Monday, August 7, 2017

The Neanderthal-Denisovan Branch Of Hominins

A new paper on archaic hominins opens with this abstract and an introductory paragraph as follows:
Extensive DNA sequence data have made it possible to reconstruct human evolutionary history in unprecedented detail. We introduce a method to study the past several hundred thousand years. Our results show that (i) the Neanderthal–Denisovan lineage declined to a small size just after separating from the modern lineage, (ii) Neanderthals and Denisovans separated soon thereafter, and (iii) the subsequent Neanderthal population was large and deeply subdivided. They also (iv) support previous estimates of gene flow from Neanderthals into modern Eurasians. These results suggest an archaic human diaspora early in the Middle Pleistocene. 
Around 600 kya, Europe was invaded by large-brained hominins using Acheulean stone tools. They were probably African immigrants, because similar fossils and tools occur earlier in Africa. They have been called archaic Homo sapiens, Homo heidelbergensis, and early Neanderthals, yet they remain mysterious. They may have been ancestors of Neanderthals and modern humans, or ancestors of Neanderthals only, or an evolutionary dead end. According to this last hypothesis, they were replaced later in the Middle Pleistocene by a wave of African immigrants that separated Neanderthals from modern humans and introduced the Levallois stone tool tradition to Europe. To address this controversy, we introduce a statistical method and use it to study genetic data of Africans, Eurasians, Neanderthals, and Denisovans.
Alan R. Rogers, Ryan J. Bohlender and Chad D. Huff. "Early history of Neanderthals and Denisovans" (PNAS August, 2017) doi: 10.1073/pnas.1706426114

The body text explores the mostly likely date of the split of the ancestors of modern humans from Neanderthals, and concludes that the evolutionary dead end hypothesis is not correct:
Our own date estimates inherit the uncertainty of the molecular clock. Using the YRI.CEU data, our point estimate of the Neanderthal–Denisovan separation time is 744 kya. Many authors prefer a higher mutation rate of 5×10^−10 per nucleotide site per year. Under this clock, our estimate becomes 616 kya.
Further along it notes:
[O]ur results also disagree with previous estimates of the Neanderthal–Denisovan separation time. On the other hand, Meyer et al. show that 430 ky-old fossils from Sima de los Huesos, Spain are more closely related to Neanderthals than to Denisovans. This implies an early separation of the two archaic lineages. Our own estimate—25,660 generations, or 744 ky—is earlier still. It is consistent with the results of Meyer et al.  but not with those of Prüfer et al., as discussed above. The cause of this discrepancy is unclear. Prüfer et al. use the pairwise sequentially Markovian coalescent (PSMC) method, which may give biased estimates of separation times in subdivided populations. 
Our results shed light on the large-brained hominins who appear in Europe early in the Middle Pleistocene. Various authors have suggested that these were African immigrants. This story is consistent with genetic estimates of the separation time of archaics and moderns. Our own results imply that, by the time these hominins show up in European archaeological sites, they had already separated from Denisovans. This agrees with Meyer et al., who show that the hominins at Sima de los Huesos were genetically more similar to Neanderthals than to Denisovans. It also agrees with Hublin, who argues that Neanderthal features emerged gradually in Europe, over an interval that began 500–600 kya.
How small was the population ancestral to Neanderthals and Denisovans before the regional split of the two species?
During the interval between the two separation events, the ancestral archaic population was apparently very small. Our point estimates of 2N(ND) range from about 100 to about 1,000, with narrow confidence intervals. Following the Neanderthal–Denisovan separation, our results imply a relatively large Neanderthal population, with 2N in the tens of thousands.

Thus, it is increasingly looking like there were at least three waves of hominins Out of Africa and into Eurasia, and there could easily have been as many as six (including two modern human waves, two Homo erectus waves, and a wave associated with Homo floresiensis). It isn't inconceivable that new discoveries could support additional waves of hominin Out of Africa migration, although there is really no evidence to support that at this time.

Also, our time resolution degrades as we get into the more remote past. For example, it would be almost impossible to determine if the Homo erectus wave was really a single migration, or was actual several migrations spaced 25,000 to 50,000 years apart from each other. What looks like it might have been two waves of modern humans leaving Africa from our vantage point, would look like a single wave of migration if we were looking at the evidence from a vantage point a million years in the future.

