-40,000 years ago. By either scenario, projectile weapons would not have been a component of the hunting arsenal of Neandertals, but may have been in use by European early modern humans and thus, projectile technology may have entered into the competitive dynamics that existed between these two groups. The origins of projectile weapons can be addressed, in part, through analyses of the skeletal remains of the prehistoric humans who made and used them. Habitual behavior patterns—including those related to the production and use of technology—can be imprinted on the skeleton through both genetic and epigenetic pathways. Recent studies in the field of sports medicine indicate that individuals who engage in habitual throwing have increased humeral retroversion angles in their throwing arms and a greater degree of bilateral asymmetry in retroversion angles than do non-throwers. This contribution investigates humeral torsion through analysis of the retroversion angle in samples of Eurasian Neandertals, European early modern humans of the middle and late Upper Paleolithic, and comparative samples of recent humans. This analysis was conducted under the assumption that if throwing-based projectile weaponry was used by early modern Europeans but not Neandertals, Upper Paleolithic samples should be similar to recent human groups engaged in habitual throwing in the degree of humeral retroversion in the dominant limb and in bilateral asymmetry in this feature. Neandertals on the other hand, would not be expected to show marked asymmetry in humeral retroversion. Consistent with other studies, Neandertals exhibit increased retroversion angles (decreased humeral torsion or a more posteriorly oriented humeral head) relative to most modern human samples, although this appears more likely related to body form and overall activity levels than to habitual throwing. Although Neandertals with bilaterally preserved humeri sufficient for measurement are rare (consisting of only two males and one female), levels of bilateral asymmetry in humeral retroversion are low, suggesting a lack of regular throwing. While patterning across fossil and comparative samples in levels of humeral retroversion was not clear cut, males of both the middle and late Upper Paleolithic demonstrate a high level of bilateral asymmetry, comparable to or in excess of that seen in samples of throwing athletes. This may indicate habitual use of throwing-based projectile weaponry by middle Upper Paleolithic times. Small sample sizes and relatively great variance in the fossil samples makes these results, however, suggestive rather than conclusive.     

Neandertal Demise: An Archaeological Analysis of the Modern Human Superiority Complex

Neandertals are the best-studied of all extinct hominins, with a rich fossil record sampling hundreds of individuals, roughly dating from between 350,000 and 40,000 years ago. Their distinct fossil remains have been retrieved from Portugal in the west to the Altai area in central Asia in the east and from below the waters of the North Sea in the north to a series of caves in Israel in the south. Having thrived in Eurasia for more than 300,000 years, Neandertals vanished from the record around 40,000 years ago, when modern humans entered Europe. Modern humans are usually seen as superior in a wide range of domains, including weaponry and subsistence strategies, which would have led to the demise of Neandertals. This systematic review of the archaeological records of Neandertals and their modern human contemporaries finds no support for such interpretations, as the Neandertal archaeological record is not different enough to explain the demise in terms of inferiority in archaeologically visible domains. Instead, current genetic data suggest that complex processes of interbreeding and assimilation may have been responsible for the disappearance of the specific Neandertal morphology from the fossil record.     

An Extended Admixture Pulse Model Reveals the Limitations to Human–Neandertal Introgression Dating

Neandertal DNA makes up 2–3% of the genomes of all non-African individuals. The patterns of Neandertal ancestry in modern humans have been used to estimate that this is the result of gene flow that occurred during the expansion of modern humans into Eurasia, but the precise dates of this event remain largely unknown. Here, we introduce an extended admixture pulse model that allows joint estimation of the timing and duration of gene flow. This model leads to simple expressions for both the admixture segment distribution and the decay curve of ancestry linkage disequilibrium, and we show that these two statistics are closely related. In simulations, we find that estimates of the mean time of admixture are largely robust to details in gene flow models, but that the duration of the gene flow can only be recovered if gene flow is very recent and the exact recombination map is known. These results imply that gene flow from Neandertals into modern humans could have happened over hundreds of generations. Ancient genomes from the time around the admixture event are thus likely required to resolve the question when, where, and for how long humans and Neandertals interacted.     

