Iberomaurusian ancient mtDNA

This is an issue that has lingered for a long time in the online anthropology circles. Once upon a time (2005) there was online a presentation in which a good deal of mitochondrial DNA (HVS-I) sequences from the key Iberomaurusian (or Oranian) culture site of Taforalt (North Morocco) were (not too formally) published. Eventually this presentation became almost impossible to find... however now Rym Kefi (the original author if I remember correctly) and colleagues have got back to resurrect that important data set from oblivion, plus sequences from Afalou cave as well.

Rym Kefi et al., On the origin of Iberomaurusians: new data based on ancient mitochondrial DNA and phylogenetic analysis of Afalou and Taforalt populations. Forsenic Sciences Research 2016. Freely available at the time & space of writing this → LINK [doi:10.1080/24701394.2016.1258406]

Abstract

The Western North African population was characterized by the presence of Iberomaurusian civilization at the Epiplaeolithic period (around 20,000 years before present (YBP) to 10,000 YBP). The origin of this population is still not clear: they may come from Europe, Near East, sub-Saharan Africa or they could have evolved in situ in North Africa. With the aim to contribute to a better knowledge of the settlement of North Africa we analysed the mitochondrial DNA extracted from Iberomaurusian skeletons exhumed from the archaeological site of Afalou (AFA) (15,000–11,000 YBP) in Algeria and from the archaeological site of Taforalt (TAF) (23,000–10,800 YBP) in Morocco. Then, we carried out a phylogenetic analysis relating these Iberomaurusians to 61 current Mediterranean populations.

The genetic structure of TAF and AFA specimens contains only North African and Eurasian maternal lineages. These finding demonstrate the presence of these haplotypes in North Africa from at least 20,000 YBP. The very low contribution of a Sub-Saharan African haplotype in the Iberomaurusian samples is confirmed. We also highlighted the existence of genetic flows between Southern and Northern coast of the Mediterranean.

The bulk of the data is this (tables 1 and 2):

Notice that all sequences are "old style", i.e. HVS-I only, and that's why haplogroup assessment is not always 100% certain, with particular emphasis on the "CRS" sequences, which have been proven in some ancient cases to belong not to the modern normal (H1, rarely H2 o other H) but to a very rare modern haplotype within U*, AFAIK only preserved in Asturias but somewhat common in the Magdalenian of South Germany. 

In any case, that they produce 100% safe H1, H6, H14, etc. and, even more surprisingly, J and T2 variants, should make people think about the hidden Paleolithic mtDNA diversity in the wider Mediterranean area. And by this I do not just mean North Africa but also all Southern Europe, including many areas that can't be considered part of the Mediterranean basin, such as most of the crucial Franco-Cantabrian Region, the most densely populated province, by far, of post-LGM Upper Paleolithic Europe, source of several cultural waves (including the Solutrean one, almost certainly at the origin of Iberomaurusian), yet outrageously neglected by research.

Table 5 and other materials in the paper also deal with which modern populations appear closest to the Iberomaurusian ancient mtDNA pool and these are:

1. Tuscans (0.00090)
2. Catalans (0.00134)
3. Galicians (0.00223)
4. Sicilians (0.00377)
5. El Alia (0.00699)
6. Valencian (0.00787)
7. Matmata (0.00788)
8. Slougia (0.00831)
9. Jerba Berbers (0.00934)

Figures in brackets are FST distances, the smaller the closer the match, statistically speaking. Populations in cursive are from Northwest Africa.

That is I'd say quite surprising because we tend to think of those near matches as quite impacted by Neolithic and post-Neolithic inflows, at least judging on other recent research. It seems that the debate on the origin of modern Europeans and North Africans refuses to come to a close, as different aspects of the evidence available may be somewhat contradictory. What do you make up of all this?

