Neanderthals and humans interbred in Europe for 5,400 years

C1 haplogroup in America

The Native American people belong to five mtDNA haplogroups, which are almost exclusive to America (there have been some minor back-migrations from America into Asia): A2, B2, C1, D1 and X2a. Of these, haplogroup C1 is widespread across the Americas, from Tierra del Fuego to central northern Canada (it is absent among the Innuit in northernomost Canada and Alaska).



C1 hg has in mutated in America and originated four subclades (C1a, C1b, C1c and C1d), of which C1b to C1d are found exclusively in America, and C1a is found in Asia where it back-migrated from the New World. These subclades, in turn have branched into other sublineages.

mtDNA C1 haplogroup in Iceland

A Thesis written in 2010 (Sigríður Sunna Ebenesersdóttir) [5], followed by a paper (Sigríður Sunna Ebenesersdóttir et al., 2011) [2] disclosed the presence of a novel C1 haplogroup in Iceland; it was named C1e.



It is not the result of recent gene flow from Native Americans or Asians. [2][5] It does not belong to any of the four known Native American (C1b, C1c, and C1d) or Asian (C1a) subclades of haplogroup C1. [2] The Viking settlers in Iceland had brief and bellicose contact with the Native Americans but could have kidnapped women and taken them to Iceland thus originating the local haplogroup C mtDNA lineage, but the differences between Amerindian C1 lineages and the Icelandic one are considerable. Since Aleut, Inuit and Eskimos are not carriers of C1 hg, they are not the vector. [2] C1 is quite infrequent among the North American Na-Dene speaking Native-Americans (Apache, Navajo, Haida and Tlingit). [2] Amerindian haplotypes are very rare in post 1492 Europe, suggesting limited Euro-Amerindian admixture. [2] It is found at very low frequencies in Iceland: about 0.3 %

An Eurasian origin for Iceandic C1e

The likely source arrived in Iceland with the original Viking settlers ca. 900 CE; since these were Europeans, it is possible "that C1e is a very rare European branch". [2] This is corroborated with another line of evidence: "one of the thirteen HVS1 sequences that potentially belong to sub-clade C1e was found in Germany" [2] and that the female settlers brought by the Scandinavian men were women from the British Isles and as "the vast majority of mtDNA lineages observed in contemporary Icelanders are descended from the original set of mtDNA lineages present in the female settlers" [2], this haplogroup was surely present in the Xth century Great Britain.

mtDNA C1 haplogroup in Northern Europe



Only recently was the C1 hg found in the remains of a prehistoric North European (Clio Der Sarkissian et al., 2014) [6], reinforcing the theory of a European source for the Icelandic haplotype. But, surprisingly, it belongs to yet another distinct clade, named C1f, distinct from all other haplotypes. It was detected in the remains of three individuals retrieved from a Mesolithic site in North Western Russia, on the Kola Peninsula, at the Yuzhnyy Oleni Ostrov site. This places C1f in Europe 7,500 years ago. But, it has not been detected in current population mtDNA data-bases.

The apparent absence in modern populations may be due to its extinction and replacement by other mtDNA haplogroups introduced by more recent migrations into Europe or a very low frequency among contemporary Europeans leading to its non-detection in the samplings that have been made. Though C1f has not been found, "HVR-I diversity has revealed extremely low frequencies of hg C1, with very few haplotypes found in Germans, Canarians, Icelanders and Bashkirs. These sequences lack HVR-I Single Nucleotide Polymorphisms (SNPs) diagnostic of the sub-clades C1a (T16356C) and C1d (A16051G)." [6] Meaning that they do not belong to the current East Asian or Amerindian groups (C1a and C1d Hg.)



Let's look a the C1f from the Yuzhnyy Oleni Ostrov site. Did they arrive via the invasions of Asian hordes? (we have already seen this hypothesis when we analyzed the Y chromosome Q haplogroup in Europe): Mongols, Huns, Cimmerians (100 BCE to 1,295 CE). It seems unlikely because "the common Asian C1a clade is characterised by the HVR-I transition T16356C, which has not been found in any European C1 haplotype" [6].

