Has the combination of genetic and fossil evidence solved the riddle of modern human origins?

Debate over the origin of modern humans continues without a clear end in sight. Currently, the genetic and fossil evidence is still used to support two different interpretations of the origin of modern humans. Some researchers claim that the genetic evidence is compatible with either an Out‐of‐Africa or a Multiregional model, while other scientists argue that the evidence supports only a Multiregional model of evolution. I argue that the fossil record and archeological evidence constrain interpretation of the genetic evidence and imply that very little, if any, admixture with Eurasian archaic hominins such as the Neanderthals occurred during the spread of modern humans out of Africa.     

The Middle/Later Stone Age transition and cultural dynamics of late Pleistocene East Africa

The Middle to Later Stone Age (MSA/LSA) transition is a prominent feature of the African archeological record that began in some places ~30,000–60,000 years ago, historically associated with the origin and/or dispersal of “modern” humans. Unlike the analogous Middle to Upper Paleolithic transition in Eurasia and associated Neanderthal extinction, the African MSA/LSA record remains poorly documented, with its potential role in explaining changes in the behavioral diversity and geographic range of Homo sapiens largely unexplored. I review archeological and biogeographic data from East Africa, show regionally diverse pathways to the MSA/LSA transition, and emphasize the need for analytical approaches that document potential ancestor‐descendent relationships visible in the archeological record, needed to assess independent invention, population interaction, dispersal, and other potential mechanisms for behavioral change. Diversity within East Africa underscores the need for regional, rather than continental‐scale narratives of the later evolutionary history of H. sapiens.     

Did a discrete event 200,000-100,000 years ago produce modern humans?

Scenarios for modern human origins are often predicated on the assumption that modern humans arose 200,000-100,000 years ago in Africa. This assumption implies that something ‘special’ happened at this point in time in Africa, such as the speciation that produced Homo sapiens, a severe bottleneck in human population size, or a combination of the two. The common thread is that after the divergence of the modern human and Neandertal evolutionary lineages ∼400,000 years ago, there was another discrete event near in time to the Middle-Late Pleistocene boundary that produced modern humans. Alternatively, modern human origins could have been a lengthy process that lasted from the divergence of the modern human and Neandertal evolutionary lineages to the expansion of modern humans out of Africa, and nothing out of the ordinary happened 200,000-100,000 years ago in Africa.Three pieces of biological (fossil morphology and DNA sequences) evidence are typically cited in support of discrete event models. First, living human mitochondrial DNA haplotypes coalesce ∼200,000 years ago. Second, fossil specimens that are usually classified as ‘anatomically modern’ seem to appear shortly afterward in the African fossil record. Third, it is argued that these anatomically modern fossils are morphologically quite different from the fossils that preceded them.Here I use theory from population and quantitative genetics to show that lengthy process models are also consistent with current biological evidence. That this class of models is a viable option has implications for how modern human origins is conceptualized.     

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     

Neandertals and moderns mixed,and it matters

Twenty‐five years ago, the Middle‐to‐Upper Paleolithic transition in Europe could be represented as a straightforward process subsuming both the emergence of symbolic behavior and the replacement of Neandertals by modern humans. The Aurignacian was a proxy for the latter, during which enhanced cognitive capabilities explained ornaments and art. The few instances of Neandertal symbolism were deemed to long postdate contact and dismissed as “imitation without understanding,” if not geological contamination. Such views were strengthened by the recent finding that, in southern Africa, several features of the European Upper Paleolithic, including bone tools, ornaments, and microliths, emerged much earlier. Coupled with genetic suggestions of a recent African origin for extant humans, fossil discoveries bridging the transition between “archaics” and “moderns” in the realm of anatomy (Omo‐Kibish, Herto) seemingly closed the case. Over the last decade, however, taphonomic critiques of the archeology of the transition have made it clear that, in Europe, fully symbolic sapiens behavior predates both the Aurignacian and moderns. And, in line with evidence from the nuclear genome rejecting strict replacement models based on mtDNA alone, the small number of early modern specimens that passed the test of direct dating present archaic features unknown in the African lineage, suggesting admixture at the time of contact. In the realm of culture, the archeological evidence also supports a Neandertal contribution to Europe's earliest modern human societies, which feature personal ornaments completely unknown before immigration and are characteristic of such Neandertal‐associated archeological entities as the Châtelperronian and the Uluzzian. The chronometric data suggest that, north of the Ebro divide, the entire interaction process may have been resolved within the millennium centered around 42,000 calendar years ago. Such a rapid absorption of the Neandertals is consistent with the size imbalance between the two gene reservoirs and further supports significant levels of admixture.     