See also:

• Leherensuge: 2009 review of mtDNA H studies (some re. North Africa).
• I'd emphasize Sykes et al 2005 on Portuguese Epipaleolithic and Neolithic mtDNA also rich on "CRS" and other H sequences, because it provides another anchor point for the presence of mtDNA H in pre-Neolithic Europe.
• But for North African mtDNA studies Enafaa 2009 is pretty much seminal, showing that SW Europe related haplogroups H1, H3, H4 and H7 are absolutely hegemonic in the region's H.
• MtDNA H in Magdalenian Cantabria
• MtDNA U6 in Aurignacian from Romania
• On South Iberian Solutrean (surely at the origin of Iberomaurusian)
• And in general the Oranian label (alternative name of Iberomaurusian)

UPDATE: single marker inferred lineages (not always the haplogroup is reported correctly):

Down in the comments' section, Capra questions with good sense the certainty of inferred haplogroups. The most clear one is TafV27, claimed to be H6a1a8, which cannot actually be that (would need another HVS-I marker defining H6, which is missing), however this means that it must be HV0 and possibly V, a lineage that appears (per the aDNA literature) in the European Neolithic, already quite towards the West, out of nowhere, and that "nowhere" should not be West Asia, where it has never been sequenced, unlike K. 

I'm therefore reviewing here all the single-marker inferred haplogroups as carefully as possible, please double-check them and report if I seem to be committing any error:

• AF22B - 16126C (reported as JT or H14b1) - JT(xJ,xT) or H14b1 indeed, notice that JT* was probably also one of the lineages described (also by the HVS-I method) for Nerja cave (Solutrean, same time frame), just across Alboran Sea (cf. Fernández-Domínguez 2005). Whether is one or the other or even something else, it's almost certain that the lineage was shared across the sea between Europe and Africa, what just makes total sense for this culture.
• Taf55-IB - 16239T (reported as H1) - I actually get specific H1 variants (H1bf'bg'bh'ch specifically) or H17c. H sublineages in any case, unless it is an extinct or unreported R* lineage, most unlikely.
• TafV27 - 16298C (reported as H6a1a8) - must be HV0, possibly even V, a distributed Euro-African lineage with three hotspots: Kabylia, Catalonia and Lappland. Per Caramelli 2003 and successor studies, this lineage was already present in Italy (Pagilicci cave) in the Gravettian era.
• TafVIII - 16223T (reported as U4a2b) - It cannot be U4 at all because it lacks the HVS-I mutation 16356C. In fact the reverse 16223C mutation defines macro-haplogroup R, and I can't find any other matches within R, so it must be L3(xR), maybe N(xR) but maybe M or other L3. The possibilities are many, for example: N1, N2, N9, N11, etc. within N, a lot of possibilities within M, and also several within L3e'i'k'x(xL3x). The only thing we should be certain here is that it is not R and also not upstream of L3 (that's how good as it gets with HVS-I methodology, really). 
• TafXXV3 - 16126C (reported as H14b1) - as with AF22B, it can be JT(xJ,xT) or H14b1 and again I must emphasize that there is an extremely good chance that this matrilineage had relatives in Iberia (Nerja) within the Solutrean culture.

In case you want to re-check, the best resource is of course PhyloTree.

IMPORTANT CAVEAT: the above update was done assuming they had fully sequenced the HVS-I, which is not that long, but it seems that in many cases (second column of the tables above) they have only sequenced up to the 16317 locus, what makes prediction of haplogroup even harder. That would explain their H6a1a8 prediction, although there's no way they can exclude the much more common HV0 (H6 is unheard of in North Africa). Thanks again to Capra for pointing that out.

MtDNA U6 in Aurignacian Europe

The U6 haplogroup of Pestera Muierii is officially confirmed. 

Extra-officially, it also seems confirmed mtDNA H in Magdalenian El Mirón, another of the haplogroup challenged (without any reasoning) by Fu et al. In this last case, my sources suggest that Fu surely tested a bone belonging to a different individual, because the heap of bones could well include several people and the bones tested by Hervella (a tooth) and Fu (a femur) were different.