The age of these remains (7,500 ya) means that they could not have arisen from European - Native American admixture post-discovery of America in 1492. This clade is definitively an Old World one. This leaves us with only one option: C1f is very old and has been in Europe at least since Mesolithic times. Its age and location could imply that it is ancestral to the C1e taken by the Vikings (actually by the British women they wed) to Iceland. It also means that C1f and C1a (the East Asian) branches split long ago from the C1 tree, evolving along separate routes. [6] This is shown in the map above where C1f splits from the one leading into America (C1b, C1c, C1d) in Central Asia, and C1a is a back flow from the New World. The pale blue area is the possible range once occupied by the primitive basal C1 root in Eurasia, which later disappeared.

As mentioned above, it has not found in the modern populations in Europe or Asia where it may still exist but has not yet been detected in genetic samplings of the populations. In depth and large scale samples may be required to find it because its originally low frequency may have been further diluted it making it even more uncommon now than it was in the recent past. To get an idea of its rarity, C1 has appeared only once in Germany, and its presence in Siberia is very low (4 individuals among 1,432 tested) [9]. Interestingly, "The Baltic coast of Europe and Poland also contains a unique C lineage, which may have expanded north from the Black Sea" [9], unfortunately no details are given about it.



The other Mesolithic remains that have been sequenced in Europe did not yield any C1 haplogroup samples [6], this means that even at that time it was quite rare or restricted to certain geographical locations, perhaps as part of relict groups of Paleolithic populations. And this brings us to... yes! the Neanderthals. Europe and Central Asia, Western Siberia were the homeland of Neanderthals for hundreds of thousands of years. The Amerindians carry the highest proportion of Neanderthal ancestry suggesting an intimate admixture with them in the New World. The region covered by C1 haplotypes coincides with the range of the Neanderthal people. They were later incorporated by cross-breeding into the modern humans that left Africa 70 kya, this effectively eliminated them by absorption.

But, for this to be true, C1 would have to be a Neanderthal mtDNA haplogroup, and we know (mainstream version) that this is not possible because Neanderthal mtDNA that we have sequenced is too different from ours, furthermore, it would lie on separate branches of the tree, not in one that sprouts from the first modern humans in Africa.

Sources

[1] Satish Kumar et al., (2011), Large scale mitochondrial sequencing in Mexican Americans suggests a reappraisal of Native American origins. BMC Evolutionary Biology 2011, 11:293
[2] Sigríður Sunna Ebenesersdóttir et al., (2011). A new subclade of mtDNA haplogroup C1 found in icelanders: Evidence of pre-columbian contact?. Am. J. Phys. Anthropol., 144: 92–99. doi: 10.1002/ajpa.21419
[3] Simon Y.W. Ho and Phillip Endicott, Letter. The Crucial Role of Calibration in Molecular Date Estimates for the Peopling of the Americas. The American Journal of Human Genetics 83, 127–147, July 2008 pp. 142
[4] Fagundes, N.J., et al., (2008). Mitochondrial population genomics supports a single pre-Clovis origin with a coastal route for the peopling of the Americas. Am. J. Hum. Genet. 82, 583–592.
[5] Sigríður Sunna Ebenesersdóttir (2010). Faculty of Social Science. MA-thesis, Anthropology. The origin of Icelandic mtDNA lineages from haplogroup C
[6] Clio Der Sarkissian et al., (2014). Mitochondrial Genome Sequencing in Mesolithic North East Europe Unearths a New Sub-Clade within the Broadly Distributed Human Haplogroup C1. PLoS One. 2014; 9(2): e87612. Feb 4, 2014. doi: 10.1371/journal.pone.0087612
[7] Tamm E, Kivisild T, Reidla M, Metspalu M, Smith DG, et al., (2007). Beringian Standstill and Spread of Native American Founders. PLoS ONE 2(9): e829. doi:10.1371/journal.pone.0000829
[8] Derenko M, Malyarchuk B, Grzybowski T, Denisova G, Rogalla U, et al., (2010). Origin and Post-Glacial Dispersal of Mitochondrial DNA Haplogroups C and D in Northern Asia. PLoS ONE 5(12): e15214. doi:10.1371/journal.pone.0015214
[9] Jeremy R. Newton, (2011). Ancient Mitochondrial DNA From Pre-historic Southeastern Europe: The Presence of East Eurasian Haplogroups Provides Evidence of Interactions with South Siberians Across the Central Asian Steppe Belt. Master Thesis Paper 5.

