Sima de los Huesos hominins: ~430 thousand years old and on the Neandertal lineage

Science 20 June 2014: Vol. 344 no. 6190 pp. 1358-1363 DOI: 10.1126/science.1253958

Neandertal roots: Cranial and chronological evidence from Sima de los Huesos

J. L. Arsuaga et al.

Seventeen Middle Pleistocene crania from the Sima de los Huesos site (Atapuerca, Spain) are analyzed, including seven new specimens. This sample makes it possible to thoroughly characterize a Middle Pleistocene hominin paleodeme and to address hypotheses about the origin and evolution of the Neandertals. Using a variety of techniques, the hominin-bearing layer could be reassigned to a period around 430,000 years ago. The sample shows a consistent morphological pattern with derived Neandertal features present in the face and anterior vault, many of which are related to the masticatory apparatus. This suggests that facial modification was the first step in the evolution of the Neandertal lineage, pointing to a mosaic pattern of evolution, with different anatomical and functional modules evolving at different rates.

Link

400 thousand year old human mtDNA from Sima de los Huesos

It will come to no surprise to people who noticed an earlier paper on cave bear mtDNA from Atapuerca that the folks at the Max Planck Institute would try to do the same for the plentiful human remains found in the Pit of Bones.

A new paper in Nature reports their success, and overnight increases by an order of magnitude the time depth for which we now have human mtDNA from what is commonly designated as Homo heidelbergensis, from right in the middle of the Middle Pleistocene. Obviously, this opens new vistas for archaeogenetic research, making it possible to directly look at early pre-sapiens forms of humans, and not only on their final forms prior to their replacement, the Neandertals and Denisovans.

The most impressive aspect of the new paper is most likely the technical challenges that the researchers must've overcome to achieve this result. The cave bear DNA showed that this was possible, but human DNA adds an additional complication in the form of contamination by a closely related species, us.

But, the new evolutionary result which will interest those of us not interested in the minutiae of biomolecules will no doubt be the fact that the Sima hominin's mtDNA formed a clade with the much more recent Denisova girl.

Until now, we knew that Neandertal mtDNA grouped together and so did modern human mtDNA. The two groups shared a Middle Pleistocene common ancestor and a much more distant common ancestor (~1 million years) with the mtDNA found in Denisova. The new Sima specimen shares descent from Denisova. This is important because it shows that whatever archaic human population the Denisovan mtDNA belonged to also extended to western Europe. And, surprisingly, the Sima specimen did not group with Neandertals, as might be expected because of the incipient Neanderthaloid morphology of the Sima hominins which has been a matter of controversy as it pushes back the evolutionary lineage of H. neandertalensis deeper into the Middle Pleistocene that some researchers accept.

Before this paper, it was believed that H. heidelbergensis evolved somewhere (perhaps Near East or Africa), a subset of it evolved to H. sapiens in Africa, and a different subset evolved in Eurasia, leading up to H. neandertalensis in the west, and unknown forms in the east, of which the Denisova girl was a matrilineal descendant. The next question is: when did Neandertals and Neandertal mtDNA appear in Europe? 

It can now be hoped that such questions will be answered directly. The Sima individual studied in this paper is not some frozen specimen from the Arctic, preserved by a freak accident in pristine form for hundreds of thousands of years, but a person who lived in Southwestern Europe. I am fairly sure that this won't be the last really old human we see a paper about in the coming years. Human mtDNA used to present a simple picture at the time of the discovery of African mitochondrial Eve: the deepest splits were in Africa and Eurasians belonged to a subset of African variation. But, as more and more archaic Eurasian mtDNA is sampled, it now appears that modern human mtDNA is a subset of world human mtDNA whose deepest splits are in Eurasia, and the next deepest splits are in Africa. Obviously, this may be a consequence of the fact that archaic human mtDNA has only been sampled from Eurasia, for factors relating to DNA preservation. But, it is nonetheless interesting to wonder where on the tree the mtDNA of archaic Africans would fall.

Nature (2013) doi:10.1038/nature12788

A mitochondrial genome sequence of a hominin from Sima de los Huesos

Matthias Meyer et al.

Excavations of a complex of caves in the Sierra de Atapuerca in northern Spain have unearthed hominin fossils that range in age from the early Pleistocene to the Holocene1. One of these sites, the ‘Sima de los Huesos’ (‘pit of bones’), has yielded the world’s largest assemblage of Middle Pleistocene hominin fossils2, 3, consisting of at least 28 individuals4 dated to over 300,000 years ago5. The skeletal remains share a number of morphological features with fossils classified as Homo heidelbergensis and also display distinct Neanderthal-derived traits6, 7, 8. Here we determine an almost complete mitochondrial genome sequence of a hominin from Sima de los Huesos and show that it is closely related to the lineage leading to mitochondrial genomes of Denisovans9, 10, an eastern Eurasian sister group to Neanderthals. Our results pave the way for DNA research on hominins from the Middle Pleistocene.

Link

Late Middle Pleistocene teeth from South China (Liu et al. 2013)

From the paper:

The Panxian Dadong P3 falls in the upper left quadrant, an area that, with the exception of two out of the nine Atapuerca-SH specimens and S7-34, is exclusively occupied by recent humans. Thus this geometric morphometric analysis indicates that the general crown conformation of the Panxian Dadong P3 resembles some European Middle Pleistocene hominins, Chinese Upper Pleistocene hominins, and particularly the recent human specimens.  

According to the above comparisons, the Panxian Dadong P3 preserves some primitive and highly polymorphic traits, but in general its conformation is derived. Its occlusal morphology is simple, and the contour is symmetrical with a lingual cusp that is narrower than the buccal one. All these features make the Panxian Dadong P3 most similar to Upper Pleistocene hominins and recent humans in our comparative samples.

I suspect that the age of these teeth will render them useless for ancient DNA work.

Journal of Human Evolution doi:10.1016/j.jhevol.2012.10.012

Late Middle Pleistocene hominin teeth from Panxian Dadong, South China

Wu Liu et al.

The hominin teeth and evidence of hominin activities recovered from 1991 to 2005 at the Panxian Dadong site in South China are dated to the late Middle Pleistocene (MIS 8–6 or ca. 130–300 ka), a period for which very little is known about the morphology of Asian populations. The present study provides the first detailed morphometric description and comparisons of four hominin teeth (I1, C1, P3 and P3) from this site. Our study shows that the Panxian Dadong teeth combine archaic and derived features that align them with Middle and Upper Pleistocene fossils from East and West Asia and Europe. These teeth do not display any typical Neanderthal features and they are generally more derived than other contemporaneous populations from Asia and Africa. However, the derived traits are not diagnostic enough to specifically link the Panxian Dadong teeth to Homo sapiens, a common problem when analyzing the Middle Pleistocene dental record from Africa and Asia. These findings are contextualized in the discussion of the evolutionary course of Asian Middle Pleistocene hominins, and they highlight the necessity of incorporating the Asian fossil record in the still open debate about the origin of H. sapiens.

Link

AAPA 2013 abstracts

The program of the 2013 meeting of the American Association of Physical Anthropologists is now online (pdf). As always, there is plenty of interest here, so I'll just highlight a few titles that caught my eye; feel free to add more in the comments.


Neolithic human mitochondrial haplogroup H genomes and the genetic origins of Europeans.

Haplogroup (hg) H dominates present-day Western European mitochondrial (mt) DNA variability (>40%), yet was less prevalent amongst early Neolithic farmers (~19%) and virtually absent in Mesolithic hunter-gatherers. To investigate this haplogroup’s significance in the maternal population history of Europeans we employed novel techniques such as DNA immortalization and hybridization-enrichment to sequence 39 hg H mt genomes from ancient human remains across a transect through time in Neolithic Central Europe. The results of our population genetic analyses reveal that the current patterns of diversity and distribution of hg H were largely established during the Mid-Neolithic, but with substantial genetic contributions from subsequent pan-European cultures such as the Bell Beakers, which expanded out of Iberia in the Late Neolithic (~2800 BC). Using a strict diachronic approach allowed us to reconcile ‘real-time’ genetic data from the most common European mtDNA hg with cultural changes that took place between the Early Neolithic (~5450 BC) and Bronze Age (~2200 BC) in Central Europe. This revealed the Late Neolithic (2800-2200 BC) as a dynamic period that profoundly shaped the genetic landscape of modern-day Europeans. Furthermore, linking ancient hg H genome sequences to specific points in time by using radiocarbon dates as tip calibrations allowed us to reconstruct a precise lineage history of hg H and to calculate a mutation rate 45% higher than traditional estimates based on the human/chimp split.

Preliminary research on hereditary features of Yinxu Population.

