Archaic Hominin Genetics Galore

tl/dr: The first modern humans left Africa at least 100,000 years ago and modern humans have admixed with at least three archaic hominin species since then (once in Africa with the Pygmies, one or more times with Neanderthals and all populations that reached Eurasia in prehistoric times, and once with Denisovans in Asia with most traces of that admixture on the far side of the Wallace line).

It remains unclear why there are discrepancies between many genetic based estimates of the common ancestors of non-African modern humans that tend to show dates almost half as old, and evidence from archaeology and recent Altai Neanderthal DNA analysis.

* All modern humans cluster together as a clade separate from other species of Great Apes, and various clades of Great Apes have comparable levels of Y-DNA and mtDNA diversity.  All archaic hominins, of course, would also cluster with modern humans in the same clade if they were included (which they were not in the linked study discussion).

* Modern humans genetic introgression into the ancestors of the Altai Neanderthals (but not the ancestors of the European Neanderthals or Denisovans for whom we have ancient DNA) took place ca. 100,000 years ago. As the abstract of the paper explains:

It has been shown that Neanderthals contributed genetically to modern humans outside Africa 47,000–65,000 years ago. Here we analyse the genomes of a Neanderthal and a Denisovan from the Altai Mountains in Siberia together with the sequences of chromosome 21 of two Neanderthals from Spain and Croatia. We find that a population that diverged early from other modern humans in Africa contributed genetically to the ancestors of Neanderthals from the Altai Mountains roughly 100,000 years ago. By contrast, we do not detect such a genetic contribution in the Denisovan or the two European Neanderthals. We conclude that in addition to later interbreeding events, the ancestors of Neanderthals from the Altai Mountains and early modern humans met and interbred, possibly in the Near East, many thousands of years earlier than previously thought.

Kuhlwilm, et al., "Ancient gene flow from early modern humans into Eastern Neanderthals", Nature (2016).

This is the first direct evidence that Neanderthal-modern human admixture was a two way street. I am among those who think that the transitional Châtelperronian archaeological culture of Neanderthal communities is indirect evidence of the intellectual and cultural influence of hybrid individuals in Neanderthal tribes.

New archaeological evidence from Southeast Asia, Arabia and India has for several years added to evidence from the Levant (the Skhul and Qafzeh hominids) that the initial modern human "Out of Africa" migration took place more than 100,000 years ago and has similarities to modern human archaeological cultures of Sudan, reached India prior to 75,000 years ago, and reached Southeast Asia at least 65,000 years ago. The best estimates for modern human arrival in Australia and Papua New Guinea are ca. 55,000 years ago.

Hominin bones from a small number of finds in China indicate that modern humans or hybrids of modern humans and archaic hominins may have existed there as early as 100,000 years ago, but no ancient DNA has been recovered from those locations and I am still not very confident of that dating of those remains, in part, because some of the finds predate modern archaeological dating methodology and, in part, because there isn't any meaningful corroboration from artifacts found accompanying the remains in that time period (which should greatly outnumber modern human bones at any given site). Some evidence of more recent archaic hominin or hybrid individuals during the Upper Paleolithic era seem somewhat more credible, however, since the finds are more recent and presumably used modern dating methods and because H. Florensis and African data discussed below provide evidence of parallel instances in which relict populations of archaic hominins survived long after most of their species went extinct.

But, three separate lines of genetic evidence have favored a younger date: (1) the genetic evidence used to estimate the most recent common ancestor of all men with Y-DNA derived from Y-DNA CF and Y-DNA D with mutation rate estimates fortified by ancient DNA, (2) the genetic evidence used to estimate the most recent common ancestor of all persons with mtDNA derived from mtDNA M and mtDNA N with mutation rate estimates fortified by ancient DNA, and (3) linkage disequilibrium based estimates of Neanderthal admixture in ancient DNA have all pointed to an Out of Africa origin from ca. 50,000-65,000 years ago, suggesting a coincidence of the Upper Paleolithic technologies adopted by modern humans and the source population of all modern humans.

Our interpretation of those uniparental lineages is likewise impacted by a new study of 55 Upper Paleolithic ancient DNA samples which establish that mtDNA M, both of which are exclusively Asian uniparental haplogroups today, were present in Europe prior to the Last Glacial Maximum (earlier ancient DNA results have also established that Asian Y-DNA haplogroup C was present in Europe in this era). That paper is Cosimo Posth et al., "Pleistocene Mitochondrial Genomes Suggest a Single Major Dispersal of Non-Africans and a Late Glacial Population Turnover in Europe"(Current Biology 2016). The abstract notes that: "Demographic modeling not only indicates an LGM genetic bottleneck, but also provides surprising evidence of a major population turnover in Europe around 14,500 years ago during the Late Glacial, a period of climatic instability at the end of the Pleistocene." Apparently, mtDNA M women didn't make it into glacial era refugia in sufficient numbers to remain in the gene pool over the many thousands of years during which most of Europe was covered with a thick layer of ice.