We conclude that all the “archaeology-based” explanations for the demise of the Neandertals reviewed here (Table 1, Text S1, Hypotheses 1–11) are flawed. They were based on much less data than we have available today and were at least in part the result of a long tradition of thinking in terms of Neandertals-AMH dichotomies, steered by overstressing developments within the Upper Paleolithic of Europe, the record of which has become almost like a yardstick for modern human behavior (Text S2).



While the debate about AMH dispersal times and routes out of Africa is intense, based on a range of archaeological as well as genetic data, the archaeological record from the various continents does not provide strong support for any of the suggested routes nor any of the suggested factors in the demise of the Neandertals. The very fact that the migration time estimates vary so widely suggests that we simply have no solid data; perhaps there was more than one migration event (in addition to the Last Interglacial limited expansion in the Levant), and in all probability the migrating groups did not have a strong cultural homogeneity. This may explain why we do not see clear archaeological signatures for AMH on the move.

Interestingly, the widely accepted date of 60 or 50 ka for the modern human expansion into Eurasia (following the earlier short-lived exodus in the Levant documented at Skuhl and Qafzeh) would rule out South Africa as the location for source populations for two reasons: (i) by 60 ka the HP tradition of backed tools made on blades and bladelets produced by soft stone hammer (supposedly associated with the AMH expansion) had given way to the post-HP assemblages characterized by a variety of flake tools and blades produced by hard hammer percussion but without backed blades [94], [103], [105], [116]; (ii) the Still Bay and HP populations were not larger than other MSA populations and might even have been smaller, thus excluding population pressure as the prime mover of the migration [117]. According to Klein [11] the Out of Africa expansion was underlain by a neural mutation that promoted the final development of the modern human brain. Direct evidence for this hypothesis may come from comparisons of Neandertal and modern human genomes.



In the recent past, much debate has been generated from the observation that Neandertals began to produce a richer archaeological record, including bone tools, personal ornaments and use of manganese and ochre, at the time when AMH started colonizing Europe. Some interpreted this change in the record as the result of Neandertal absorption of ideas and techniques from the incoming AMH. After having produced a rather monotonous record for almost 300,000 years, an independent invention of these new items just at the time of the arrival of AMH would have to be seen as an “impossible coincidence” [28]. However, as reviewed here, use of ochre, of personal ornaments, production of specialized bone tools and complex hafting techniques were part of the Neandertal repertoire already before the arrival of AMH in western Eurasia.

The present review also suggests that some of the innovative technologies of the Protoaurignacian and of the Aurignacian may have developed out of a Middle Paleolithic base (for a similar viewpoint, see [118]). Some components that occur sporadically or episodically in Neandertal and late MSA assemblages become much more common later, like pigment use, symbolic objects, extensive transport of raw materials and even specialized bone tools [79]. The same goes for another element, the intentional production of bladelets (<4 cm in length) from bladelet cores. Bladelets have been considered a discriminant factor between the Upper and Middle Paleolithic and therefore between AMH and Neandertals [119]. Production of bladelets has been securely identified in French Mousterian assemblages, e.g. at Combe Grenal (layers 30–29 and layers 16 and 14), Champ Grand and Grotte Mandrin, and in Spain at sites such as El Castillo and Cueva Morin [120], [121]. All these assemblages belong to the final Mousterian, with the exception of Combe Grenal and Grotte Mandrin; at the latter site, a layer with blades, bladelets and microlithic points is overlain by five layers with flake-based Mousterian assemblages [121]. At Combe Grenal layers 29–30 have an estimated age of late MIS 4, i.e. around 60 ka. Bladelets and bladelet cores are not abundant (5% of the assemblage at Combe Grenal layers 29–30), yet they show that Neandertals, like late MSA humans and the makers of the Protoaurignacian, mastered the technology of bladelet production, albeit using methods different from the HP small blade technology. It is their frequency, not cognition or technical competence, that distinguishes AMH bladelet production from that of Neandertals [120]. The techniques and methods of bladelet making in the Mousterian are different from those of the Protoaurignacian, just as the kind of possible symbolic objects are also different (use of raptor claws; on perforated or grooved animal teeth (see Text SI, Hypothesis 1). Perhaps the nature of the contacts should be seen in terms of diffusion of ideas rather than as face to face interaction and the copying of specific objects [122]. The occurrence of Dufour bladelets (often used as projectile elements in the Aurignacian and the Protoaurignacian) with very specific techniques of manufacture in the Châtelperronian of Quincay is interpreted in a similar way, as a form of low-degree social interaction between Neandertals and modern humans [123].