Anyhow, to the matter at hand:

Montserrat Hervella et al. The mitogenome of a 35,000-year-old Homo sapiens from Europe supports a Palaeolithic back-migration to Africa. Nature 2016. Open access → LINK [doi:10.1038/srep25501]

Abstract

After the dispersal of modern humans (Homo sapiens) Out of Africa, hominins with a similar morphology to that of present-day humans initiated the gradual demographic expansion into Eurasia. The mitogenome (33-fold coverage) of the Peştera Muierii 1 individual (PM1) from Romania (35 ky cal BP) we present in this article corresponds fully to Homo sapiens, whilst exhibiting a mosaic of morphological features related to both modern humans and Neandertals. We have identified the PM1 mitogenome as a basal haplogroup U6*, not previously found in any ancient or present-day humans. The derived U6 haplotypes are predominantly found in present-day North-Western African populations. Concomitantly, those found in Europe have been attributed to recent gene-flow from North Africa. The presence of the basal haplogroup U6* in South East Europe (Romania) at 35 ky BP confirms a Eurasian origin of the U6 mitochondrial lineage. Consequently, we propose that the PM1 lineage is an offshoot to South East Europe that can be traced to the Early Upper Paleolithic back migration from Western Asia to North Africa, during which the U6 lineage diversified, until the emergence of the present-day U6 African lineages.

The interesting part is that today U6 is pretty much constrained to Northwest Africa and parts of Iberia and it has usually been considered until now as a North African haplogroup, even if of Eurasian derivation. 

Fig. 2 - (A) Phylogenetic analysis and temporal estimates for lineages including the Peştera Muierii-1 (PM1) from the mitochondrial tree. (B) Location of the Peştera Muierii cave and surface map based on current frequencies of U6 lineages³⁰; the European borders map was generated in ArcMap 10.1 (ESRI, http://www.esri.com) by modifying the World Borders Dataset (http://www.thematicmapping.org/downloads/world_borders.php), which is licensed under the Attribution-ShareAlike 3.0 Unported license. The license terms can be found on the following link: http://creativecommons.org/licenses/by-sa/3.0/ (This map was created by A.A.).

Another interesting bit is that U6(xU6a'b'd,U6c), U6* for short, is not known to exist today anymore. So it is reasonable to speculate about the "ancestral" position of Muierii in the lineage, regardless of whether Muierii-2 was a true ancestor or just a more or less distant relative of the real ancestor of modern day U6 carriers. 

Complementary information is to be found Secher et al. (2014), which refined the knowledge of the U6 mitochondrial haplogroup, unveiling that the key basal (and rare) U6c sublineage is not only found in Morocco (as known earlier) but also in Europe. Specifically U6c, which hangs directly from the U6 root node, is found in: Hispanic America (5.7% of all U6 carriers), Spain (2.2%), Canada (12.5%), NW Europe (16.7%), Morocco (4.5%), Algeria (10%) and Tunisia (5.9%). It is missing in Brazil, Western, Central and East Africa, Romani ("Gypsies"), Jews, Azores, Madeira, Canary and Cape Verde Islands, Portugal, Central and Eastern Mediterranean, West Sahara, Mauritania and USA (African-Americans,  European-Americans and Hispanics).

Figure 1

Surface maps, based on HVI frequencies (in o/oo), for total U6 (U6), total U6a (Tot U6a), U6a without 16189 (U6a), U6a with 16189 (U6a-189), U6b'd, U6c, U6b and U6d.

While the exact pattern of U6 expansion is not clear except for Africa (with a Moroccan origin surely), Sacher et al. believe that at least this part is related to the Iberomaurusian (aka Oranian) culture, which seems primarily an offshoot of Iberian Solutrean, also with origin in North Morocco (Taforalt) and European-like human looks (Cromagnoid).

Another complementary reference is Carmela L. Hernández et al. (2015):

An inspection of the U6 phylogenetic tree (S1 Dataset) showed that it is not easy to infer whether Iberia or North Africa bear more basal lineages. (...) The U6c (9.9 ky [5.0–15.0]) and U6d (12.0 ky [6.9–17.3]) are present in Iberia, Europe and North Africa at low frequencies.

