climate

Bornean and Sumatran orangutans are the most highly divergent subspecies within any of the living species of great apes. The two farther apart even than chimpanzees and bonobos, which are good biological species. The time of the Bornean-Sumatran orangutan divergence as estimated from mtDNA is around 3.5 million years ago.

This is old enough that many primatologists consider the two populations as separate biological species. The species distinction is supported by some aspects of morphology, but as yet we have no good nuclear DNA information about the extent of divergence. In chimpanzees, nuclear genetic comparisons suggest a relatively recent founding of one subspecies and recurrent gene flow between the others, despite high mtDNA divergence between the subspecies. So information from across the genomes of Bornean and Sumatran orangutans may be necessary to substantiate the hypothesis of long isolation suggested by mtDNA.

Within Borneo, different local populations of orangutans have strong genetic differentiation, with few shared mtDNA haplotypes among them. A new study by Natasha Arora and colleagues [1] has provided further detail about these relationships within Borneo. Based on earlier work, they expected to find high population differentiation within Borneo, and that is what they found:

[O]ur analyses revealed high and significant mitochondrial differentiation, with populations within currently recognized subspecies generally displaying as much differentiation as those between subspecies. Of notable interest is the great extent of subdivision and lack of reciprocal monophyly for the morphologically recognized subspecies P. p. morio and P. p. wurmbii. MtDNA haplotype sharing is uncommon and for populations separated by rivers occurs only in two instances: (i) for SA and GP and (ii) for the northern and southern populations across the Kinabatangan river. In both cases, very recent common ancestry could explain the incomplete mtDNA lineage sorting. For North Kinabatangan (NK) and SK, Jalil et al. (27) proposed an expansion from a recent common refugium further west in Mount Kinabalu, as posited for other Bornean species (46, 47, 49). DV, with its low haplotype diversity, might also be the result of a recent range expansion. GP is located proximally to the Bangka–Belitung–Karimata–Schwaner divide, from where orangutans are presumed to have dispersed to the rest of Borneo (12) and where we might expect a rich haplotype diversity. However, the presence of only one mtDNA haplotype shared with populations further east suggests that the current population in GP is recent and/or underwent a severe recent bottleneck. This and other local bottlenecks make it impossible to reconstruct a colonization of Borneo through the southwestern “choke point” (52).

They were able to confirm the relatively strong differentiation of Bornean populations by examining nuclear microsatellites. These do not give a great indication of the time period over which the populations may have developed their differentiation, but the microsatellites do document the relative lack of allele sharing between the populations, attesting a history of low gene flow in the recent past. The populations they identify as strongly differentiated do not correspond entirely with the subspecies recognized along morphological lines, but there are strongly differentiated populations here.

The "news" aspect of the paper is the one unexpected observation: the mtDNA ancestor of Bornean orangutans lived relatively recently, only around 176,000 years ago (with a range of error stretching from 72,000 to 320,000 years ago. The data in the study do not allow us to distinguish whether this was a time when the Bornean population may have been founded, or whether instead the mtDNA lineage spread through pre-existing populations. The authors pursue the hypothesis that Bornean orangutans were limited to a refugium sometime during the early Late Pleistocene:

Assuming that orangutans arrived in Borneo around the same time as gibbons and macaques, the recent coalescence of Bornean orangutans could be explained by a bottleneck through a severe rainforest contraction. Such a bottleneck would have had a more dramatic impact on the mtDNA structure of orangutans compared with other species as a result of their low densities and slow life histories (18) as well as habitat requirements.

The comparison with gibbons and macaques is necessary because both have substantially deeper mtDNA coalescence times within their Bornean populations. If the forest had been substantially reduced to a small area where orangutans could survive, we might expect the other primates to reflect this event -- and they don't. Nevertheless, a grab-bag of climate change scenarios appear next:

Geomorphological and palynological data indicate the presence of dryer, more open vegetation in southern and western Borneo during the last glaciation (2, 41), and by extrapolation also during other glaciations (but c.f. refs. 42, 43). Climate change was especially severe during an extended cold period within the penultimate glaciation between 130 and 190 ka (44, 45), which occurred approximately at the time of mean coalescence of Bornean mtDNA haplotypes. More recently, the last Toba eruption approximately 74 ka resulted in a short, albeit signi␣cant, decrease in regional temperatures, ensued by a 1,800-y cold stadial (9, 10). Our data do not provide clear signals to make conclusive statements about potential Toba effects. Nonetheless, the coldest period of the penultimate glaciation (44, 45) was more prolonged than the cold period following the last Toba eruption, suggesting more severe effects of the former on the extent of rainforest across Sundaland. In any event, suitable rainforest habitat for orangutans should have existed in certain regions in Borneo where a refugium population survived the dry glacial conditions.