... The 37 individuals sampled in this study have been discovered in middle to small size burials, and therefore constitute a representative sample to study Yinxu commoners’ society. Mitochondrial DNA analysis showed that the Yinxu population included the haplogroups D, G, A, C, Z, M10, M*, B, F and N9a. According to the analysis of molecular variance, the distribution frequency and the rare published data, the Yinxu population shows a closest genetic affinity with the populations of Dadianzi and Zhukaigou early Bronze Age sites (Inner Mongolia), but a more distant relation to the historical period populations. The Yinxu population is also very similar to the modern northern Han Chinese. ... 

Investigating lactase persistence in a Medieval German cemetery: A step towards understanding the rise of the European lactase persistence polymorphism (-3910C/T).

Previous ancient DNA-based studies on the Neolithic found that the incidence of LP falls below detection levels in most regions. Our research shows that between the Neolithic and Medieval periods, the frequency of LP rose from near 0% to over 50%. Also, given that the frequency of LP genotypes in modern-day Germany is estimated at 78.5%, our results indicate that rather than being stable by the Medieval period, the lactase persistent genotype has continued to increase in frequency over the last 1000 years. This new evidence sheds light on the dynamic evolutionary history of the European lactase persistent trait and its global cultural implications.

 New Neanderthal remains from Kalamakia cave, Mani peninsula, Southern Greece.

Peeling back the layers: additional evidence for the date of the Petralona skull (Homo heidelbergensis), Greece.

,.. We conclude that there is no white sinter deposited directly on the skull and therefore the initial date of the skull given by Henning et al. and Grun’s revised date of ca. 200 ka are correct.

Analysis of archaic introgression in Ötzi the Tyrolean Iceman, a 5300 year-old prehistoric modern human.

... We carried out a series of comparisons to address these questions. By examining the Neandertal similarity of individuals from the 1000 Genomes Project, we have substantially expanded the sample of Neandertal-human comparisons. We also examined the genome of the Tyrolean Iceman, a European from approximately 5300 years ago. This is the first comparison of Neandertal genomes to the genome of a prehistoric modern human individual.

A quantitative approach for late Pleistocene hominin brain size.

... The results of our study show that Neanderthals have smaller brains than the Pleistocene AMH despite the fact that the latter are smaller in body mass. However, the Holocene AMH (7 populations) have smaller brain sizes than those of Neanderthals. ...

Re-evaluating the functional and adaptive significance of Neandertal nasofacial anatomy.

... Among Middle and Late Pleistocene Homo, there is evidence that nasal morphology varies with climate, albeit within an archaic architectural nasofacial framework. Neandertal internal nasal dimensions are greater in both height and length than archaic humans from sub-Saharan Africa. Furthermore, while other aspects of the nose are relatively broad, superior internal breadth dimensions in Neandertals are narrowed relative to sub-Saharan archaics. These differences parallel those seen in modern humans, indicating that Neandertals had an increased capacity for nasal heat and moisture exchange over their African counterparts and thus exhibit clear evidence for cold-climate adaptation. 

Balanica BH-1: 397-525 thousand years old

The occurrence of derived Neandertal traits in Sima vs. their absence in penecontemporaneous samples from  southeastern Europe is fairly interesting. It might suggest that the Neandertal suite of traits first appeared in western Europe.

We tend to think of Old World H. heidelbergensis as a parental species which produced -at least in the western part of the Old World- two descendant species, sapiens and neanderthalensis, but clearly that is not the whole story. Unrelated to the current paper, but perhaps worthy of note is that these two descendant species make their appearance far apart in time, with Neandertaloid traits already in evidence very early in Europe, and modern human ones late in east Africa. We may wonder about what was taking place in the temporal gap between 600 and 200 thousand years ago, and the spatial gap between Europe and Africaa.

PLoS ONE 8(2): e54608. doi:10.1371/journal.pone.0054608

New Radiometric Ages for the BH-1 Hominin from Balanica (Serbia): Implications for Understanding the Role of the Balkans in Middle Pleistocene Human Evolution

William J. Rink et al.

Newly obtained ages, based on electron spin resonance combined with uranium series isotopic analysis, and infrared/post-infrared luminescence dating, provide a minimum age that lies between 397 and 525 ka for the hominin mandible BH-1 from Mala Balanica cave, Serbia. This confirms it as the easternmost hominin specimen in Europe dated to the Middle Pleistocene. Inferences drawn from the morphology of the mandible BH-1 place it outside currently observed variation of European Homo heidelbergensis. The lack of derived Neandertal traits in BH-1 and its contemporary specimens in Southeast Europe, such as Kocabaş, Vasogliano and Ceprano, coupled with Middle Pleistocene synapomorphies, suggests different evolutionary forces acting in the east of the continent where isolation did not play such an important role during glaciations.

Link

Who inhabited the Jubbah lake in the Nefud Desert during the Middle Paleolithic?

Many readers may have heard of the Nefud Desert while watching Lawrence of Arabia (was that filmed on location?). It is hard to imagine that desolate landscape as being instrumental in the tale of human origins, but it may very well have been. A new paper describes Middle Paleolithic settlement evidence from the Jubbah Palaeolake, especially during MIS stages 7 and 5.

Arabia is a very interesting case for a variety of reasons: It has to be implicated one way or another in the tale of human origins and dispersals: it lies in the natural route Out-of-Africa, and in the intermediate space between the early modern human remains from Ethiopia, the later modern humans from the Levant, as well as the disputed late Neandertals of West Asia.

Unfortunately, current climatic conditions, as well as past episodes desiccation have resulted in substantial population; if anyone wanted to find out what the people who lived there during the Middle Paleolithic were like, he will find little continuity between them and the current inhabitants. The lack of genetic evidence is, unfortunately also accompanied by a general lack of anthropological evidence. Industries with links to Africa or the Levant are devoid of associated remains. But, the paper produces a hopeful note:

Yet, recent support for an MIS 5 expansion of Homo sapiens comes from archaeological finds of characteristic Middle Palaeolithic technologies in Arabia in MIS 5e–c [19]–[20] and nuclear genomic estimates which indicate that the split between Africans and non-Africans occurred as early as 130 to 90 ka [41], consistent with fossil finds of Homo sapiens in the Levant [52], [53] and at the time of possible interbreeding of Homo sapiens and Neanderthals [54]. These controversies indicate the need to recover hominin fossils in Arabia, which is feasible given the identification of Pleistocene mammalian fauna in a nearby lake basin of the Nefud [24], [55].

In the absence of genes or bones, we can only make inferences based on stones, which may not have a direct correspondence with populations. While Figure 17 from the paper (left) shows a clear differentiation of India vis a vis. the west, relationships in the Near East and Africa are not as clear cut; Skhul resembles North Africa (Haua Fteah and Aterian) and it would be tempting to associate them with Homo sapiens. But, Horn of Africa MSA  -where the earliest anatomically modern humans were found- is linked to El Wad, Tabun C, and Jebel Qattar/Katefeh, the latter two sites being the ones from the Nefud.

Tabun is associated with Neandertals, although that attribution, like most everything in palaeoanthropology is controversial.So, it might be possible that the Jubbah was occupied by Neandertals too, and this might make this population a prime candidate for the signal of Neandertal admixture carried by non-Africans.

At present, there seem to be two candidates for the modern human Out-of-Africa: Skhul (Levant; linked to Northwest Africa here) and the Nubian technocomplex of (south Arabia; linked to Northeast Africa). I don't have a clear picture of how it may have all played out; it would certainly be wonderful if it were possible to extract DNA from, say, Skhul/Qafzeh modern humans or the Levantine Neandertals, because that would definitely show how (i) the former may either be related to later Eurasians, or may be a failed experiment as hitherto supposed, and (ii) the latter might be a source of Neandertal DNA in non-Africans, or indeed something much closer to modern humans as their morphological intermediacy might suggest.

PLoS ONE 7(11): e49840. doi:10.1371/journal.pone.0049840

Hominin Dispersal into the Nefud Desert and Middle Palaeolithic Settlement along the Jubbah Palaeolake, Northern Arabia

Michael D. Petraglia et al.