Ancient DNA: would the real Neandertal please stand up?

Mitochondrial DNA sequences recovered from eight Neandertal specimens cannot be detected in either early fossil Europeans or in modern populations. This indicates that, if Neandertals made any genetic contribution at all to modern humans, it must have been limited, though the extent of the contribution cannot be resolved at present.     

Genetic evidence and the modern human origins debate

A continued debate in anthropology concerns the evolutionary origin of 'anatomically modern humans' (Homo sapiens sapiens). Different models have been proposed to examine the related questions of (1) where and when anatomically modern humans first appeared and (2) the genetic and evolutionary relationship between modern humans and earlier human populations. Genetic data have been increasingly used to address these questions. Genetic data on living human populations have been used to reconstruct the evolutionary history of the human species by considering how global patterns of human variation could be produced given different evolutionary scenarios. Of particular interest are gene trees that reconstruct the time and place of the most recent common ancestor of humanity for a given haplotype and the analysis of regional differences in genetic diversity. Ancient DNA has also allowed a direct assessment of genetic variation in European Neandertals. Together with the fossil record, genetic data provide insight into the origin of modern humans. The evidence points to an African origin of modern humans dating back to 200,000 years followed by later expansions of moderns out of Africa across the Old World. What is less clear is what happened when these early modern humans met preexisting 'archaic human' populations outside of Africa. At present, it is difficult to distinguish between a model of total genetic replacement and a model that includes some degree of genetic mixture.     

Comparing models on the genealogical relationships among Neandertal, Cro-Magnoid and modern Europeans by serial coalescent simulations

Populations of anatomically archaic (Neandertal) and early modern (Cro-Magnoid) humans are jointly documented in the European fossil record, in the period between 40 000 and 25 000 years BP, but the large differences between their cultures, morphologies and DNAs suggest that the two groups were not close relatives. However, it is still unclear whether any genealogical continuity between them can be ruled out. Here, we simulated a broad range of demographic scenarios by means of a serial coalescence algorithm in which Neandertals, Cro-Magnoids and modern Europeans were either part of the same mitochondrial genealogy or of two separate genealogies. Mutation rates, population sizes, population structure and demographic growth rates varied across simulations. All models in which anatomically modern (that is, Cro-Magnoid and current) Europeans belong to a distinct genealogy performed better than any model in which the three groups were assigned to the same mitochondrial genealogy. The maximum admissible level of gene flow between Neandertals and the ancestors of current Europeans is 0.001% per generation, one order of magnitude lower than estimated in previous studies not considering genetic data on Cro-Magnoid people.     

An X-linked haplotype of Neandertal origin is present among all non-African populations

Recent work on the Neandertal genome has raised the possibility of admixture between Neandertals and the expanding population of Homo sapiens who left Africa between 80 and 50 Kya (thousand years ago) to colonize the rest of the world. Here, we provide evidence of a notable presence (9% overall) of a Neandertal-derived X chromosome segment among all contemporary human populations outside Africa. Our analysis of 6,092 X-chromosomes from all inhabited continents supports earlier contentions that a mosaic of lineages of different time depths and different geographic provenance could have contributed to the genetic constitution of modern humans. It indicates a very early admixture between expanding African migrants and Neandertals prior to or very early on the route of the out-of-Africa expansion that led to the successful colonization of the planet.     

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.     

Is human longevity a consequence of cultural change or modern biology?