A coalescence time of 176,000 years ago does not point to a short-duration bottleneck that began 74,000 years ago. If orangutans in the Middle Pleistocene of Borneo had high genetic differentiation, a crash would have to have been very severe -- eliminating all but one small regional population -- to have effected the present distribution. Still, the great uncertainty in the actual coalescence time leaves open many possibilities, and the refugium hypothesis in the general case is worth testing, even if the Toba eruption in particular cannot explain the data.

Given the uncertainty about the habitat structure of the now-submerged areas of Sunda, we may also want to consider the hypothesis that the present orangutans arrived recently on Borneo from mainland Southeast Asia. Even if orangutans had lived on Borneo during the Middle Pleistocene, they may not have been the current orangutans. Or even better, they may have been Neanderorangs -- an initial population that was genetically swamped by migrants arriving from elsewhere. The deep Sumatra-Borneo divergence means that the Bornean population was probably not recently derived from Sumatra, but that's a very restricted source compared to the Late Pleistocene distribution of orangutans across mainland and island East and Southeast Asia.

Some other animals walked from Sumatra to Borneo repeatedly during the Pleistocene, including humans. In the human case, we know that a large fraction of the genetic ancestry of Bornean and Javan people was derived from Asia within the last 100,000 years -- in other words, Late Pleistocene gene flow. The movement of genes may have happened in the context of a dispersal of Asian (or ultimately, African-derived) populations into island Southeast Asia. The paper includes some discussion of other primate species:

For instance, the south Bornean gibbon Hylobates albibarbis and the Sumatran–Malaysian gibbon Hylobates agilis have a TMRCA of 1.56 Ma (36), and Bornean and Sumatran pig-tailed macaques have one of 3 to 4 Ma (37). By contrast, the Bornean–Sumatran common ancestor of both the silvered langur(39) and clouded leopard (40) is much more recent than that of orangutans, gibbons, and pig-tailed macaques, probably because of a higher ␣exibility in habitat use.

The pig-tailed macaque divergence time is more or less the same as the orangutan divergence; the others are more like the time range for human dispersals into island Southeast Asia. We can add to the primates a few other medium-sized mammals; for example, clouded leopards are highly differentiated between Sumatran and Bornean populations, and their mtDNA divergence occurred sometime after 3 million years ago.

There may be no contradiction between the recent mtDNA common ancestor and the high degree of population structure in Bornean orangutans; the mtDNA could have been selected. We really would want resequencing of a lot more loci in these orangtuan populations, for which we may not have to wait too long. Mitochondrial DNA is convenient in many ways, including its greater sensitivity to restricted population size and higher mutation rate. But the intrinsic variance of a single gene system under genetic drift is so high that this disadvantage probably outweighs all advantages for reconstructing population sizes.

At any rate, the orangutans now provide an additional case where the subspecies-level history of hominoids is more complex than depicted five or six years ago. Uncovering these kinds of dynamics highlights the need for better modeling of demography and dispersal within a geographically widespread species. Isolation-by-distance and long-lasting subspecies are well-defined models, but when they are refuted, we have a lack of well-defined alternatives.

References

I'm reviewing some old viewpoints about the relationships of Neandertals and other peoples. These include mainstream opinions that persisted over decades as well as more idiosyncratic ideas. This is mostly pre-1960 stuff for the time being.

To the extent that old ideas are wrong it is no surprise: Science progresses by rejecting wrong ideas, and paleoanthropologists of the past lacked the luxury of today's data. To the extent that the ideas look familiar, they remind us that our current hypotheses in many instances echo ideas that were advanced fifty years ago or more.

Weckler's model

A bit off the mainstream was a paper published by Joseph E. Weckler [1], titled "The relationships between Neanderthal Man and Homo sapiens." Weckler was a cultural anthropologist who had done fieldwork in the American Southwest and the South Pacific [2]. He wrote only one paper on Neandertals but this received substantial attention, first published in the American Anthropologist and later revised in a simplified version for Scientific American. Weckler was very interested in the migration and dispersal of ancient populations, maybe because of his work on the ethnography of the South Pacific. He brought that perspective to the Neandertals and other ancient groups.

Weckler saw Pleistocene human population dynamics as having been directed by glaciations and geographic barriers. In general, Weckler thought that the pre-modern population had been divided into allopatric species or subspecies. These groups would have been isolated from each other much of the time, but occasionally thrust back into contact by shifts in the climate. During glacial phases, Weckler posited that Europe and Asia north of the Caucusus-Himalaya axis would have been uninhabitable. During warmer interglacials humans moved into these northern areas, where water and mountainous barriers tended to isolate them. The overall pattern was evolutionary differentiation punctuated by occasional hybridization and cultural contact between long-separated groups.

Weckler was not the first to propose that Neanderthal and modern lineages had been relatively isolated and later hybridized. The idea was widespread after the description of the Mount Carmel remains by McCown and Keith [3]. McCown and Keith themselves had favored a different explanation -- that the Skhul and Tabun remains represented a transient between a less specialized and more specialized (Neandertal-like) extreme. Others, including Carleton Coon [4] and Theodosius Dobzhansky [5], immediately favored the idea that the Mt. Carmel sample represented a hybrid population.