Models Mesolithic and early Neolithic population genetics will also be enhanced by the imminent arrival of Natufian ancient DNA.  The Natufian culture was the last pre-Neolithic culture of the Levant from modern Gaza to Syria ca. 12,500 to 9,500 years ago, and may have engaged in proto-farming of wild type crops and fishing in a sedentary settlement pattern, in addition to hunting and gathering with the assistance of domesticated dogs.  Some commentators have suggested that they may be the historical counterpart for the "basal Eurasian" component identified statistically as a ghost population in whole genome studies of ancient European DNA.

One hypothesis for this disconnect is that a Eurasian population bottleneck makes the most recent common ancestors of modern humans artificially recent, and that LD dates for Neanderthal admixture are capturing only the most recent round of a Neanderthal admixture process that occurred in several stages (a known bias of LD based dating similar to the bias of effective population size estimates towards the lowest historical reproducing population of a species since it arises from a harmonic mean of the reproducing population size of a population).

The alternative, and more widely held view, is that there was an "Out of Africa" event that failed ca. 100,000 years ago or earlier, and that the Out of Africa event that struck coincides with the Upper Paleolithic revolution ca. 50,000 years ago. I personally don't think that this is the most likely possibility, but it is a common one and can fit the data so far.

But, the new evidence of modern human introgression into Altai Neanderthals ca. 100,000 years ago combined with the new archaeological data mentioned above, has effectively ruled out the possibility that the initial Out of Africa event actually took place ca. 50,000 years ago, as many authoritative sources have previously claimed based mostly upon DNA mutation rate evidence and conservatively young dates for modern human arrivals in Europe and Australia.

Rumor has it that genetic evidence of a ca. 100,000 year old component to Sahul (i.e. Australian and Papuan) modern human indigeneous population genetics is common soon as well.

* Updated carbon-14 dating of the youngest Neanderthal sties in Western and Central Europe has established that the extinction of Neanderthals in Western and Central Europe took place much earlier and more rapidly than previously assumed (41,030-39,260 years ago), over about 4,000 years (a roughly 2,600-5,400 year confidence interval).

The timing of Neanderthal disappearance and the extent to which they overlapped with the earliest incoming anatomically modern humans (AMHs) in Eurasia are key questions in palaeoanthropology. Determining the spatiotemporal relationship between the two populations is crucial if we are to understand the processes, timing and reasons leading to the disappearance of Neanderthals and the likelihood of cultural and genetic exchange. Serious technical challenges, however, have hindered reliable dating of the period, as the radiocarbon method reaches its limit at ~50,000 years ago3. Here we apply improved accelerator mass spectrometry 14C techniques to construct robust chronologies from 40 key Mousterian and Neanderthal archaeological sites, ranging from Russia to Spain. Bayesian age modelling was used to generate probability distribution functions to determine the latest appearance date. We show that the Mousterian ended by 41,030–39,260 calibrated years BP (at 95.4% probability) across Europe. We also demonstrate that succeeding ‘transitional’ archaeological industries, one of which has been linked with Neanderthals (Châtelperronian), end at a similar time. Our data indicate that the disappearance of Neanderthals occurred at different times in different regions. Comparing the data with results obtained from the earliest dated AMH sites in Europe, associated with the Uluzzian technocomplex, allows us to quantify the temporal overlap between the two human groups. The results reveal a significant overlap of 2,600–5,400 years (at 95.4% probability). This has important implications for models seeking to explain the cultural, technological and biological elements involved in the replacement of Neanderthals by AMHs. A mosaic of populations in Europe during the Middle to Upper Palaeolithic transition suggests that there was ample time for the transmission of cultural and symbolic behaviours, as well as possible genetic exchanges, between the two groups.

Higham, et al., "The timing and spatiotemporal patterning of Neanderthal disappearance", Nature, (August 21, 2014).

This paper doesn't outright rule out the more recent dates from the Caucasus mountains (ca. 29,000 years ago), but does cast real doubt on those dates given the discovered inaccuracies of dates computed using the same methods elsewhere in Europe.

* We are learning how Neanderthal DNA influences modern humans in observable ways (i.e. their phenotypic impact), which appears to be a mixed bag of good and bad news. Corinne N. Simonti et al., "The phenotypic legacy of admixture between modern humans and Neandertals", Science (February 12, 2016). As the abstract explains:

Many modern human genomes retain DNA inherited from interbreeding with archaic hominins, such as Neandertals, yet the influence of this admixture on human traits is largely unknown. We analyzed the contribution of common Neandertal variants to over 1000 electronic health record (EHR)–derived phenotypes in ~28,000 adults of European ancestry. We discovered and replicated associations of Neandertal alleles with neurological, psychiatric, immunological, and dermatological phenotypes. Neandertal alleles together explained a significant fraction of the variation in risk for depression and skin lesions resulting from sun exposure (actinic keratosis), and individual Neandertal alleles were significantly associated with specific human phenotypes, including hypercoagulation and tobacco use. Our results establish that archaic admixture influences disease risk in modern humans, provide hypotheses about the effects of hundreds of Neandertal haplotypes, and demonstrate the utility of EHR data in evolutionary analyses. 