While she seems to support a North African origin, the data is in fact somewhat contradictory:

Fig 5. Founder analysis for mtDNA U6 haplogroup. The plots show probabilistic distributions of U6 founder clusters for HVS-I sequences (A) and complete genomes (B) across migration times scanned at 200-year intervals from 0 to 60 ky.

Fig 7. Bayesian Skyline Plot (BSP) analysis of entire mtDNA U6 sequences.

Temporal changes of the effective population size, Ne in sub-Saharan Africa (brown color), North Africa (green color), and Iberian Peninsula (red color) are depicted. Solid lines represent the median values for the log10 of Ne on the Y-axis within each analyzed geographic region. The 95% HPD (highest posterior density) interval is shown for the three distributions (dashed lines).
Notice that the "LGM" label is very wrong: it should be around 21.000 years ago!

Usually U6 genetic history is envisioned as a migration from southwest Asia through North Africa [50]. This hypothesis is based on the general origin of haplogroup U sub-clades in Southwest Asia, which is also the center of the geographical distribution of U sub-clades: Europe, India, Central Asia, East Africa and North Africa. Two possible scenarios for the first U6 haplotype (bearing mutations 3348 and 16172) can be advanced: i) these mutations aroused in the founder region but did not leave any genetic legacy in current human populations there; ii) they originated probably somewhere in North Africa, after the arrival of the U6 founder haplotype. Within North Africa U6 is only significantly frequent at its western edge (as well as in South-western Europe). More importantly, all the most basal branches are virtually restricted to that region (U6b, U6c and U6d), what could indicate its western origin. Nevertheless, it cannot be excluded the major sub-clade U6a, which shows a richness of sub-clades in Northwest Africa [29] although a few of derivative branches also include sequences from East African and the Middle Eastern populations (e.g. U6a2).

Her conclusions (insisting on an African origin and first arrival via Egypt) are not something I can share at this stage of the research but her data is clearly very interesting and, combined with the rest, useful in discerning the possible route of primeval U6 to the Gibraltar Strait area, where it found no doubt its niche for consolidated expansion. 

After the Muierii finding the question is open: did primeval U6 arrive to North Africa via Iberia, being pruned in Europe afterwards just because of genetic drift and the sizable impact of Paleolithic migrations in low density areas? I cannot be 100% sure but I would say it is a very likely conclusion based not just on Muierii but also on the rather high basal diversity of U6 in Iberia (and surprisingly NW Europe!) and also on the archaeological data that makes almost necessary to root the first Upper Paleolithic of NW Africa (the Iberomaurusian) in the Iberian Solutrean.


(Special thanks to Jean Lohizun again).


Update (Jun 17):

The Hernández 2015 paper also mentions that  U6a1 appears to be of European and specifically Portuguese origin:

Our U6 tree built from mitogenomes shows that U6a1 is predominantly European because it contains a significant number of sequences of Mediterranean individuals mainly from the northwestern shore with a leading Iberian contribution (21 of the 29 European samples) and has an ancestral node in Portugal (accession number HQ651694).

Thanks to Geog M. for highlighting this important detail.

A genetic legacy of North Africa: mtDNA U6 under the microscope

An excellent new study on mtDNA haplogroup U6 has been published this week:

Bernard Sechel et al., The history of the North African mitochondrial DNA haplogroup U6 gene flow into the African, Eurasian and American continents. BMC Evolutionary Biology 2014. Open access → LINK [doi:10.1186/1471-2148-14-109]

Abstract (provisional)

Background

Complete mitochondrial DNA (mtDNA) genome analyses have greatly improved the phylogeny and phylogeography of human mtDNA. Human mitochondrial DNA haplogroup U6 has been considered as a molecular signal of a Paleolithic return to North Africa of modern humans from southwestern Asia.

Results

Using 230 complete sequences we have refined the U6 phylogeny, and improved the phylogeographic information by the analysis of 761 partial sequences. This approach provides chronological limits for its arrival to Africa, followed by its spreads there according to climatic fluctuations, and its secondary prehistoric and historic migrations out of Africa colonizing Europe, the Canary Islands and the American Continent.