The Arabian Peninsula is a key region for understanding hominin dispersals and the effect of climate change on prehistoric demography, although little information on these topics is presently available owing to the poor preservation of archaeological sites in this desert environment. Here, we describe the discovery of three stratified and buried archaeological sites in the Nefud Desert, which includes the oldest dated occupation for the region. The stone tool assemblages are identified as a Middle Palaeolithic industry that includes Levallois manufacturing methods and the production of tools on flakes. Hominin occupations correspond with humid periods, particularly Marine Isotope Stages 7 and 5 of the Late Pleistocene. The Middle Palaeolithic occupations were situated along the Jubbah palaeolake-shores, in a grassland setting with some trees. Populations procured different raw materials across the lake region to manufacture stone tools, using the implements to process plants and animals. To reach the Jubbah palaeolake, Middle Palaeolithic populations travelled into the ameliorated Nefud Desert interior, possibly gaining access from multiple directions, either using routes from the north and west (the Levant and the Sinai), the north (the Mesopotamian plains and the Euphrates basin), or the east (the Persian Gulf). The Jubbah stone tool assemblages have their own suite of technological characters, but have types reminiscent of both African Middle Stone Age and Levantine Middle Palaeolithic industries. Comparative inter-regional analysis of core technology indicates morphological similarities with the Levantine Tabun C assemblage, associated with human fossils controversially identified as either Neanderthals or Homo sapiens.

Link

Pre-Neolithic Mediterranean Island settlement

PhysOrg coverage of a Science perspective:

Modern science has held that islands such as Cyprus and Crete were first inhabited by seafaring humans approximately 9,000 years ago by agriculturists from the late Neolithic period. Simmons writes that research over the past 20 years has cast doubt on that assumption however and suggests that it might be time to rewrite the history books. He cites evidence such as pieces of obsidian found in a cave in mainland Greece that were found to have come from Melos, an island in the Aegean Sea and were dated at 11,000 years ago as well as artifacts from recent digs on Cyprus that are believed to be from approximately 12,000 years ago. He adds that some researchers have also found evidence that something, or someone caused the extinction of pygmy hippos on Cyprus around the same time.  

Simmons also suggests that the first inhabitants of many of the Mediterranean islands may not have been modern humans at all. Instead, he says evidence has been found that shows that they might have been Neanderthals, or Homo Erectus. Recent excavations on Crete have turned up artifacts that are thought to be 110,000 years old, for example, and a stone axe was found that is believed to have been made on the same island as far back as 170,000 years ago. Since modern humans are believed to have come into being roughly 100,000 to 200,000 years ago, the possibility exists that such artifacts were left behind by an early ancestor or cousin.

Science 16 November 2012: Vol. 338 no. 6109 pp. 895-897 DOI: 10.1126/science.1228880

Mediterranean Island Voyages

Alan Simmons

Some of the classical world's most innovative cultures developed on Mediterranean islands, but their earlier human use is poorly known. The islands, particularly those further from the mainland such as Crete and Cyprus, were thought to have been first colonized about 9000 years ago by late Neolithic agriculturalists with domesticated resources. Until about 20 years ago, claims of earlier, pre-Neolithic occupations on any of the islands did not stand up to critical scrutiny (1), but current investigations are challenging these perceptions. Discoveries on Cyprus, Crete, and some Ionian islands suggest seafaring abilities by pre-Neolithic peoples, perhaps extending back to Neanderthals or even earlier hominins. In Cyprus, Neolithic sites have been documented that are nearly as early as those on the mainland.

Link

Longer time scale for human evolution (Hawks 2012)

Scally and Durbin published a recent review on the implications of a slower human autosomal mutation rate, and now John Hawks has a commentary on the same topic in PNAS (pdf; paywall). He goes through a lot of the evidence of early fossil hominins and ape and mentions several examples that harmonize with the slower mutation rate. As expected, he also finds a better agreement of the slow mutation rate with the evidence for Neandertals where 530,000 year old finds from Atapuerca show signs of belonging to the Neandertal lineage, a date that is inconsistent with a late divergence of modern humans and Neandertals. Finally, he has this to say about modern humans:

Across this same time scale, the archaic ancestors of today’s Africans had already developed an intricate population structure. Genomic investigation of African hunter–gatherers has opened new windows onto this deep genetic history of differentiation and introgression (14, 15), bringing the origin of modern African diversity into the population structure of the early Middle Pleistocene. A simple hypothesis of modern human origins in a bottlenecked population cannot account for this diverse genetic history.    

The mtDNA time scale now poses a hanging question. Mitochondrial mutations occur much more often than nuclear DNA mutations, with greater heterogeneity among sites (16). Still, our estimate of mtDNA substitution rates depends on our estimates of branch lengths of the primate phylogeny. Until now, mitochondrial comparisons have been the strongest evidence in favor of a short time scale for the dispersal and differentiation of non-African peoples, within the past 70,000 y (17). Some recent attempts to examine the relationships of non-African populations using nuclear genome data have led to time scales in excess of 100,000 y (18), and others favor more recent estimates (19). Despite the recency of this work, most authors have continued to use an outdated fast molecular clock and short generation time estimates. As we move forward, such results will need to be corrected or adjusted to enable comparisons with current work. 

There is a very interesting question here, which I've mentioned before, but is worth repeating: admixture between divergent lineages can inflate split times. Acceptance of the slow autosomal mutation rate will result in split times in excess of 100 thousand years for Africans vs. non-Africans, and perhaps 300 thousand years for African hunter-gatherers. On the other hand, the mtDNA clock (haplogroup L3 = 70ky), no matter how it is recalibrated is unlikely to match these old dates, and the Y-chromosome clock (current estimate of its root a little more than 100 ky, and of the dominant African lineage E on the cusp of the LSA) will certainly not match them.

In my opinion, it will slowly become apparent that the way to harmonize our picture of human origins is to accept a substantial degree of archaic admixture in Africa. Such admixture cannot be detected directly, because there are no archaic genomes from Africa, and the hot climate throughout much of the continent may make preservation of DNA more difficult than in northern parts of Eurasia (where Neandertal and Denisovan individuals were from). Nor can it always be detected with LD-based methods, since LD decays exponentially and really old admixture is indistinguishable from an excess of mutation in a large population size. But, its acceptance will simultaneously solve the riddle of excess polymorphism in Africans, remove the need for an Out-of-Africa bottleneck of biblical proportions, and resolve the discrepancy between autosomal and uniparental evidence.

Why We Prevailed: Evolution and the Battle for Dominance

 I haven't watched it yet, but the list of participants is interesting. From the description:

We once shared the planet with Neanderthals and other human species. Some of our relatives may have had tools, language and culture. Why did we thrive while they perished? Join evolutionary biologists, geneticists and anthropologists as they share profound insights about the origin of man and retrace our singular journey from fledgling prototype to the most dominant species on Earth.

I'll update this entry if I notice anything novel said in the program.

Population-specific SNPs and archaic admixture in Homo sapiens

A population-specific SNP is one which both alleles occur in a population X and only one in the rest of mankind. The existence of such SNPs can be explained in three different ways:

1. Both alleles belong to the ancestral gene pool of H. sapiens but were lost (by selection or drift) in most populations except one.
2. Ancestral humans were monomorphic, but a new allele appeared by mutation in one population, and there has not been enough time or opportunity for it to spread to the others.
3. An additional allele introgressed into a population by admixture with a regional population of archaic humans; this is equivalent to (2), with the new allele appearing through admixture, rather than new mutation.

In order to identify alleles that are specific to the major human groups, I carried out an ADMIXTURE analysis of the Harvard HGDP set with K=5. The results can be seen below, and as is expected, five major clusters emerge:

ADMIXTURE outputs a *.P file of allele frequencies in the inferred components. I used this file to identify population-specific alleles. Specifically, I identified, for each of the 5 components, SNPs where they were polymorphic, but all the other 4 components were fixed. This is the harvest of such component-specific alleles:

Asian: 2,321
West_Eurasian: 4,516
African: 50,835
Australasian: 1,726
Amerindian: 62

Note, that these numbers do not reflect on the relative number of population-specific SNPs across the genome. Nonetheless, they do appear concordant with what we know about the diminution of genetic diversity away from Africa.

Note also that these SNPs were identified only on the basis of comparisons between modern populations.

In all the following experiments, I will calculate D-statistics of the form D(Pop1, Pop2, Neandertal, Chimp) and D(Pop1,Pop2, Denisova, Chimp) to assess whether Pop1 matches Neandertal/Denisova more than Pop2 does.

Using Asian-specific SNPs

Han matches Neandertal 69% more than Sardinian does
Japanese matches Neandertal 71% more than Orcadian does
Dai matches Neandertal 69% more than Mandenka does
Cambodian matches Neandertal 52% more than San does
She matches Neandertal 5% more than Miao does

These results are consistent with a large number of Asian-specific alleles having been inherited from Neandertals or a Neandertal-like population.

Using West Eurasian-specific SNPs

Sardinian matches Neandertal 63% more than Han does
Orcadian matches Neandertal  61% more than Japanese does
Italian matches Neandertal 55% more than Mandenka does
French matches Neandertal 57% more than San does
Tuscan matches Neandertal 11% more than Basque does

Again, these results are consistent with many West Eurasian-specific alleles having been inherited from Neandertals or a Neandertal-like population.