* A new study also confirms previous results showing that at least one African populations (Pygmies) show genetic evidence of admixture with archaic hominin species in Africa within the last 30,000 years.  The archaic hominin species involved in the admixture event in Africa was not either a Neanderthal or a Denisovan, as direct comparisons with ancient genomes from these species have ruled out that possibility.

This study sheds little or no light by itself, however, regarding the nature of these archaic hominins and limitations on fossil preservation (and a lack of professional archaeological study) in the tropical jungles where Pygmies have lived in historically documented eras reduce efforts to do so to guesswork based upon the more recent archaic hominin remains found in Africa in more favorable preservation conditions.  The extinction of the pygmy languages via language shift to West African farmer languages (mostly or entirely Bantu languages), also impairs efforts to look for linguistic clues regarding these archaic hominin admixture events.

Comparisons of whole-genome sequences from ancient and contemporary samples have pointed to several instances of archaic admixture through interbreeding between the ancestors of modern non-Africans and now extinct hominids such as Neanderthals and Denisovans. One implication of these findings is that some adaptive features in contemporary humans may have entered the population via gene flow with archaic forms in Eurasia. Within Africa, fossil evidence suggests that anatomically modern humans (AMH) and various archaic forms coexisted for much of the last 200,000 yr; however, the absence of ancient DNA in Africa has limited our ability to make a direct comparison between archaic and modern human genomes. Here, we use statistical inference based on high coverage whole-genome data (greater than 60×) from contemporary African Pygmy hunter-gatherers as an alternative means to study the evolutionary history of the genus Homo. Using whole-genome simulations that consider demographic histories that include both isolation and gene flow with neighboring farming populations, our inference method rejects the hypothesis that the ancestors of AMH were genetically isolated in Africa, thus providing the first whole genome-level evidence of African archaic admixture. Our inferences also suggest a complex human evolutionary history in Africa, which involves at least a single admixture event from an unknown archaic population into the ancestors of AMH, likely within the last 30,000 yr.

Hsieh et al., "Model-based analyses of whole-genome data reveal a complex evolutionary history involving archaic introgression in Central African Pygmies", Genome Research (February 17, 2016).

Other prior research has also identified a second possible instance of archaic admixture in a modern African population. I read this study as agnostic on the validity of that claim which it does not study.

Similar methods have also identified an unidentified archaic hominin species that introgressed into the Denisovan genome (parsimony would favor an identification with H. Erectus for that component, although parsimony has not been a particularly fruitful principal in developing accurate pictures of archaic admixture so far).

But, it looks increasingly likely that there are no more than seven archaic hominin species for which genomic data may ultimately be found (Neanderthals, Denisovans, the archaic contributor to Denisovans, two archaic African archaic hominins and possibly H. Florensis and a Chinese archaic species if it is distinct from all of the above and is found from ancient DNA to not be one of the other species above).

Our database of modern and ancient DNA, and the archaeological record, is comprehensive enough to largely rule out additional admixing species that have left us either traces of admixture in modern DNA or ancient DNA samples, although the possibility that there were a few other archaic hominin species that existed in the last 250,000 years that did not admix with modern humans who have descendants alive today, but did leave remains or artifacts from which ancient DNA cannot be extracted is still plausible.  Still, there were probably no more than 10 species of hominins anywhere on Earth in the last 10,000 years.

Razib also notes a related paper putting the split between "Paleo-African" Pygmies and the predominant clade of modern Africans at 95,000-150,000 years ago. (Importantly, Asian Negrito populations are not derived from "Paleo-African" populations whom they resemble phenotypically. This is basically a case of convergent evolution.)

Some recent papers' estimates of the split between Khoi-San hunter-gatherers in African and other Africans at ca. 200,000 years ago (apart from admixture in the historic era), is also quite a bit later than the ca. 70,000 year split estimate for Paleo-African Pygmies and Khoi-San populations that I have previously seen based upon mutation rate dating of uniparental haplogroups found in these populations.

There has been some speculation in the blogs that this very early date based upon whole genomes is also really a methodological artifact of archaic admixture, because modern humans themselves are only 200,000-250,000 years old (see, e.g., the Omo remains in Ethiopia) and there would be many opportunities for admixture in early modern human populations between their speciation and modern times.