Conclusions

The U6 expansions and contractions inside Africa faithfully reflect the climatic fluctuations that occurred in this Continent affecting also the Canary Islands. Mediterranean contacts drove these lineages to Europe, at least since the Neolithic. In turn, the European colonization brought different U6 lineages throughout the American Continent leaving the specific sign of the colonizers origin.

Figure 1 Surface maps, based on HVI frequencies (in o/oo), for total U6 (U6), total U6a
(Tot U6a), U6a without 16189 (U6a), U6a with 16189 (U6a-189), U6b'd, U6c, U6b and U6d.

U6 can be considered a somewhat strange haplogroup. While it is derived from U (and hence from R and N), which has an Asian origin, it seems to have expanded from NW Africa, more specifically from the Northern mountainous areas of the Moroccan state, a country known as Rif or in the native Tamazigh language Arif (of which Rif is an Arabized version), not the usual place one tends to imagine as the origin of any human expansion wave. 

Actually there is at least one important cultural expansion from that area: the Oranian or Iberomaurusian culture of the Mid-to-Late Upper Paleolithic. To some extent at least the expansion of this lineage is probably associated to this ancient culture. 

Whatever the case, U6 is not a common haplogroup: its highest peak in frequency is in the Canary Islands (16%), followed by North-West Africa (5-9%). Then come Portugal and its insular colonies, as well as Cape Verde and Ethiopia (~3%) and then there is some scatter in Spain, West Africa, NE Africa and peninsular Arabia (~1%), as well as in some other parts of Europe, Africa and West Asia (<1%). 

On the other hand it is one of the four basal branches of the major West Eurasian haplogroup U (U5 and U2'3'4'7'8'9 are more common, while U1 is even rarer and less studied), so understanding U6 seems important to better understand its parent lineage. 

Therefore this new study with its great wealth of detail and care is much welcome.

Chronological estimates and expansion patterns of U6

It may surprise you that I am even in tentative agreement with the chronological estimates for U6 and its subclades, listed in tables 2 and 3. But it is for a good reason: they make sense (assuming a reasonable CI). And the fact that they seem to make sense is probably because the authors took great care to calibrate the ages for this lineage, using as main (but not only) reference a Canadian derived lineage that seems to be a colonial founder effect. 

Anyhow all these dates should be considered as center-points of a variably wider range of possibilities, the so-called confidence interval (CI) or error margin (em). If we do that, as we should, we get the "power" to stretch the figures forth and back as need be to some extent without losing consistency, and that alone should be enough to get the estimates fit better with the material evidence (archaeology mostly). 

The authors actually mention some of those CIs in a lengthy section dedicated to explore the possible patterns of U6 spread in Africa and elsewhere.

Interestingly they suggest that the first radiation of U6 took place from NW Africa in largely eastwards direction, belonging almost necessarily to the Iberomaurusian (Oranian) culture:

This first African expansion of U6a in the Maghreb was suggested in a previous analysis [6]. This radiation inside Africa occurred in Morocco around 26 kya (Table 2) and, ruling out the earlier Aterian, we suggested the Iberomaurusian as the most probable archaeological and anthropological correlate of this spread in the Maghreb [6]. Others have pointed to the Dabban industry in North Africa and its supposed source in the Levant, the Ahmarian, as the archaeological footprints of U6 coming back to Africa [7,9]. However, we disagree for several reasons: firstly, they most probably evolved in situ from previous cultures, not being intrusive in their respective areas [42-44]; second, their chronologies are out of phase with U6 and third, Dabban is a local industry in Cyrenaica not showing the whole coastal expansion of U6. In addition, recent archaeological evidence, based on securely dated layers, also points to the Maghreb as the place with the oldest implantation of the Iberomaurusian culture [45], which is coincidental with the U6 radiation from this region proposed in this and previous studies [6].

Some millennia later, U62 appears to expand in Ethiopia, while, as mentioned, U6a1 does the same in Europe (mostly Western Iberia) and other sister lineages do the same in NW Africa itself.