Using African-specific SNPs


Dai matches Neandertal 55% more than Mandenka does
Cambodian matches Neandertal 41% more than San does
Italian matches Neandertal 55% more than Mandenka does
French matches Neandertal 41% more than San does
BantuKenya matches Neandertal 11% more than MbutiPygmy does

It thus appears that a substantial number of African-specific SNPs make Africans appear less Neandertal-like than Eurasians. This is unexpected if African-specific SNPs are common human SNPs that were retained in Africa but lost Out-of-Africa due to a bottleneck, or if they are SNPs that appeared recently by mutation in the African population.

They are, however, consistent with the following model:

This model is consistent with the evidence: Eurasian-specific alleles tend to match Neandertals, consistent with Neandertal introgression into the population of Eurasians. But, African-specific alleles tend not to match Neandertals.

This can be explained by the presence of archaic African admixture that stems from before the common ancestor of modern humans and Neandertals.

Denisova admixture in Australasian-specific SNPs

Papuan matches Denisova 84% more than Mandenka does
Melanesian matches Denisova 85% more than San does
Papuan matches Denisova 84% more than Sardinian does
Melanesian matches Denisova 85% more than Orcadian does
Papuan matches Denisova 84% more than Japanese does
Melanesian matches Denisova 85% more than Dai does
Papuan matches Denisova 24% more than Melanesia does

It will thus appear that in many Australasian-specific SNPs, Papuans/Melanesians match the Denisovan allele much more often than other populations.

(As a sanity check for my calculations, I note that Reich et al. 2011 (Table 2) inferred that Bougainville Melanesians have 82% of the Denisova ancestry that Papuans do on the basis of genotype data, and hence, Papuans have (100-82)/82 = 22% more, which closely matches my 24% figure)

African diversity in perspective

It is often said that non-Africans harbor a subset of African genetic variation, but that is not really generally true in the strict mathematical sense of "subset". For the 50,835 African-specific SNPs it is true that Africans are polymorphic whereas all other populations are monomorphic. But, for the 2,321 Asian-specific, and 4,516 West Eurasian-specific SNPs it is Asians and West Eurasians respectively that are polymorphic, whereas Africans and all remaining populations are monomorphic.

By examining these special sets of SNPs, where a regional human population is polymorphic and all the rest of mankind is not, we have been able to show that relationships with archaic humans are amplified. The implication is direct: regional-specific variation in humans is in part the heritage of regional continuity in both Africa and Eurasia. However it was that H. sapiens came to dominate our planet, it was not by extinction of archaic humans.

Human population differentiation: tree-like divergence or admixture between divergent demes?

What can account for differences between continental human populations? There are two explanations: (1) Tree-Like Divergence and (2) Incomplete Admixture between divergent demes.

(1) Until quite recently, it was near-universally thought that modern humans are the descendants of a single recent African population. Differences between human groups were ascribed to the operation of genetic drift, natural selection, and new mutation, as modern humans left their primordial Eden and expanded to populate the rest of the globe. According to this model: humans became more different from each other over time.

(2) But, there is a different idea, the reverse of the previous one: that modern humans are descended from many regional groups of earlier hominins that were very highly differentiated from each other. These earlier groups did of course diverge from common ancestors, but in the remote past; perhaps they represent long branches stemming from Homo heidelbergensis. Gene flow between them intensified as humans became more numerous and more mobile, According to this idea, humans around the world became more similar to each other over time.

We are now in a position, through the power of ancient DNA, to answer this question empirically. I am pretty sure that we will answer it over the next decade. And, the way to answer it is simple: take an UP West Eurasian, an UP East Asian, and a LSA African. Under the model of tree-like divergence, these ought to be genetically closer than a living European, a living East Asian, and a living African are to each other, because ~30-40ky of drift and selection acted independently on the three branches:

I suspect that we will be quite surprised when we look at the data, for a number of reasons:

1. Low genetic diversity of Denisova hominin, consistent with a model in which human diversity is generated by admixture between populations with low intra-group (as in Denisova), but high inter-group diversity (see point #2).
2. Higher genetic divergence between Denisova and Vindija (across ~6Mm of distance) than between any two living humans from the entire globe.
3. Diminution of human cranial variability over time, and disappearance of archaic forms.
4. Possibility of greater Neandertal admixture in UP Europeans than in recent ones.

In any case, if the the UP/LSA folks look like close relatives, we will know for sure that tree-like divergence did indeed shape our differentiation: we started very similar, and ended up different. But if they're not, then the door will open for a greater appreciation of how substantial archaic admixture, tempered by gene flow, has been a major cause of differences between living populations of mankind.

Looking forward to finding out...

Raising a peace banner in the Neandertal Wars

The two camps in the Second Neandertal Wars (*)  have assumed maximalist positions on opposing sides of the argument: African structure explains it! vs. Neandertal admixture explains it!. Armed with the Vindija genome, that marvel of technological ingenuity, and a suite of impressive statistical models, the two sides have reached completely opposing conclusions.

In order to formulate my own position, I decided to do what I love best, i.e., to look at the data for myself. My main idea is that the signals of Neandertal and Denisova admixture as measured by these quantities (D-statistics) ...

D(Pop1, Yoruba, Neandertal, Chimp)

D(Pop1, Yoruba, Denisova, Chimp)

... will vary on different SNP ascertainment panels. SNPs ascertained in Africans may have a great number of Palaeoafrican alleles; SNPs in Neandertal-admixed populations will have a great number of Neandertal alleles; SNPs in Denisova-admixed populations will have a great number of Denisova alleles. If a population has admixture from hominin X, this admixture, as measured by the D-statistic, will tend to be inflated in panels possessing alleles that introgressed from X, and suppressed in panels that lack them.

The issue of ascertainment and archaic admixture was addressed by Skoglund and Jakobsson (2011); my aim is different: I am not so much interested in how ascertainment affects admixture estimates, but rather in exploiting the observation of the preceding paragraph (that Palaeoafrican, Neandertal, or Denisovan SNPs will lurk at different rates when ascertained in different individuals) to see what it tells us about human differences.

The signal of "archaic admixture" may be generated by genuine archaic admixture in one population (e.g., Eurasians), making it more similar to the archaic group (e.g., Neandertals), or by archaic admixture -of a different sort- in another population (e.g., Africans), making it less similar to that group. Both these processes may be at work, operating at different intensity in different populations and across different timelines.

I used the Harvard HGDP set, which contains 12 SNP panels, each of which has been ascertained in two chromosomes of a single individual. These panels are:

San, Yoruba, Mbuti, French, Sardinian, Han, Cambodian, Mongolian, Karitiana, Papuan1, Papuan2, Melanesian

A D-statistic was calculated relative to either Neandertal or Denisova for all HGDP populations, as well as the two archaic hominins. Subsequently, I used MCLUST to infer the number of different clusters on the basis of these statistics. In the optimal solution, MCLUST inferred 7 clusters, with each archaic hominin getting its own cluster, while the modern human populations were assigned to 5 clusters corresponding to five major human races recognized by traditional physical anthropology (Mongoloid, Negroid, Australoid, Capoid, and Caucasoid).

Note that these are not admixture proportions, but assignment probabilities! All populations fell into their expected clusters. The populations from Pakistan who are believed to be predominantly Caucasoid with varying degrees of minor admixture of an Ancestral South Indian element were assigned to the Caucasoid cluster. So did the Mozabite Berbers, a Caucasoid population with minority Negroid admixture. Finally, of the Central Asian populations, the Hazara of Pakistan showed mixed affiliations in the Caucasoid and Mongoloid clusters, while the Uygur were assigned to the Mongoloid cluster.

It is noteworthy that by exploiting patterns of relationship of modern to regional archaic humans, we have managed to recreate the major human groups. This is, perhaps, supportive of those who have argued that a degree of regional continuity across the Old World, and not only recent post-Out of Africa genetic divergence is responsible for present-day inter-population differences.

MCLUST also gave us the D-statistic means for the 7 inferred clusters. Remember that these are differences between a population Pop1 and Yoruba, relative to an archaic hominin (Neandertal or Denisova), and for 12 different ascertainment panels:

There are wonderful patterns to be discovered here; you can look at the data for yourselves; that's the open science thing to do.

All our ideas about human origins are conditioned on the availability of genomes from two archaic Eurasian hominins, and the lack of genomes of similar age from Africa.

But, remember:

• You can fit Europe, China, India, and the US into Africa, with room to spare. 
• If Vindija and Denisova, two caves less than 5,000km apart were home to people more divergent from each other than any two humans are today, it's strange to think that only "modern humans" inhabited Africa at the same time. 
• The maximum genetic distance between living Africans is much higher than the maximum distance between living Eurasians: Africa is much more diverse than Eurasia. It's simpler to assume that the same relative pattern was true during the Middle Stone Age. The palaeoanthropology seems to support this, showing archaic forms present even during the terminal Pleistocene in Africa.
• If modern humans did interbreed with 2/2 archaic humans whose sequences we possess, it's strange to think that they somehow shunned the African Others.