The Date of the Demise

Various new dates support the idea of some chronological overlap between AMH and Neandertals, which may have enabled interbreeding and cultural interaction in western Europe: AMS dates on ultrafiltered bone collagen from the Châtelperronian layers X and IX of Grotte du Renne at Arcy, c. 44 to 41 kyr cal BP; the date of the Saint-Césaire Neandertal at 41.9−40.6 kyr cal BP [63]; the fact that the Protoaurignacian at the Italian sites of Castelcivita and Serino is overlain by the Campanian Ignimbrite tephra, dated to 39.28±0.11 ka by 40Ar/39Ar [124]; the modeled age ranges of c. 41.5−39.9 kyr cal BP of several radiocarbon-dated Proto-Aurignacian sites [95]; the date of the Oase 2 early modern cranium at c. 40 ka [125]; the AMS dates for the Neandertal child from Spy cave (Belgium), 36,870 to 38,494 and 37,297 to 40,490 cal BP [126]; the AMS dates for the Vindija (Croatia) Neandertal remains at c. 38 kyr cal BP [127], [128]; the 37.4 ka cal BP date for the final Mousterian level of Cueva Antón in southeastern Spain [75]. Even if we do not consider dates judged by some as controversial such as (i) the AMS dates on shell beads for the layer containing the modern human teeth at Grotta del Cavallo at 45.010−43,380 cal BP [5, contra 2]; (ii) the dates for the Kent’s Cavern modern human maxilla [3, contra 2, 129]; and (iii) the dates for the Aurignacian at Geissenklösterle at c. 42 kyr cal BP [4, contra 2], some millennia of overlap are indicated The latest Neandertal currently known from the Levant is the adult male skeleton from Amud Cave (Israel) with an ESR date of 53±8 ka on tooth enamel [130].

Interbreeding and Assimilation

For some authors replacement and supposedly rapid extinction of Neandertals can be explained only in terms of substantial cognitive, technological and demographic differences between the Neandertals and AMH [42], [131]. But, as we tried to show here, the Neandertal archaeological record was not different enough to explain their demise in terms of inferiority in archaeologically visible domains. Thus, if Neandertals were not technologically and cognitively “disadvantaged”, how can we explain that they did not survive?



Some modern human-like anatomical characteristics are said to occur in late Neandertal fossils (as in the Vindja, St. Césaire and Riparo Mezzena late Neandertals [132], [133] and refs therein) and vice versa some Neandertal features are present in early specimens of modern humans in Europe [134], [135] supporting a hypothesis of some degree of admixture between the two groups. However, until recently the morphological evidence of admixture was often dismissed. In 2010 a draft sequence of the Neandertal nuclear DNA provided clear evidence of interbreeding between Neandertals and modern humans [48], estimating that Neandertal inheritance makes up 1–4% of the genomes of people outside of Africa. A revised estimate based on a high-coverage sequence of a Neandertal from the Altai Mountains now suggests 1.5–2.1% [49]. Genes of Neandertals may have been favored through natural selection, and possibly played a role in the development of the immune system of modern humans [136] or in UV-light adaptations [137]. According to [138] gene flow from Neandertals to modern humans occurred between 47,000 and 65,000 years ago, and most likely happened at the time when Neandertals and modern humans encountered each other in Europe and the Middle East around 50,000 years ago.