Increased longevity, expressed as the number of individuals surviving to older adulthood, represents a key way that Upper Paleolithic Europeans differ from earlier European (Neandertal) populations. Here, we address whether longevity increased as a result of cultural/adaptive change in Upper Paleolithic Europe, or whether it was introduced to Europe as a part of modern human biology. We compare the ratio of older to younger adults (OY ratio) in an early modern human sample associated with the Middle Paleolithic from Western Asia with OY ratios of European Upper Paleolithic moderns and penecontemporary Neandertals from the same region. We also compare these Neandertals to European Neandertals. The difference between the OY ratios of modern humans of the Middle and Upper Paleolithic is large and significant, but there is no significant difference between the Neandertals and early modern humans of Western Asia. Longevity for the West Asian Neandertals is significantly more common than for the European Neandertals. We conclude that the increase in adult survivorship associated with the Upper Paleolithic is not a biological attribute of modern humans, but reflects important cultural adaptations promoting the demographic and material representations of modernity.     

Brief communication: The distribution of perikymata on Qafzeh anterior teeth

Recent studies have suggested that Neandertals and modern humans differ in the distribution of perikymata (enamel growth increments) over their permanent anterior tooth crowns. In modern humans, perikymata become increasingly more compact toward the cervix than they do in Neandertals. Previous studies have suggested that a more homogeneous distribution of perikymata, like that of Neandertals, characterizes the anterior teeth of Homo heidelbergensis and Homo erectus as well. Here, we investigated whether Qafzeh anterior teeth (N = 14) differ from those of modern southern Africans, northern Europeans, and Alaskans (N = 47–74 depending on tooth type) in the percentage of perikymata present in their cervical halves. Using the normally distributed modern human values for each tooth type, we calculated Z‐scores for the 14 Qafzeh teeth. All but two of the 14 Qafzeh teeth had negative Z‐scores, meaning that values equal to these would be found in the bottom 50% of the modern human samples. Seven of the 14 would be found in the lowest 5% of the modern human distribution. Qafzeh teeth therefore appear to differ from those of modern humans in the same direction that Neandertals do: with generally lower percentages of perikymata in their cervical regions. The similarity between them appears to represent the retention of a perikymata distribution pattern present in earlier members of the genus Homo, but not generally characteristic of modern humans from diverse regions of the world. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

The effects of distal limb segment shortening on locomotor efficiency in sloped terrain: implications for Neandertal locomotor behavior

Past studies of human locomotor efficiency focused on movement over flat surfaces and concluded that Neandertals were less efficient than modern humans due to a truncated limb morphology, which may have developed to aid thermoregulation in cold climates. However, it is not clear whether this potential locomotor disadvantage would also exist in nonflat terrain. This issue takes on added importance since Neandertals likely spent a significant proportion of their locomotor schedule on sloped, mountainous terrains in the Eurasian landscape. Here a model is developed that determines the relationship between lower limb segment lengths, terrain slope, excursion angle at the hip, and step length. The model is applied to Neandertal and modern human lower limb reconstructions. In addition, for a further independent test that also allows more climateterrain cross comparisons, the same model is applied to bovids living in different terrains and climates. Results indicate that: (1) Neandertals, despite exhibiting shorter lower limbs, would have been able to use similar stride frequencies per speed as longer-limbed modern humans on sloped terrain, due to their lower crural indices; and (2) shortened distal limb segments are characteristic of bovids that inhabit more rugged terrains, regardless of climate. These results suggest that the shortened distal lower limb segments of Neandertals were not a locomotor disadvantage within more rugged environments.     

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.     

Were neandertal and modern human cranial differences produced by natural selection or genetic drift?

Most evolutionary explanations for cranial differences between Neandertals and modern humans emphasize adaptation by natural selection. Features of the crania of Neandertals could be adaptations to the glacial climate of Pleistocene Europe or to the high mechanical strains produced by habitually using the front teeth as tools, while those of modern humans could be adaptations for articulate speech production. A few researchers have proposed non-adaptive explanations. These stress that isolation between Neandertal and modern human populations would have lead to cranial diversification by genetic drift (chance changes in the frequencies of alleles at genetic loci contributing to variation in cranial morphology). Here we use a variety of statistical tests founded on explicit predictions from quantitative- and population-genetic theory to show that genetic drift can explain cranial differences between Neandertals and modern humans. These tests are based on thirty-seven standard cranial measurements from a sample of 2524 modern humans from 30 populations and 20 Neandertal fossils. As a further test, we compare our results for modern human cranial measurements with those for a genetic dataset consisting of 377 microsatellites typed for a sample of 1056 modern humans from 52 populations. We conclude that rather than requiring special adaptive accounts, Neandertal and modern human crania may simply represent two outcomes from a vast space of random evolutionary possibilities.     