A second wave of radiation corresponds to the early Holocene:

Basic clusters like U6b, U6c and U6d also emerged within a window between 13 to 10 kya (Table 2). U6b lineages spread from the Maghreb, through the Sahel, to West Africa and the Canary Islands (U6b1a), and are also present from the Sudan to Arabia, but not detected in Ethiopia. In contrast, U6c and U6d are more localized in the Maghreb. Further spreads of secondary U6a branches are also apparent, going southwards to Sahel countries and  reaching West Africa (U6a5a). Autochthonous clusters in sub-Saharan Africa first appeared at around 7 kya (U6a5b), coinciding with a period of gradual desiccation that would have obliged pastoralists to abandon many desert areas [52]. Consequently, no more U6 lineages in the Sahel are detected, while later expansions continued in West Africa (U6a3f, U6a3c, and U6b3) and the Maghreb with an additional spread to the Mediterranean shores of Europe involving U6b2, U6a3e, U6a1b and U6a3b1.

For easier understanding of the U6 phylogeny and its sometimes hard to interpret migration patterns, I made up the following graph, based on the supplemental material of this study:

U6 phylogeny, color coded by regions:

• North Africa
• Europe
• Tropical Africa
• West Asia
• intermediate colors: equal weight between two regions, black: undecided
• italic type: unnamed lineages

I must say that, I have some doubts about the exact origins of several subhaplogroups, notably:

• U6a is so diverse in some branches that it is difficult to identify it as unmistakably of NW African origin. NW Africa still gets the greatest weight (3/7) but not a clear majority.
• In U6b Tropical African lineages weight 4.5/10, while NW African ones weight only 3/10. It is a good candidate for expansion from the "Wet Sahara" indeed.
• In U6c1 European and NW African lineages weight exactly the same, although I guess that it may be reasonable to imagine Andalusian U6c1c as derived from North Africa.

However overall U6, as well as its derived lineages U6b'd and U6c clearly originated in NW Africa, so I understand that, when unclear, NW Africa gets the benefit of doubt for the derived origins.

Hunter-gatherers, acorns and tooth trouble

It has been commonplace to believe that hunter-gatherers had good tooth health and that it was farming what caused dental problems because as cereals became a staple. There was good reason for that: caries were detected only rarely among hunter-gatherer remains (0-14%) while early farmers had much such painful problems much more frequently.

However the Upper Paleolithic people of Taforalt caves (Rif, North Africa), some 14,000 years ago (Oranian culture), had caries in 51% of adult teeth, a frequency comparable to those of early farmers.

This is attributed to the very high levels of nut consumptions, particularly acorns but also pine nuts, juniper berries, pistachios and wild oats. The number of acorn remains found is so large that the archaeologists had to conclude that they were used as year-long staple.

Late Upper Paleolithic of North Africa
· Iberomaurusian, aka Oranian, is shaded in dark green ·
· The core area of Capsian is shaded in gray-blue ·
(credit: Locutus Borg (anticopyright))

Taforalt people had hand mills, which they used to process some of these nuts, most likely the acorns, whose consumption as bread has been documented since antiquity.

Another finding are esparto grasses, which the authors believe were used in basketry. However I must mention that this versatile fiber has known many uses, being documented in Neolithic clothing of nearby Andalusia, used for some types of shoes even today and, of course, being a prime material for rope-making.

Esparto bale

Oranian culture dates to c. 22,000 years ago, with likely (partial?) roots in the Southern Iberian Gravetto-Solutrean (hence the name Iberomaurusian, although the culture as such is not known in Iberia). It was replaced in the Epipaleolithic by Capsian culture, with ultimate roots at the Nile (and hence the most likely vector of Afroasiatic languages leading to Tamazigh, aka Berber).

Source: PhysOrg.

Ref. Louise T. Humphrey et al., Earliest evidence for caries and exploitation of starchy plant foods in Pleistocene hunter-gatherers from Morocco. PNAS 2013 (pay per view, free after 6 months) → LINK [doi: 10.1073/pnas.1318176111]