Technological complexity and the global dispersal of modern humans

Anatomically modern humans (Homo sapiens) dispersed out of Africa roughly 120,000 years ago and again after 75,000 years ago. The early dispersal was geographically restricted to the Arabian Peninsula, Levant, and possibly parts of southern Asia. The later dispersal was ultimately global in scope, including areas not previously occupied by Homo. One explanation for the contrast between the two out‐of‐Africa dispersals is that the modern humans who expanded into Eurasia 120,000 years ago lacked the functionally and structurally complex technology of recent hunter‐gatherers. This technology, which includes, for example, mechanical projectiles, snares and traps, and sewn clothing, provides not only expanded dietary breadth and increased rates of foraging efficiency and success in places where plant and animal productivity is low, but protection from cold weather in places where winter temperatures are low. The absence of complex technology before 75,000 years ago also may explain why modern humans in the Levant did not develop sedentary settlements and agriculture 120,000 years ago (i.e., during the Last Interglacial).     

The Expansion of mtDNA Haplogroup L3 within and out of Africa

Although fossil remains show that anatomically modern humans dispersed out of Africa into the Near East ～100 to 130 ka, genetic evidence from extant populations has suggested that non-Africans descend primarily from a single successful later migration. Within the human mitochondrial DNA (mtDNA) tree, haplogroup L3 encompasses not only many sub-Saharan Africans but also all ancient non-African lineages, and its age therefore provides an upper bound for the dispersal out of Africa. An analysis of 369 complete African L3 sequences places this maximum at ～70 ka, virtually ruling out a successful exit before 74 ka, the date of the Toba volcanic supereruption in Sumatra. The similarity of the age of L3 to its two non-African daughter haplogroups, M and N, suggests that the same process was likely responsible for both the L3 expansion in Eastern Africa and the dispersal of a small group of modern humans out of Africa to settle the rest of the world. The timing of the expansion of L3 suggests a link to improved climatic conditions after ～70 ka in Eastern and Central Africa rather than to symbolically mediated behavior, which evidently arose considerably earlier. The L3 mtDNA pool within Africa suggests a migration from Eastern Africa to Central Africa ～60 to 35 ka and major migrations in the immediate postglacial again linked to climate. The largest population size increase seen in the L3 data is 3-4 ka in Central Africa, corresponding to Bantu expansions, leading diverse L3 lineages to spread into Eastern and Southern Africa in the last 3-2 ka.     

Late Pleistocene human population bottlenecks, volcanic winter, and differentiation of modern humans

The “Weak Garden of Eden” model for the origin and dispersal of modern humans (Harpendinget al., 1993) posits that modern humans spread into separate regions from a restricted source, around 100 ka (thousand years ago), then passed through population bottlenecks. Around 50 ka, dramatic growth occurred within dispersed populations that were genetically isolated from each other. Population growth began earliest in Africa and later in Eurasia and is hypothesized to have been caused by the invention and spread of a more efficient Later Stone Age/Upper Paleolithic technology, which developed in equatorial Africa.Climatic and geological evidence suggest an alternative hypothesis for Late Pleistocene population bottlenecks and releases. The last glacial period was preceded by one thousand years of the coldest temperatures of the Later Pleistocene (∼71–70 ka), apparently caused by the eruption of Toba, Sumatra. Toba was the largest known explosive eruption of the Quaternary. Toba's volcanic winter could have decimated most modern human populations, especially outside of isolated tropical refugia. Release from the bottleneck could have occurred either at the end of this hypercold phase, or 10,000 years later, at the transition from cold oxygen isotope stage 4 to warmer stage 3. The largest populations surviving through the bottleneck should have been found in the largest tropical refugia, and thus in equatorial Africa. High genetic diversity in modern Africans may thus reflect a less severe bottleneck rather than earlier population growth.Volcanic winter may have reduced populations to levels low enough for founder effects, genetic drift and local adaptations to produce rapid population differentiation. If Toba caused the bottlenecks, then modern human races may have differentiated abruptly, only 70 thousand years ago.     