Wave One: Homo Erectus

The first hominin Out of Africa wave occurred about 1,900,000 years ago with Homo erectus. Some of the Homo erectus who stayed in Africa probably evolved into an archaic hominin species which is the common ancestor of modern humans, Neanderthals and Denisovans. (Homo ergaster is now mostly seen as a primitive and transitional species directly ancestral to and arguably part of the species Homo erectus, which in turn probably evolved from Homo habilis.)
Early African Homo erectus fossils (sometimes called Homo ergaster) are the oldest known early humans to have possessed modern human-like body proportions with relatively elongated legs and shorter arms compared to the size of the torso. These features are considered adaptations to a life lived on the ground, indicating the loss of earlier tree-climbing adaptations, with the ability to walk and possibly run long distances.
The spread of Acheulian stone tool technology, which was not possessed by the first Homo erectus to leave Africa, suggests that around 1,500,000 to 1,400,000 years ago, there was a secondary wave either of a second wave of Out of Africa migrating Homo erectus, or of cultural diffusion between Homo erectus of stone tool technology from Africa.
Current thinking is that Acheulian technology originated in East Africa (possibly West Turkana, Kenya) at least 1.76 million years ago (Ma), that it became distributed somewhat widely across Africa (e.g., Vaal River Valley and Gona) at ∼1.6 Ma, and then spread to the Levant at ∼1.4 Ma, South Asia at 1.5–1.1 Ma, and Europe at 1.0–0.9 Ma. The 0.8–0.9 Ma Acheulian stone stools from South and central China suggest that Acheulian technology arose in China at least during the terminal Early Pleistocene. However, there are only a few sites with in situ Acheulian artefacts from North China with ages ranging from the late Mid-Pleistocene to the Late Pleistocene. [Ed. Later the paper dates the oldest sites in North China to 0.9 Ma.]
From this paper (with citations to the literature from 1993 through 2014 omitted).

Wave Two: Proto-Neanderthal-Denisovan

The second hominin Out of Africa wave occurred around 745,000 to 600,0000 years ago that gave rise to a common Neanderthal-Denisovan lineage (which was probably synonymous with Homo heidelbergensis) that in turn split into two regional branches. The lineage ancestral to modern humans (who became a distinct species about 300,000 to 200,000 years ago) was not distinct from the lineage ancestral to Neanderthals and Denisovans at that point.

In this scenario, the Levallois stone tool tradition in Europe was a local Neanderthal development in the Middle Pleistocene, that was apparently not shared with or paralleled by the Denisovan hominins from whom they had separated hundreds of thousands of years before, perhaps because their smaller effective population impeded their ability to improve upon the Acheulian stone tools they used when they left Africa and then split from the Neanderthals.

What About The Denisovan?

The dog that isn't barking in this hypothesis is the Denisovan lineage which appears to have migrated to the east, relative to Neanderthals.

We have extensive fossil and archaeological tool evidence of the Neanderthal branch of the Homo heidelbergensis tree, and pretty good evidence of the Homo sapiens branch. But, we have only the slightest evidence of what the Denisovan lineage, which apparently did not see the population expansion that the proto-Neanderthals did, was doing for 400,000 or more years between their separation from Neanderthals and their admixture with modern humans ancestral to Papuan and Australian modern humans.

What was the Denisovan range?  How was the Denisovan range impacted by the pre-existing Homo erectus population? Did the Denisovan people replace Homo erectus in fairly short order, or did they co-exist with them?

Are the oldest hominin remains in China that aren't clearly Homo erectus really Denisovans (perhaps highly evolved from the time they left Africa)? Or, are they hybrids of modern humans and Denisovans?

Or, are they some other branch of the hominin tree entirely (e.g. highly evolved Homo erectus or a previously entirely unknown archaic hominin species from Africa), with or without modern human admixture?

This final option puts pressure on the principle of parsimony, since it would require either another wave of Out of Africa hominin migration with no obvious African candidate, or in situ evolution not demonstrated with transitional fossils anywhere in a 1.5 million year plus time span. But, parsimony has not been a terribly reliable principle for investigators looking at hominin evolution in recent years.

What about Homo floresiensis?

In particular, there are fairly strong indications that Homo floresiensis may actually have been either a different more primitive hominin species than Homo erectus, perhaps a close relation of Homo habilis who evolved ca. 2,400,000 years ago (about 400,000 years before Homo erectus, but overlapping with it for about 600,000 years in Africa) and is the oldest definitively identified member of the genus Homo.