In view of the above, I humbly raise my peace banner in the Neandertal Wars, and declare that it isn't either-or: it's both!

(*) The First Neandertal Wars were fought decades ago by anthropologists working with calipers and magnifying lenses. Their outcome was to relegate Neandertals from the enviable position of our likely ancestors to that of an irrelevant sidekick, although a not-negligible minority continued an insurgency against the Out-of-Africa-only victors.

Neandertals converging with modern humans, not evolving separately

In my discussion of Di Vincenzo et al. (2012) and Freidline et al. (2012), I noted how Neandertals appeared to be converging towards a modern human form; this seemed to occur both with respect to the ancestral forms usually assigned to the taxon H. heidelbergensis, but also with respect to earlier Neandertals. Some of the most "modern-looking" Neandertals are late specimens such as Vindija (the main source of the Neandertal genome), and these often appear more similar to modern humans than many earlier (pre-100ka) specimens.

A book chapter by Milford Wolpoff and Sang-Hee Lee ("The African origin of recent humanity" in African Genesis: Perspectives on Hominin Evolution (2012), eds. Sally C. Reynolds and AndrewGallagher) explores a similar topic.

The following figure illustrates a model in which recent African Homo, represented by Herto, the hypodigm of H. sapiens idaltu, and Neandertals represent separately evolving lineages whose precursors are the Broken Hill cranium (Kabwe) and Petralona, a pre-Neandertal European hominin from Greece.

Kabwe is much more primitive than Herto. A recent paper lists it simply as greater than 125ka, and Chris Stringer has cast doubt about its great antiquity. Tim White, on the other hand, considered it a precursor of the Herto skull, which he considered the first evidence of anatomically modern humans in Africa, still possessing archaic traits. This contention was, however, upset by the redating of the Omo remains from Ethiopia to ~195ka, making them much older than Herto. So, if Kabwe is near 125ka, it might even appear that the chronological sequence Omo-to-Herto-to-Kabwe is associated with increasing archaicity. So much for a model of H. sapiens gradually emerging in Africa out of more primitive forms; the recent publication of the Iwo Eleru skulls from Nigeria, and Ishango from the Congo are certainly not adding to our confidence that any such process of linear Ascent of Man in Africa ever took place.

But, I'm digressing; if we can't really find a clear signal of a series of human forms in Africa leading to modern humans, perhaps we can find that Neandertals are becoming less and less like modern humans, as time passes since their last "common ancestor".

So, let's get back to the Wolpoff and Lee chapter. The authors contrast the model of separately evolving lineages with one of paleo-demes, defined as:

A palaeo-deme as used here is a ‘designation, reflecting inclusive genealogically related geographic group(s)’ (Howell, 1999 : 203)

The whole matter revolves around the issue of gene flow and selection. If Herto and Neandertals represent separately evolving lineages, then their distance from each other ought to be greater than the distance of either one to the more archaic specimen from the same region. Herto ought to be closer to Petralona than to Neandertals if Neandertals continued to evolve as a separate lineage for 100-200 thousand years after Petralona lived (depending on the age of that specimen).

But, this is not what is observed at all (right). Herto appears closer to Neandertals Shanidar 1, La Ferassie 1, and Amud than to Petralona. Contrary to expectation, Neandertals are apparently converging with African groups of similar age, they are not diverging from them.

One could also observe, that lower differences occur between Herto and some Neandertals (e.g., with Shanidar 1) than between Herto and some anatomically modern humans (e.g., with Skhul 5, Qafzeh 6, and Jebel Irhoud 1).

So, while we will probably continue to hear about estimates of the "time of divergence" between Neandertals and modern humans, we must remember that this may be a mirage. Of course, when geneticists do their calculations, they can fit a tree model to human evolution, in which lineages branch out, become reproductively isolated, and die out, leaving a single twig, African H. sapiens to survive. But, admixture matters:

In fact, the ability of admixture to "converge" populations is the basis of the multi-regional evolution theory, although that is usually posited in terms of gene flow. But, the basic idea is still the same: our relatively uniform human species may not be entirely the result of tree-like divergence of populations from an original African population, but rather of a confluence of streams of ancestry derived from Lower and Middle Paleolithic populations of Homo.

Here are the facts:

1. Geneticists have sequenced the genomes of two archaic hominins (Neandertals and Denisovans): both are differentially affiliated to regional groups modern humans: archaic humans can no longer be considered irrelevant twigs of the human family tree.
2. Geneticists have identified segments of archaic DNA that have introgressed in certain African populations. It seems that archaic admixture is ubiquitous in the human species, even in its supposed cradle.
3. Neandertals and modern humans do not appear to diverge from each other phenotypically as time goes by: rather they seem to converge; they increasingly become more modern-like as time goes by. The analysis on the left beautifully illustrates this (Freidline et al. 2012): Shanidar 5 Sh5 a late Neandertal is within the modern human convex hull and several other Neandertals are close to modern humans; strange behavior indeed, if these guys are supposed to be diverging on a separate path from African humanity)

There is other evidence besides: Mounier et al. (2011) noted that even within the group of modern skulls the most ancient examples were more archaic-looking.  This would agree with the findings of Crevecoeur et al. (2009) that recent mankind possesses a subset of Late Pleistocene variation. It is also, indirectly supported by the findings of Reich et al. (2010), according to which, the genetic divergence of Neandertals and Denisovans (644ky), two contemporaneous populations living in a part of Eurasia exceed the total genetic divergence of all modern human populations (maximum: San-Papuan, 607ky).

An objection to the multiregional model of evolution revolves around the idea that we have "very little" Neandertal or Denisovan ancestry to qualify as truly "multiregional." But, there are two flaws to this objection:

First, it introduces an arbitrary distinction: no one expects different regional human groups to have contributed equally, or even comparably to recent mankind: some populations (say Homo floresiensisis) may have been truly isolated and may have contributed nothing. Others may have inhabited lands with low carrying capacity (say dense, impenetrable tropical rainforest or the fringes of the glaciers), or may have acquired key innovations later than others. So, while the majority of modern human ancestry may stem from a restricted geographical region (in my opinion the Sahara-Arabia belt around 100 thousand years ago), other human groups (such as Neandertals, Denisovans, archaic Africans, etc.) are not irrelevant: they are our ancestors too.

Second, the idea that admixture with archaic hominins was "little" is based on little more than a misunderstanding of the evidence. Mike Hammer explains this succinctly in this talk:

But remember, this is all relative to Africans, it doesn't tell you if Africans have a lot of Neandertal DNA or a little bit of Neandertal DNA: it's just that non-Africans are elevated one little bit up, a step higher than the Africans with respect to Neandertal sharing.

In other words, it's not only x% Neandertal in Eurasians and 0% in Africans; it can also be 10+x% in Eurasians and 10% in Africans: we can only estimate relative levels of influence, not absolute ones. Absolute levels could only be estimated if we had the genomes of old Africans: we would then see modern Eurasians and Africans arrayed on the Old African-Neandertal line, the former a little closer to Neandertals than the latter. But it is far from clear that modern humans in Africa would have escaped Neandertal gene flow altogether.

To conclude, a final quotation from Wolpoff and Lee:

The Europeans are not evolving in a different direction, away from the rest of humanity. The European palaeo-deme , including Neandertals, evolved to be more similar to the descendents of Herto over time, not less similar. The convergence of African and European palaeo-demes demonstrates the presence of gene flow between them, and we agree with the description of these palaeo-demes as ‘varieties in a single metapopulation’ (Hawks and Cochran, 2006 ). Moreover, later than the Neandertals, post-Neandertal anatomical variation in Europe includes Neandertal features, even features that evolved locally to be characteristic of most or all Neandertals and were rare or absent in other regions. 

I am strongly leaning towards acceptance of something quite akin to multiregionalism; it is almost certainly true in a sense: the evidence for widespread archaic admixture it irrefutable. On the other hand, there does seem to have been a Big Bang in human evolution, associated with mtDNA haplogroup L3, Y-haplogroup BT, and the reduced genetic diversity observed in Eurasians relative to Africans. But this appears to have been more akin to the success of a particular local population within a widespread species, rather than the emergence of an altogether new species.

Morphometric analysis of Zuttiyeh (Freidline et al. 2012)

The Zuttiyeh specimen from Israel (unknown date, but between 500-200ka) is extremely important, because it was found in a region of the world in which the earliest co-existence of modern humans and Neandertals is attested. As such, it may be part of a population that led to either (or both) of these species; the population divergence of the Homo sapiens and Homo neandertalensis lineages intersects the 500-200ka range of this specimen.