Age of the Association between Helicobacter pylori and Man

When modern humans left Africa ca. 60,000 years ago (60 kya), they were already infected with Helicobacter pylori, and these bacteria have subsequently diversified in parallel with their human hosts. But how long were humans infected by H. pylori prior to the out-of-Africa event? Did this co-evolution predate the emergence of modern humans, spanning the species divide? To answer these questions, we investigated the diversity of H. pylori in Africa, where both humans and H. pylori originated. Three distinct H. pylori populations are native to Africa: hpNEAfrica in Afro-Asiatic and Nilo-Saharan speakers, hpAfrica1 in Niger-Congo speakers and hpAfrica2 in South Africa. Rather than representing a sustained co-evolution over millions of years, we find that the coalescent for all H. pylori plus its closest relative H. acinonychis dates to 88–116 kya. At that time the phylogeny split into two primary super-lineages, one of which is associated with the former hunter-gatherers in southern Africa known as the San. H. acinonychis, which infects large felines, resulted from a later host jump from the San, 43–56 kya. These dating estimates, together with striking phylogenetic and quantitative human-bacterial similarities show that H. pylori is approximately as old as are anatomically modern humans. They also suggest that H. pylori may have been acquired via a single host jump from an unknown, non-human host. We also find evidence for a second Out of Africa migration in the last 52,000 years, because hpEurope is a hybrid population between hpAsia2 and hpNEAfrica, the latter of which arose in northeast Africa 36–52 kya, after the Out of Africa migrations around 60 kya.     

Postcranial remains and the origin of modern humans

The nature, timing, and location of the origin of modern humans has been the subject of intense controversy for the last 15 years.^1–4 Genetic data and new radiometric dates for key fossils that lie beyond the range of radiocarbon dating have substantially added to the knowledge derived from the fossil evidence documenting the transition from archaic to modern humans. These new data, however, have failed to resolve the problem in its entirety. Most authorities now accept that Africa played an important, and probably central, role in the origin of modern humans.^7–13 The genetic evidence seems to be particularly emphatic that an African population that existed between 200,000 and 100,000 years ago (100 ka) is ancestral to all living humans.^6,7 Controversy still surrounds the question of how much, if at all, archaic humans from outside of Africa, such as Neandertals, late archaic Chinese hominins such as Jinniushan, and the Indonesian Ngandong hominins, may have contributed to the morphological and genetic diversity present in living populations and the morphology of the earliest fossils of modern humans.¹⁰     

Do modern humans and Neandertals have different patterns of cranial integration?

Studies of cranial differences between modern humans and Neandertals have identified several characteristics for which the two groups differ in their mean values, the proportional relationships with other traits, or both. However, the limited number of fairly complete Neandertals has hindered investigations into patterns of integration – covariance and correlation among traits – in this fossil group. Here, we use multiple approaches specifically designed to deal with fragmentary fossils to test if metric cranial traits in Neandertals fit modern human patterns of integration. Based on 37 traits collected from a sample of 2524 modern humans from Howells’ data set and 20 Neandertals, we show that overall patterns of cranial integration are significantly different between Neandertals and modern humans. However, at the same time, Neandertals are consistent with a modern human pattern of integration for more than three-quarters of the traits. Additionally, the differences between the predicted and actual values for the deviating traits are rather small, indicating that the differences in integration are subtle. Traits for which Neandertals deviate from modern human integration patterns tend to be found in regions where Neandertals and modern humans are known to also differ in their mean values. We conclude that the evolution of patterns of cranial integration is a cause for caution but also presents an opportunity for understanding cranial differences between modern humans and Neandertals.