Homo habilis was more adapted for a life in the trees (as opposed to walking longer distances on the ground) than Homo erectus, used more primitive stone tools than Homo erectus, and while also an omnivorous meat eater had a diet that was more plant heavy and lighter on meat than Homo erectus who ate "some tougher foods like leaves, woody plants, and some animal tissues, but that they did not routinely consume or specialize in eating hard foods like brittle nuts or seeds, dried meat, or very hard tubers." Homo erectus used fire (although it isn't clear just how much mastery they had over it) while Homo habilis did not - which would have encouraged Homo habilis to live in places not easily razed by intentionally set forest and brush fires (a key tool used by Australian Aborigines to defeat impressive Australian megafauna).

Homo habilis averaged 3 foot 4 inches to 4 foot 5 inches and averaged about 70 pounds, consistent with Homo floresiensis which averaged about 3 foot 6 inches. In contrast, Homo erectus had body proportions similar to modern humans an averaged 4 foot 9 inches to 6 foot 1 inch, and averaged about 88-150 pounds.

So, it is possible to image that Homo erectus and Homo habilis could have co-existed in different ecological niches in Asia, with Homo habilis favoring dense Asian jungles, while Homo erectus favored lightly wooded area and other more open spaces similar to the African savannah which may have been favored by their ancestors.

Homo floresiensis or its ancestors, could have been a fellow traveler with Homo erectus or Homo heidelbergensis, or may have arrived in a separate Out of Africa migration of its own.

Oldowan stone tools, normally associated with Homo habilis in Africa, are found in Asia from very ancient times until about 200,000 to 300,000 years ago.

The earliest hard evidence of Homo floresiensis is only about 190,000 years old on the island of Flores (implying that "Hobbits" still left Africa well before the earliest modern human departure from Africa in any scenario), but this could simply be due to a lack of well preserved evidence of them in mainland Asia and island Southeast Asia to the west of the Wallace line.

There is a wide time frame in which the small population of Homo habilis-like hominins necessary to give rise to the relict population that survived until after modern humans evolved on Flores, could have left Africa (really any time from 2,400,000 years ago to 200,000 years ago).

But, a migration in the roughly 500,000 year long pre-Homo erectus migration time period would seem to make the most sense. The youngest Homo habilis remains found in Africa date to 1,400,000 years ago reducing the likelihood of a migration of a relict population long after that date, but after Homo erectus left Africa, Homo habilis would face tough competition in Eurasia.

Still, once out of Africa and past the Middle East, there would have been some places in Asia where a small Homo habilis population could have survived competition with Homo erectus. Their best strategy may have been to stay out of the way of the larger members of genus Homo, such as in jungles better suited to smaller hominins.

Most importantly, Homo floresiensis could not have been the source of Denisovan ancestry in modern humans in Papua New Guinea and Australia, even though the only location where their remains are observed is perfectly located to fit the distribution of Denisovan ancestry in modern humans.

Some Wild Speculations About A Hobbit/Denisovan/Homo Erectus Pre-History Narrative

Indeed, speculatively, the appearance of Homo floresiensis on the island of Flores around 190,000 years ago could have been the culmination of their desperate flight from the Denisovans, leading the Hobbits to take a chance on driftwood rafts across the strait to Flores, a trip that the predatory Denisovans weren't willing to risk. Perhaps Denisovans, as they arrived in Southeast Asia were sufficiently smart and versatile to pose a genocidal threat to the Hobbits, even in their jungle-like environments which had protected them in the past because these environments were less well suited to Homo erectus, who also had less of an edge in intelligence over the Hobbits and were more rigid and ecologically inflexible than the Denisovans.

This scenario also puts Denisovans in the right place, at the right time to explain the geographic pattern of their introgression into modern humans, while making their arrival recent enough and brief enough (assuming that all of the Denisovans were in turn dispatched or assimilated by modern humans) that we would not expect them to leave much of an archaeological trace in Southeast Asia.

This scenario also coincides fairly well with a time period in which there are relatively few traces of Homo erectus in Asia. About 300,000 to 200,000 years ago, stone tools made with the Oldowan technology, previously associated with Asian Homo Erectus and with African Homo habilis disappear. If Denisovans had a lighter archaeological footprint than Homo erectus, one would expect a gap in the hominin archaeological record during a period in which Denisovans partially or entirely replaced Asia's Homo erectus population. The last Homo erectus remains date to 143,000 years ago in Indonesia which would have been the last frontier in a wave of Denisovan expansion if this narrative bears any resemblance to reality.

The appearance of Acheulian tools in China around 800,000 to 900,000 years ago, could coincide with the arrival of the first Denisovans in Asia, who may have co-existed with Homo erectus (and perhaps Homo habilis as well) for about 500,000 years or more in Asia.