A recent paper in the Journal of Human Evolution studied Zuttiyeh using geometric morphometric techniques.

Zuttiyeh (Zt) was compared with a wide range of other specimens from various periods, ranging from Homo erectus to modern humans. The PCA analysis is shown on the left. It is clear that Zuttiyeh clusters with Neandertals in Eurasia (open triangles), as well as "transitional" Homo sapiens from Africa (open squares: Florisbad Fl, 290-230ka from South Africa, and Jebel Irhoud 1 I1, 160ka from Morocco).

On the left (filled triangles) are various specimens assigned to Homo heidelbergensis, the presumed common ancestor of modern humans and Neandertals. For more on this, see Chris Stringer's recent overview article. But, this is no simple ancestor species: rather, it encompasses skulls that are very old (Bodo Bd; Ethiopia ca. 600ka), and very young (Dali Dl; China ca. 200ka). Indeed, Zhoukoudian 12 (Zh12; >500ka China) classified as Homo erectus appears quite modern in comparison to many of the heidelbergensis skulls.

On the right (crosses) are the modern humans, including UP Europeans, as well as, intriguingly Liujiang (Ljg), a modern human from China that may be 119-139ka old according to the people who dated it, but at least 68ka old. If the latter date is accepted, this would be within the error bars of the major 70ka Event that may correspond to the earliest colonization of Eurasia. If the former, then Liujiang will join the Qafzeh 9 specimen as an extremely modern pre-100ka find from Asia.

The Mount Carmel specimens (Qafzeh 6 Q6 and Skhul 5 Sk5; Levant 135-100ka) appear intermediate between H. heidelbergensis/H. neanderthalensis and H. sapiens but can usefully be called H. sapiens, since there are modern humans who appear as "left-shifted" as they are.

Intriguingly, Shanidar 5 (Sh5; ca. 50ka) a Neandertal appears to be much closer to H. sapiens than to his Neandertal brethren (including contemporaneous Sh1). This seems to be in line with a recent analysis of shoulder blades in which Shanidar 3 was included, as was a contemporaneous Vindija Neandertal (= the source of the Neandertal genome). It may well appear that late Neandertals were not diverging away from a modern humans, but rather changing from the ancestral heidelbergensis state in the same way that modern humans are.

A neglected possibility is that the late Neandertals, around the time of the apparent modern human Big Bang experienced gene flow from modern humans. This scenario was rejected in the original publication of the Neandertal genome on the basis of the idea that modern human admixture in Neandertals would have been modern non-African-like, because, presumably it was effected by a wave of Proto-Eurasians leaving Africa. But, if the Big Bang of human expansion occurred in Asia, perhaps in Arabia as it dried up post-70ka, as I have suggested, then modern human admixture could have affected late Neandertals.

The discriminant function analysis is also interesting:

The groups were defined a priori according to the population grouping shown in Table 1. Zuttiyeh as well as all transitional (Jebel Irhoud 1 and Florisbad), early (Skhul 5, Qafzeh 6 and Luijiang) and Upper Paleolithic H. sapiens were treated as individuals with unknown group affinities to be classified by posterior probabilities.

 Florisbad appears to be quite distinct here, while Skhul5 and Qafzeh6 are clearly on their way to becoming modern; Zhoukoudian 101 joins this group (13-33ka), but is about 70-100 thousand years younger. Apparently the population of modern humans in Eurasia pre-100ka was widespread. Individuals of regular modern aspect appear post-70ka Event in both West and East Eurasia (Zh102 and Liujiang, assuming the latter is 68ka old). They probably appear in Africa as well probably in Africa as well.

Sadly, neither Hofmeyr, nor Omo I/II and Herto were included in this analysis. All of the above are often mentioned in connection to modern human origins. So is Kabwe (Broken Hill; Homo rhodesiensis) which is listed here as 700-400ka but may in fact be much younger. Jebel Irhoud 1 a "transitional" Homo sapiens from Morocco seems to have a long way to go to transition to a fully modern shape. Both Amud 1 (Am1; a big-brained late Neandertal from the Levant 50ka) and the aforementioned Shanidar 5 appear just as modern as Irhoud 1.

Can we make any sense of these various facts? I will list some observations:

• Zuttiyeh appears linked to Neandertal and transitional H. sapiens. It is unclear where to place it, except to say that it is an archaic-looking human who is in the process of evolving in the same direction that both Neandertals and modern humans did.
• There does not appear to be any good evidence in this data that H. heidelbergensis underwent a split that led to modern humans and Neandertals. On the contrary, often younger skulls appear more archaic than older ones, and skulls from the same period/region seem to occupy different positions in the archaic/modern range.
• Modern humans appear distinctive, with their closest pre-100ka relatives being the Mt. Carmel hominins from the Levant (Skhul and Qafzeh), as well as, intriguingly, late Near Eastern Neandertals (Amud and Shanidar)

Even during the last 50ky, there seems to have been elevated diversity in modern humans. Zhoukoudian 101 from this study appears to be one example of unusual morphology for so late a specimen; recent discoveries from China and Sub-Saharan Africa point to the same phenomenon.

I continue to think that within the Homo heidelbergensis lineage there was progress towards more modern forms throughout the old world. But, this progress did not replace the older forms; nor did it materialize as obviously divergent lineages. The last few hundred thousand years appear very much like a serious of experiments that lead in some vague way to something akin to us. There probably was a long, drawn-out road to us.

In Africa, the Near East, and Asia, there was a co-existence of quite divergent forms; even Europe, long-considered the exclusive abode of Neandertals, there apparently lived humans  that did not possess the derived Neandertal morphology.

The simple story of our origins is that our common ancestor H. heidelbergensis split into an African and Eurasian lineage that eventually evolved into H. sapiens and H. neanderthalensis, and finally the former replaced the latter, with perhaps a little admixture along the way.

It would appear that aspects of modernity appeared throughout the Old World during the last few hundred thousand years. Perhaps (as the multi-regionalists would have it), this was facilitated by gene flow between distant human groups; alternatively, H. heidelbergensis already had the seeds of his future evolution, and similar solutions were found for similar selective pressures independently.

For the time being, we must probably accept the fact that a great variety of human groups of the last 500,000 years at least have contributed to modern mankind. Only isolated groups like Homo floresiensis who disappeared before having the chance to affect us may have escaped the honor of being our ancestors. But, it also seems that much of our ancestry does come from a unique population emerging somewhere within that broader milieu. Where this population lived and why it became so successful is an open problem, but, until there is evidence to the contrary, I would say that my two deserts theory, as elaborated here, may be a reasonably candidate.

Journal of Human Evolution Volume 62, Issue 2, February 2012, Pages 225–241

A comprehensive morphometric analysis of the frontal and zygomatic bone of the Zuttiyeh fossil from Israel

S.E. Freidline et al.


The Zuttiyeh hominin craniofacial fossil was discovered in Israel in 1925. Radiometric dates and the archaeological context (Acheulo-Yabrudian) bracket the associated cave layers to between 200 and 500 ka (thousands of years ago), making it one of the earliest cranial fossils discovered in the Near East thus far. Its geographic position, at the corridor between Africa and Eurasia, in combination with its probable Middle Pleistocene date make it a crucial specimen for interpreting later human evolution. Since its discovery, qualitative descriptive and traditional morphometric methods have variously suggested affinities to Homo erectus (Zhoukoudian), Homo neanderthalensis (Tabun), and early Homo sapiens (Skhul and Qafzeh). To better determine the taxonomic affinities of the Zuttiyeh fossil, this study uses 3D semilandmark geometric morphometric techniques and multivariate statistical analyses to quantify the frontal and zygomatic region and compare it with other Middle to Late Pleistocene African and Eurasian hominins.

Our results show that the frontal and zygomatic morphology of Zuttiyeh is most similar to Shanidar 5, a Near East Neanderthal, Arago 21, a European Middle Pleistocene hominin, and Skhul 5, an early H. sapiens. The shape differences between archaic hominins (i.e., Homo heidelbergensis and H. neanderthalensis) in this anatomical region are very subtle.

We conclude that Zuttiyeh exhibits a generalized frontal and zygomatic morphology, possibly indicative of the population that gave rise to modern humans and Neanderthals. However, given that it most likely postdates the split between these two lineages, Zuttiyeh might also be an early representative of the Neanderthal lineage. Neanderthals largely retained this generalized overall morphology, whereas recent modern humans depart from this presumably ancestral morphology.