Global invasion history of the Mediterranean recluse spider: a concordance with human expansion

The dispersal of modern humans from their African origins to the rest of the occupied world is a topic of lively debate centering principally on single versus multiple dispersals. The Mediterranean recluse spider Loxosceles rufescens, a significant pest, has gained much of its current distribution through commensalism with humans. Therefore, the matrilineal history of this spider should reflect dispersal patterns of human females. Here, an assessment of genetic variation at mitochondrial markers in 347 colonies of L. rufescens from 104 geographic sites worldwide reveals a north African origin of the global populations of L. rufescens. This involves at least three separate events among which two involve coincidental dispersals, including one to north Africa, Europe, Asia, North America, and Australia and the other to north Africa, Europe, and Asia only. North African L. rufescens appear to have expanded initially into Israel and subsequently spread into Greece, where a subset of these populations went eastward into Iran and southeastern Asia. This corresponds to the modern human southern dispersal theory. Chinese populations appear to have expanded approximately 42 710–46 008 yr ago. The initial split between the Greek and Chinese populations dates to 41 412–44 444 yr ago, which coincides with the expansion of modern humans into Southeast and East Asia. Thus, the matrilineal history of Asian L. rufescens tracks the history of human dispersals over tens of thousands of years.     

The environmental context for the origins of modern human diversity: a synthesis of regional variability in African climate 150,000-30,000 years ago

We synthesize African paleoclimate from 150 to 30 ka (thousand years ago) using 85 diverse datasets at a regional scale, testing for coherence with North Atlantic glacial/interglacial phases and northern and southern hemisphere insolation cycles. Two major determinants of circum-African climate variability over this time period are supported by principal components analysis: North Atlantic sea surface temperature (SST) variations and local insolation maxima. North Atlantic SSTs correlated with the variability found in most circum-African SST records, whereas the variability of the majority of terrestrial temperature and precipitation records is explained by local insolation maxima, particularly at times when solar radiation was intense and highly variable (e.g., 150-75 ka). We demonstrate that climates varied with latitude, such that periods of relatively increased aridity or humidity were asynchronous across the northern, eastern, tropical and southern portions of Africa. Comparisons of the archaeological, fossil, or genetic records with generalized patterns of environmental change based solely on northern hemisphere glacial/interglacial cycles are therefore imprecise.We compare our refined climatic framework to a database of 64 radiometrically-dated paleoanthropological sites to test hypotheses of demographic response to climatic change among African hominin populations during the 150-30 ka interval. We argue that at a continental scale, population and climate changes were asynchronous and likely occurred under different regimes of climate forcing, creating alternating opportunities for migration into adjacent regions. Our results suggest little relation between large scale demographic and climate change in southern Africa during this time span, but strongly support the hypothesis of hominin occupation of the Sahara during discrete humid intervals ∼135-115 ka and 105-75 ka. Hominin populations in equatorial and eastern Africa may have been buffered from the extremes of climate change by locally steep altitudinal and rainfall gradients and the complex and variable effects of increased aridity on human habitat suitability in the tropics. Our data are consistent with hominin migrations out of Africa through varying exit points from ∼140-80 ka.     

Indian Siddis: African descendants with Indian admixture

The Siddis (Afro-Indians) are a tribal population whose members live in coastal Karnataka, Gujarat, and in some parts of Andhra Pradesh. Historical records indicate that the Portuguese brought the Siddis to India from Africa about 300-500 years ago; however, there is little information about their more precise ancestral origins. Here, we perform a genome-wide survey to understand the population history of the Siddis. Using hundreds of thousands of autosomal markers, we show that they have inherited ancestry from Africans, Indians, and possibly Europeans (Portuguese). Additionally, analyses of the uniparental (Y-chromosomal and mitochondrial DNA) markers indicate that the Siddis trace their ancestry to Bantu speakers from sub-Saharan Africa. We estimate that the admixture between the African ancestors of the Siddis and neighboring South Asian groups probably occurred in the past eight generations (～200 years ago), consistent with historical records.     