The lack of Acheulian tools in Asian Homo erectus (at least until the Denisovans arrive in Asia) unlike Homo erectus in Africa, Europe and South Asia who made this innovation much earlier (and before the migration of Homo heidelbergensis out of Africa) may have also made it possible for Homo habilis to avoid the extinction at the hands of Homo erectus that it experienced in Africa where the adoption of Acheulian tools by Homo erectus/ergaster and the demise of Homo habilis come fairly close in time.

A Denisovan surge, after hundreds of thousands of years to the north of Homo erectus territory and perhaps co-existing with Homo erectus in China, might reflect some paradigm shifting cultural innovation that the Denisovan's developed around that time in lieu of the Levallois stone tool tradition developed around that time by their Neanderthal cousins in Europe. This unspecified cultural innovation may have given them an edge in hunting and warfare compared to their previous, rather marginal selective fitness in Eurasia that finally made them clearly superior to both Homo erectus and Homo habilis who might have been found, until then, in different ecozone of Asia.

Perhaps this Denisovan breakthrough that finally allowed them to become dominant was an innovation with a light archaeological footprint such as something comparable to the development of bamboo weapons, or frog poison blow darts, or an advance in language abilities, as opposed to more advanced stone tools than they had from the outset. Or perhaps, the break through was a matter not of technology, but of a major climate event that the more intelligent Denisovans managed to survive better than the duller and more rigid Homo erectus and Homo habilis.

Perhaps, by the time modern humans arrived in Asia, the Denisovan has brought about the extinction of Homo erectus and Homo habilis in all but a few small relict communities in Asia, a favor that modern humans returned by causing the extinction and/or assimilation of all of the remaining Denisovans around 75,000 to 65,000 years ago, or perhaps earlier, with an initial boost created by the ecological disruption arising from the Toba super volcano explosion.

Wave Three: Modern Humans

A third hominin Out of Africa wave brought Homo sapiens, with a first Homo sapien Out of Africa wave about 125,000 to 100,000 years ago and possibly with a second wave of Homo sapiens to leave Africa about 75,000 to 60,000 years ago. It isn't clear if the second Homo sapiens Out of Africa wave is derived from the first Homo sapiens Out of Africa wave, or if the second Homo sapiens Out of Africa wave was separate from the first, with the first wave being largely a dead end leaving only some Middle Eastern relics and some admixture of ancestors of the Altai Neanderthals. We have very little evidence to guide us one way or the other.

Loose ends in Africa

It is fairly likely that other archaic hominin species with admixed with modern humans within Africa who can only be identified as "ghost populations" in African whole genomes right now may also have arisen from this Homo heidelbergensis lineage as well with one study noting that: "On the basis of an excess of shared derived alleles between San, Neanderthal, and Denisova we suggest that a third archaic population related more closely to Neanderthal and Denisova than to modern humans introgressed into the San genomes studied here." The admixture with the San probably took place in the last 100,000 years.

There was also probably another archaic admixture, possibly with a different "ghost species" in Africa, that impacted the African Pygmy genome.

An unknown archaic species that broke off from the lineage that includes Homo heidelbergensis about 3,450,000 years ago (quite possibly, given the timing, the pre-Homo species affectionately known as "Lucy" a.k.a. Australopithecus afarensis or Australopithecus africanusfor whom 3.45mya is a bit of a stretch, but which persists much later than Lucy) may have introgressed into a quite basal version of Homo heidelbergensis.

Homo naledi in Southern Africa is a recently discovered diminutive species of archaic hominins that still existed when modern human evolved (those found are from 300,000 to 200,000 years ago), although their remains suggest that they are part of a fairly archaic and basal branch of the human evolutionary tree, with estimates based upon how archaic its features were in the range of 2,500,000 to 912,000 years ago.

Homo rudolfensis known from only one decent set of remains from about 1,850,000 years ago that was discovered in Kenya in 1986 seems similar to Homo habilis but with a larger brain case. It isn't clear exactly where this specimen belongs in the evolutionary tree.

Other Archaic Hominin Stories

In other archaic hominin news, John Hawks muses over why stable hybrid zones apparently didn't emerge between Neanderthals, Denisovans and modern humans respectively.

As the above discussions suggest, however, even if stable hybrid zones didn't emerge in Eurasia, they probably did exist for some extended periods of time in parts of Africa, where hominins originated and hominin populations were larger. Some of the populations in Eurasia may have been too greatly diverged from each other, and too small in effective population size themselves, to give rise to reasonably sized stable hybrid populations.


Matty K said...

Great summary, thanks

andrew said...

It looks like hobbits were in Flores much earlier than I supposed in this post, so that bit needs to be tweaked.