Link (pdf)

Chris Stringer on the status of Homo heidelbergensis

The Natural History Museum has an overview of the status of Homo heidelbergensis, the widely accepted common ancestor of modern humans and Neandertals. This accompanies Chris Stringer's article that will soon appear in Evolutionary Anthropology. The piece from the NHM is quite instructive as it highlights the dubious attribution of the Sima de los Huesos remains to heidelbergensis; Stringer expresses doubts on both their 600ky antiquity and their taxonomic classification, preferring to assign them to early Neandertals.

There was an earlier story in the Guardian with a rather misleading title which quotes some other opinions on the controversy.

(I'll add the abstract to this paper and any further comments on it when it appears on the journal website).

UPDATE (Aug 3): Abstract added; paper is open access.

Evolutionary Anthropology Volume 21, Issue 3, pages 101–107, May/June 2012

The status of Homo heidelbergensis (Schoetensack 1908)

Chris Stringer

The species Homo heidelbergensis is central to many discussions about recent human evolution. For some workers, it was the last common ancestor for the subsequent species Homo sapiens and Homo neanderthalensis; others regard it as only a European form, giving rise to the Neanderthals. Following the impact of recent genomic studies indicating hybridization between modern humans and both Neanderthals and “Denisovans”, the status of these as separate taxa is now under discussion. Accordingly, clarifying the status of Homo heidelbergensis is fundamental to the debate about modern human origins.

Link

Early Neandertals used red ochre

I have never quite understood the fascination of archaeologists with red ochre. As far as I can tell, this fascination stems from the fact that it is a pigment that survives in time, and had been used by the earliest artists during the Upper Paleolithic. By extrapolation, its presence in earlier contexts has been interpreted as evidence of "art" or "symbolic behavior". So, a new paper that appeared in PNAS slightly demystifies the pigment by discovering its use more than 200 thousand years in Europe, probably by early Neandertals, and at the same time as its earliest traces in Africa.

In my opinion, this points to the conclusion that use of pigments and red ochre in particular is not a modern human innovation that was adopted (late) by the sister Neandertal taxon, but rather that something that humans used long-before the advent of "modernity", dating, perhaps, to H. heidelbergensis, the common ancestor of modern humans and Neandertals.

Of interest in that regard is the following tidbit of information from an unrelated source:

Sicevo Gorge - a canyon cut into the Kunivica plateau in southeastern Serbia - contains a series of caves, at least one of which has yielded evidence of human presence during the Ice Age of present-day Europe. In 2008, anthropologists excavating in a small cave uncovered a partial human lower jaw with three teeth. 

"We were looking for Neanderthals," said Dr. Mirjana Roksandic, a participating palaeo-anthropologist with the University of Winnepeg (Canada) and a leading research team member. "But this is much better. 

"What they discovered was definitely a human that, at least in terms of morphology, predated the Neanderthal and may have had more in common physically with Homo erectus - thought by many scientists to be the precursor to both Neanderthals and modern humans. Recent tests conducted by Dr. Norbert Mercier at the University of Bordeaux (France) produced a date of "older than" 113,000 years BP - long before modern humans in present-day Europe - and the fossil could be substantially older.

So, I would not assume that 200-250ky ago in Europe was definitely "early Neandertals".

John Hawks covers the paper in detail.

PNAS doi: 10.1073/pnas.1112261109

Use of red ochre by early Neandertals

Wil Roebroeks et al.

Abstract

The use of manganese and iron oxides by late Neandertals is well documented in Europe, especially for the period 60–40 kya. Such finds often have been interpreted as pigments even though their exact function is largely unknown. Here we report significantly older iron oxide finds that constitute the earliest documented use of red ochre by Neandertals. These finds were small concentrates of red material retrieved during excavations at Maastricht-Belvédère, The Netherlands. The excavations exposed a series of well-preserved flint artifact (and occasionally bone) scatters, formed in a river valley setting during a late Middle Pleistocene full interglacial period. Samples of the reddish material were submitted to various forms of analyses to study their physical properties. All analyses identified the red material as hematite. This is a nonlocal material that was imported to the site, possibly over dozens of kilometers. Identification of the Maastricht-Belvédère finds as hematite pushes the use of red ochre by (early) Neandertals back in time significantly, to minimally 200–250 kya (i.e., to the same time range as the early ochre use in the African record).

Link

Stature of prehistoric Europeans

J Hum Evol. 2011 Dec 22. [Epub ahead of print]

Stature estimation from complete long bones in the Middle Pleistocene humans from the Sima de los Huesos, Sierra de Atapuerca (Spain). 

Carretero JM, Rodríguez L, García-González R, Arsuaga JL, Gómez-Olivencia A, Lorenzo C, Bonmatí A, Gracia A, Martínez I, Quam R.

Abstract Systematic excavations at the site of the Sima de los Huesos (SH) in the Sierra de Atapuerca (Burgos, Spain) have allowed us to reconstruct 27 complete long bones of the human species Homo heidelbergensis. The SH sample is used here, together with a sample of 39 complete Homo neanderthalensis long bones and 17 complete early Homo sapiens (Skhul/Qafzeh) long bones, to compare the stature of these three different human species. Stature is estimated for each bone using race- and sex-independent regression formulae, yielding an average stature for each bone within each taxon. The mean length of each long bone from SH is significantly greater (p < 0.05) than the corresponding mean values in the Neandertal sample. The stature has been calculated for male and female specimens separately, averaging both means to calculate a general mean. This general mean stature for the entire sample of long bones is 163.6 cm for the SH hominins, 160.6 cm for Neandertals and 177.4 cm for early modern humans. Despite some overlap in the ranges of variation, all mean values in the SH sample (whether considering isolated bones, the upper or lower limb, males or females or more complete individuals) are larger than those of Neandertals. Given the strong relationship between long bone length and stature, we conclude that SH hominins represent a slightly taller population or species than the Neandertals. However, compared with living European Mediterranean populations, neither the Sima de los Huesos hominins nor the Neandertals should be considered 'short' people. In fact, the average stature within the genus Homo seems to have changed little over the course of the last two million years, since the appearance of Homo ergaster in East Africa. It is only with the emergence of H. sapiens, whose earliest representatives were 'very tall', that a significant increase in stature can be documented. 

Link

Of Elephants and Men

The same team described dental remains from Qesem cave.

The press release:

The elephant, a huge package of food that is easy to hunt, disappeared from the Middle East 400,000 years ago -- an event that must have imposed considerable nutritional stress on Homo erectus. Working with Prof. Israel Hershkovitz of TAU's Sackler Faculty of Medicine, the researchers connected this evidence about diet with other cultural and anatomical clues and concluded that the new hominids recently discovered at Qesem Cave in Israel -- who had to be more agile and knowledgeable to satisfy their dietary needs with smaller and faster prey -- took over the Middle Eastern landscape and eventually replaced Homo erectus.

The findings, which have been reported in the journal PLoS One, suggest that the disappearance of elephants 400,000 years ago was the reason that modern humans first appeared in the Middle East. In Africa, elephants disappeared from archaeological sites and Homo sapiens emerged much later -- only 200,000 years ago.

It would be useful to get something more substantial than teeth to estimate the presence of a new hominin lineage as proposed by the authors. In their earlier work they noted some Neandertal traits in their teeth sample, although, on balance, they linked the Qesem pre-200ka teeth with the much later modern humans from the Levant. The 400ka date is (roughly) when geneticists tell us modern humans and Neandertals had already began to diverge genetically.

Neandertal-like traits have been noted in European hominins (such as Atapuerca) well in advance of this age. A priori, the idea that the common ancestor of modern humans and Neandertals lived in the Near East seems attractive to me, since that is the area where the demarcation line between the two species appears to have been. While the authors' theory about the disappearance of elephants and the emergence of the Acheulo-Yabrudian merits attention, I don't think the evidence for it is strong enough yet.

PLoS ONE 6(12): e28689. doi:10.1371/journal.pone.0028689

Man the Fat Hunter: The Demise of Homo erectus and the Emergence of a New Hominin Lineage in the Middle Pleistocene (ca. 400 kyr) Levant

Miki Ben-Dor et al.

The worldwide association of H. erectus with elephants is well documented and so is the preference of humans for fat as a source of energy. We show that rather than a matter of preference, H. erectus in the Levant was dependent on both elephants and fat for his survival. The disappearance of elephants from the Levant some 400 kyr ago coincides with the appearance of a new and innovative local cultural complex – the Levantine Acheulo-Yabrudian and, as is evident from teeth recently found in the Acheulo-Yabrudian 400-200 kyr site of Qesem Cave, the replacement of H. erectus by a new hominin. We employ a bio-energetic model to present a hypothesis that the disappearance of the elephants, which created a need to hunt an increased number of smaller and faster animals while maintaining an adequate fat content in the diet, was the evolutionary drive behind the emergence of the lighter, more agile, and cognitively capable hominins. Qesem Cave thus provides a rare opportunity to study the mechanisms that underlie the emergence of our post-erectus ancestors, the fat hunters.