The Date of Interbreeding between Neandertals and Modern Humans

Comparisons of DNA sequences between Neandertals and present-day humans have shown that Neandertals share more genetic variants with non-Africans than with Africans. This could be due to interbreeding between Neandertals and modern humans when the two groups met subsequent to the emergence of modern humans outside Africa. However, it could also be due to population structure that antedates the origin of Neandertal ancestors in Africa. We measure the extent of linkage disequilibrium (LD) in the genomes of present-day Europeans and find that the last gene flow from Neandertals (or their relatives) into Europeans likely occurred 37,000–86,000 years before the present (BP), and most likely 47,000–65,000 years ago. This supports the recent interbreeding hypothesis and suggests that interbreeding may have occurred when modern humans carrying Upper Paleolithic technologies encountered Neandertals as they expanded out of Africa.     

Natives or immigrants: modern human origin in east Asia

East Asia is one of the few regions in the world where a relatively large number of human fossils have been unearthed--a discovery that has been taken as evidence for an independent local origin of modern humans outside of Africa. However, genetic studies conducted in the past ten years, especially using Y chromosomes, have provided unequivocal evidence for an African origin of East Asian populations. The genetic signatures present in diverse East Asian populations mark the footsteps of prehistoric migrations that occurred tens of thousands of years ago.     

Human evolution

The common ancestor of modern humans and the great apes is estimated to have lived between 5 and 8 Myrs ago, but the earliest evidence in the human, or hominid, fossil record is Ardipithecus ramidus, from a 4.5 Myr Ethiopian site. This genus was succeeded by Australopithecus, within which four species are presently recognised. All combine a relatively primitive postcranial skeleton, a dentition with expanded chewing teeth and a small brain. The most primitive species in our own genus, Homo habilis and Homo rudolfensis, are little advanced over the australopithecines and with hindsight their inclusion in Homo may not be appropriate. The first species to share a substantial number of features with later Homo is Homo ergaster, or ‘early African Homo erectus’, which appears in the fossil record around 2.0 Myr. Outside Africa, fossil hominids appear as Homo erectus-like hominids, in mainland Asia and in Indonesia close to 2 Myr ago; the earliest good evidence of ‘archaic Homo’ in Europe is dated at between 600–700 Kyr before the present. Anatomically modern human, or Homo sapiens, fossils are seen first in the fossil record in Africa around 150 Kyr ago. Taken together with molecular evidence on the extent of DNA variation, this suggests that the transition from ‘archiac’ to ‘modern’ Homo may have taken place in Africa.     

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.     

Continuity of Microblade Technology in the Indian Subcontinent Since 45 ka: Implications for the Dispersal of Modern Humans

We extend the continuity of microblade technology in the Indian Subcontinent to 45 ka, on the basis of optical dating of microblade assemblages from the site of Mehtakheri, (22° 13'' 44″ N Lat 76° 01'' 36″ E Long) in Madhya Pradesh, India. Microblade technology in the Indian Subcontinent is continuously present from its first appearance until the Iron Age (~3 ka), making its association with modern humans undisputed. It has been suggested that microblade technology in the Indian Subcontinent was developed locally by modern humans after 35 ka. The dates reported here from Mehtakheri show this inference to be untenable and suggest alternatively that this technology arrived in the Indian Subcontinent with the earliest modern humans. It also shows that modern humans in Indian Subcontinent and SE Asia were associated with differing technologies and this calls into question the “southern dispersal” route of modern humans from Africa through India to SE Asia and then to Australia. We suggest that modern humans dispersed from Africa in two stages coinciding with the warmer interglacial conditions of MIS 5 and MIS 3. Competitive interactions between African modern humans and Indian archaics who shared an adaptation to tropical environments differed from that between modern humans and archaics like Neanderthals and Denisovans, who were adapted to temperate environments. Thus, while modern humans expanded into temperate regions during warmer climates, their expansion into tropical regions, like the Indian Subcontinent, in competition with similarly adapted populations, occurred during arid climates. Thus modern humans probably entered the Indian Subcontinent during the arid climate of MIS 4 coinciding with their disappearance from the Middle East and Northern Africa. The out of phase expansion of modern humans into tropical versus temperate regions has been one of the factors affecting the dispersal of modern humans from Africa during the period 200–40 ka.     