In sum, interbreeding and assimilation, the tenants of a model first proposed by Fred Smith [139] are now supported by genetic data [134], [140]. It can be argued that the level of interbreeding may have been too limited to support an assimilation scenario. An interestingly parallel to this complex situation can be found in another “revolution”, the so-called Neolithic Revolution [43], [141], which does not feature explanations in terms of “cognitive” differences. The first farmers swept into Europe from the Near East at about 7500y BP displacing the local Late Mesolithic hunter-gatherers. But the Mesolithic hunter-gatherers, who cannot be described as cognitively inferior, were not submerged by hordes of farmers. Farmers and foragers coexisted for thousands of years in NW Europe; in Central Europe local hunter-gatherers adopted farming but in southern Scandinavia local foragers retained the Mesolithic lifestyle for c. 1500 years after farming arrived in Central Europe [142], [143]. Cultural contact is suggested by clear continuities in flint technology between the Mesolithic and early Neolithic in the region. After a very complex pattern of expansions and genetic shifts of the last 8,000 years the hunter-gatherer mitochondrial DNA haplogroups form 16% of the present-day Central European genetic composition [143]. It would take at least one millennium between the first arrival of immigrants and a notable increase in their population size.



The original Neandertal contribution to modern human biology may have been larger 40,000 years ago - equivalent to 2000 generations (with generation time at 20 years) – than estimates based on genomic regions of present-day humans suggest [144], [145]. Interbreeding of Neandertals and modern humans may have helped modern humans to adapt to non-African environments but also introduced alleles that were not tolerated and contributed to male hybrid sterility thus reducing the proportion of Neandertal ancestry of the period of contact to that seen today [144].

Mitochondrial genetic diversity of eight early modern European humans dated to ca 38,000 to 4,500 (14C cal BP, from Kostienki 14 to Őtzi The Iceman) is 1.5 times higher than that of five European Neandertals spanning the time to 38 to 70 ka [23], [146]. The high coverage genome of the Altai Neandertal [49] also suggests low genetic diversity which could indicate small population sizes (see Text S1 Hypothesis 8 for archaeological data). These genetic data suggest that differences in population sizes between the “resident” Neandertals and incoming AMH populations may have been a contributing factor in the absorption of Neandertal populations [23]. The momentous cultural changes that followed the arrival of AMH in Western Eurasia were not uniquely due to the residents’ cognitive or technological inferiority causing rapid and total replacement. The Neandertal demise appears to have resulted from a complex and protracted process [147] including multiple dynamic factors such as low population density, interbreeding with some cultural contact, possible male hybrid sterility and contraction in geographic distribution [148] followed by genetic swamping and assimilation by the increasing numbers of modern immigrants.



Conclusion

In a review of the MSA and Middle Paleolithic archaeological record we have shown that inferred markers of modern human cognitive and behavioral capacities have a greater time depth in the Middle Palaeolithic record than commonly acknowledged. We have found no data in support of the supposed technological, social and cognitive inferiority of Neandertals compared to their AMH contemporaries. The results of our study imply that single-factor explanations for the disappearance of the Neandertals are not warranted any more, and that their demise was clearly more complex than many archaeology-based scenarios of “cognitive inferiority” reviewed here seem to suggest. This has implications beyond the field of archaeology per se: archaeologists’ characterizations of Neandertals as cognitively inferior to modern humans [149] have created an interpretive framework within which subtle biological differences between Neandertals and modern humans tend to be overinterpreted (see for instance [150].

After 40,000 years and 2000 generations the Neandertal fraction in non-African modern human genomes still constitutes a substantial legacy from these ancient hominins who differed from contemporary AMHs in both geno- and phenotypes [151] but whose archeological record was not different enough to support the purported cognitive “gap” between them and their contemporary modern humans.

Villa, Paola, and Wil Roebroeks. "Neandertal Demise: An Archaeological Analysis of the Modern Human Superiority Complex." PloS one 9.4 (2014): e96424.