Link

Loss of air sacs and hominin speech

Journal of Human Evolution
doi:10.1016/j.jhevol.2011.07.007

Loss of air sacs improved hominin speech abilities
Bart de Boer

Abstract
In this paper, the acoustic-perceptual effects of air sacs are investigated. Using an adaptive hearing experiment, it is shown that air sacs reduce the perceptual effect of vowel-like articulations. Air sacs are a feature of the vocal tract of all great apes, except humans. Because the presence or absence of air sacs is correlated with the anatomy of the hyoid bone, a probable minimum and maximum date of the loss of air sacs can be estimated from fossil hyoid bones. Australopithecus afarensis still had air sacs about 3.3 Ma, while Homo heidelbergensis, some 600 000 years ago and Homo neandethalensis some 60 000 years ago, did no longer. The reduced distinctiveness of articulations produced with an air sac is in line with the hypothesis that air sacs were selected against because of the evolution of complex vocal communication. This relation between complex vocal communication and fossil evidence may help to get a firmer estimate of when speech first evolved.

Link

MCLUST analysis of Mounier et al. (2011) data

I have recently updated my MCLUST analysis of the classical Howells craniometric dataset. Unfortunately, paleoanthropological data are not easy to come by, but the new paper by Mounier et al. (2011) presents scored morphological data on 50 traits for 36 important paleoanthropological specimens.

I began by filling missing values: I used the median of each trait when that was the case. Subsequently, I ran multidimensional scaling on the Euclidean distance matrix, followed by MCLUST on the resulting scalar representation. The number of clusters varied between 4-6, depending on how many dimensions were retained, but was overwhelmingly 4 across dimensions, so I consider 4 groups to be the most stable solution supported by the data.

In the first two dimensions we see a figure quite similar to that for geometric morphometrics in the Mounier et al. paper, with the first dimension contrasting modern humans (right) with archaics (left), and the second dimension contrasting Neandertals (top) with the rest.

The third dimension contrasts Dali (top) from East Asia with the extremely old D2700 from Dmanisi (Georgia).

The MCLUST results are mostly as expected, these are posterior probabilities of assignment of each specimen to each of four clusters; I've labeled the clusters a posteriori based on the skulls that were assigned to them.

The dendrogram of the centroids of the four components matches that presented by Mounier et al.

Discover News covers this paper by claiming that it reinforces the idea that H. heidelbergensis was ancestral to modern humans and Neandertals. I don't think that's borne out by the data, and even the paper does not make that claim, being concerned more with establishing H. h as a valid taxon.

An inspection of the first two MDS dimensions, in addition to the figures of the Mounier et al. paper really makes it clear that both Neandertals and modern humans cannot be very reliably routed to preceding samples. Perhaps there is a hint of that for Steinheim and Sima de los Huesos 5, but none at all for modern humans. Kabwe 1 is clearly not particularly modern or more related to modern humans than any of the other early skulls, so the idea that it could belong to the ancestral lineage that gave rise to Omo must be retired.

Modern humans seem to emerge out of thin air 200-100ky in East/North Africa and West Asia, and Skhul V, Qafzeh 9 (West Asia), Omo II (Ethiopia), Singa (Sudan), LH 18 (Tanzania), and Irhoud 1 (Morocco) all appear to be closely allied to the modern group. Where/how our species emerged, and which are the forms leading to it remain open questions.

Homo heidelbergensis and the Ceprano calvarium

The type specimen of Homo heidelbergensis is the Mauer mandible. There is considerable controversy about the validity of this taxon, with some "stretching" it to include many different fossils from Europe, Asia, and Africa, while others limiting it to the pre-Neandertal population of Europe. There are also those who want to get rid of H. h altogether.

What constitutes the hypodigm Homo heidelbergensis? The Mauer mandible is insufficient for a definitive description of the species, as it is, well, just a mandible. A new paper suggests that the Ceprano calvarium from Italy is the "counterpart" of the Mauer mandible and can be used to complete the description of the taxon.

Personally, I'm not that invested in taxonomy. The sequencing of the Neandertal and Denisova Cave genomes suggests that modern humans were interfertile with archaic specimens that have been assigned to a different species on morphological grounds. So, if one adopts an evolutionary species perspective, it's hard to argue against those who've maintained that a single species within the genus Homo has existed long before the emergence of so-called "anatomical modernity" and Homo sapiens in the anatomical sense.

Also, the fact that interfertility of moderns with "archaics" has been proven true twice in two DNA-tested fossils has led me to recognize that all fossil hominids are relevant to the story of human origins. It may very well be true that modern humans share synapomorphies not shared by the "archaics" (and the current paper reinforces that idea), but it is not clear how they came to share these synapomorphies: by dispersal of an originally geographical circumscribed tribe (as Out-of-Africa holds) or by homogenizing gene flow between distant populations of a single Homo sapiens species.

I will sidestep all issues of taxonomy, and go right to the core of the paper which is quite interesting in itself. The auhors used a combination of geometric morphometrics and scored morphological traits to place Ceprano in the proper context.

The discriminant function analysis based on geometric morphometrics is shown on Figure 1 (left).

F1 seems correlated with time, with the Early Pleistocene samples (including Ceprano) on the left, Neandertals in the middle, and modern humans on the right. Even within the modern human "reds", the more recent Holocene samples dominate the right-most edge, suggesting that the process that brought us modern humans has continued within the sapiens lineage itself.

Neandertal specificity is captured by F2, with Neandertal groups aggregating in the bottom of the Figure.

Of particular interest are the non-red points (that are not assessed a priori as modern humans) that cluster, nonetheless, with moderns. These include: Singa from Sudan, LH 18 from Tanzania, Irhoud 1 from Morocco, and, most surprisingly, the quite old Steinheim skull from Germany. I also find it interesting that Rhodesian Man (Kabwe 1), often cited as a possibly African precursor to sapiens is not closer to the modern group than Sima de los Huesos 5, nor is the Dali skull from the far east particularly modern. Jinniu Shan, on the other hand is in the middle of the Neandertal cluster, which is interesting as it's from a region well to the east of the normally considered Neandertal range.

Turning to the morphological features, modern humans seem to be quite specific again compared to the other groups (red), and Omo II, the most archaic of the Omo skulls, earliest anatomically modern humans is assigned to the modern branch. In black are samples often assigned to Homo heidelbergensis, in blue the Neandertals.

Interestingly, 39 morphological traits are associated with modern humans (out of a total of 50), and this seems to confirm the quite distinctive nature of modern humans in comparison to other human groups that preceded them.

The full dendrograms are also quite interesting, expanding on the various modern human skulls that are summarized by letters in the above figure. Skhul 5 from the Levant joins Irhoud 1 and Omo II, and these are skulls that will usually be classified as modern but with substantial archaic traits.

In conclusion, I'd say that H. heidelbergensis seems to be a valid taxon but I don't quite see how a strong argument can be made that it gave birth to modern humans in Africa and Neandertals in West Eurasia. Both these species have a number of synapomorphies that cannot really be rooted on heidelbergensis variation in their respective regions. The emergence of Homo sapiens does appear to be a punctuational event, but whether this occurred as part of a migration or species-wide selection process remains to be seen.

Related:

• Study of Apidima 2 skull
• Is Homo heidelbergensis a distinct species?
• Fossil evidence for the origin of Homo sapiens

PLoS ONE 6(4): e18821. doi:10.1371/journal.pone.0018821

The Stem Species of Our Species: A Place for the Archaic Human Cranium from Ceprano, Italy

Aurélien Mounier, Silvana Condemi, Giorgio Manzi

Abstract

One of the present challenges in the study of human evolution is to recognize the hominin taxon that was ancestral to Homo sapiens. Some researchers regard H. heidelbergensis as the stem species involved in the evolutionary divergence leading to the emergence of H. sapiens in Africa, and to the evolution of the Neandertals in Europe. Nevertheless, the diagnosis and hypodigm of H. heidelbergensis still remain to be clarified. Here we evaluate the morphology of the incomplete cranium (calvarium) known as Ceprano whose age has been recently revised to the mid of the Middle Pleistocene, so as to test whether this specimen may be included in H. heidelbergensis. The analyses were performed according to a phenetic routine including geometric morphometrics and the evaluation of diagnostic discrete traits. The results strongly support the uniqueness of H. heidelbergensis on a wide geographical horizon, including both Eurasia and Africa. In this framework, the Ceprano calvarium – with its peculiar combination of archaic and derived traits – may represent, better than other penecontemporaneous specimens, an appropriate ancestral stock of this species, preceding the appearance of regional autapomorphic features.

Link