Geography predicts neutral genetic diversity of human populations

A leading theory for the origin of modern humans, the ‘recent African origin’ (RAO) model [1], postulates that the ancestors of all modern humans originated in East Africa and that, around 100,000 years ago, some modern humans left the African continent and subsequently colonised the entire world, displacing previously established human species such as Neanderthals in Europe 2., 3.. This scenario is supported by the observation that human populations from Africa are genetically the most diverse [2] and that the genetic diversity of non-African populations is negatively correlated with their genetic differentiation towards populations from Africa [3].     

The First Modern Human Dispersals across Africa

The emergence of more refined chronologies for climate change and archaeology in prehistoric Africa, and for the evolution of human mitochondrial DNA (mtDNA), now make it feasible to test more sophisticated models of early modern human dispersals suggested by mtDNA distributions. Here we have generated 42 novel whole-mtDNA genomes belonging to haplogroup L0, the most divergent clade in the maternal line of descent, and analysed them alongside the growing database of African lineages belonging to L0’s sister clade, L1’6. We propose that the last common ancestor of modern human mtDNAs (carried by “mitochondrial Eve”) possibly arose in central Africa ~180 ka, at a time of low population size. By ~130 ka two distinct groups of anatomically modern humans co-existed in Africa: broadly, the ancestors of many modern-day Khoe and San populations in the south and a second central/eastern African group that includes the ancestors of most extant worldwide populations. Early modern human dispersals correlate with climate changes, particularly the tropical African “megadroughts” of MIS 5 (marine isotope stage 5, 135–75 ka) which paradoxically may have facilitated expansions in central and eastern Africa, ultimately triggering the dispersal out of Africa of people carrying haplogroup L3 ~60 ka. Two south to east migrations are discernible within haplogroup LO. One, between 120 and 75 ka, represents the first unambiguous long-range modern human dispersal detected by mtDNA and might have allowed the dispersal of several markers of modernity. A second one, within the last 20 ka signalled by L0d, may have been responsible for the spread of southern click-consonant languages to eastern Africa, contrary to the view that these eastern examples constitute relicts of an ancient, much wider distribution.     

古DNA的新发现支持现代人东亚起源说

1983年,科学家们根据线粒体DNA（mtDNA）系统发育树构建了首个现代人起源的分子模型,认为现代人起源于亚洲,但1987年非洲起源说的提出取代了这一亚洲起源说。非洲起源说所依赖的无限多位点假说以及分子钟假说后来被普遍认为是错误的且不切实际的。我们近几年提出了一个新的分子进化模式,即遗传多样性上限理论,重新构建了一个新的人类起源模型。这一模型与多地区起源说基本吻合, 重新把现代人类起源地定位在了东亚。非洲说与东亚说在线粒体进化树上的主要区别是单倍型N和R的关系,非洲起源说认为N是R的祖先,东亚说则反之。本研究引用了已发表的古代人群mtDNA数据,重点分析了线粒体单倍群N和R的关系。结果显示,三个最古老的人类（一个距今45000年,其他两个约40000年）都属于单倍群R;在距今39500到30000年前的人类样本中,绝大部分属于单倍群R下游的亚单倍群U,只有两例为单倍群N（Oase1距今39500年,Salkhit距今34425年）。这两例所属单倍型位于单倍群N下游最基本的未分化亚型,不属于今天存在的任何N下游单倍型,所以可能靠近单倍群N的根部。这些古DNA数据揭示单倍群R比单倍群N古老大约5000年,进一步证实了亚洲起源说的正确性,非洲说的依据不足。