Weckler broadened the idea of hybridization into a general theme. He supposed that we might expect recurrent contact during second (Mindel-Riss) interglacial times in Central Asia, and repeated dispersal from India into Southeast Asia throughout the Pleistocene. Thus, hybridization between divergent groups was not a one-time affair but instead was a fundamental aspect of Pleistocene human evolution.

Interglacial population contact

This scenario faced an obvious problem: There were essentially no data to test the hypothesis of population contact at any of these earlier times. Only the third interglacial, already treated by other authors, gave the appearance of sufficient information for a test. To illustrate the plausibility of recurrent exchanges, Weckler fleshed out a third interglacial model of population contact in some detail:

Some of these pre-Neanderthal men wandered inland into Asia north of 40° during a period of warm climate. Part of this population may subsequently have been trapped north of the barrier in the general vicinity of Inner Mongolia or Sinkiang at the onset of the next glacial period. Primitive man caught in this area would have been unable to retreat directly southward because the great mountain mass that lay in that direction became frigid sooner than the lower lands to the north. Having lived where he was for hundreds of generations, primitive man might not have known he could escape the increasingly rigorous climate by moving east several hundred miles before turning south. Howell (1951:409) suggested that some of the physical characteristics of classic Neanderthal man may represent biological adaptation to a glacial climate. Coon stated in a letter to me (1953) that he has long been of that opinion. If this is so, I suggest the evolution occurred, not in Europe during the fourth glaciation, but in eastern Asia during an earlier one (Weckler 1954:1010).

This is an early exposition of the idea that Neandertals repeatedly invaded the west from a homeland somewhere in central Asia or further east. Weckler discussed the idea that these populations originated in northwestern China, but he had no good examples (as indeed there are still no such examples).

Weckler's discussion may seem confused because he accepted Zhoukoudian as an eastern "Neanderthaloid" population. His division of humanity can best be aligned along a "paleanthropic/neanthropic" distinction. Today, we might more simply state his biogeographic model as a shifting border between the paleanthropic "Neanderthaloids" and neanthropic "Homo sapiens" along a shifting Movius line somewhere in India or the Middle East, stretching to northwestern China.

A central Asian source

Teshik Tash bears much importance to Weckler's ideas, as it did to Movius, Howell, Weidenreich, and many others. To those unfamiliar with the site, an interesting place to start is my interview with Mica Glantz. Teshik-Tash is once again central to our ideas of Neandertal biogeography, with the addition of genetic evidence from the juvenile specimen from the site and others in Central Asia.

In the early 1950s, Teshik-Tash raised many of the same issues that it does today. Today, of course, Teshik-Tash is far from alone, with several sites in Central Asia bearing evidence of a local Mousterian, physical remains with Neandertal-like mtDNA sequences. There was great uncertainty about the date represented by the Teshik-Tash specimen. Teshik-Tash had a classic "Western" archaeological industry (in this case, Mousterian) and therefore evidenced long-range population contact with Europe. The East Asian fossil record was known to be very different from the west, raising the question of boundaries. Where did the Western sphere of biological influence end, and the Eastern begin?

Today Denisova Cave, embedding a highly divergent mtDNA clade in an initial Upper Paleolithic assemblage [6], presents the same issues with even greater relief.

Probably the most common interpretation of the Central Asian "Neandertal" sites is that they represent an eastward migration from the Neandertals' center of evolution in Europe. But the opposite hypothesis is an obvious alternative: that the center of Neandertal evolution was somewhere in Central Asia, and that they invaded Europe from outside. Some may see parallels for a Neandertal invasion of Europe from outside, by looking both earlier in evolution (the first Europeans obviously came from somewhere) and later (the Upper Paleolithic, the Neolithic).

Why posit Central Asia in particular as a source area, above and beyond the general idea of invasion? I thought the idea might have originated with Henry Fairfield Osborn because of his long interest in Central Asia as a center of human evolution. For Osborn, Central Asia was a source of humanity, but his "Dawn Man" idea supposed that the modern human form had long resided in Central Asia, with more primitive humans at the periphery. The idea that a Neandertal center of evolution existed in Asia is quite different from Osborn's idea, which was itself a sketch supported by little evidence. I'll have more on Osborn later.

Weckler presented his idea to address a classic problem: To many paleoanthropologists, early Neandertals appeared to be more like later human than were the later, "classic" Neandertals. Howell [7] summed up this observation as follows:

Many features of early Neanderthal morphology, both cranial and postcranial, are incipiently classic Neanderthal. However, the general morphological pattern of these early Neanderthal peoples bore a close resemblance to that of anatomically modern man, a fact which indicates again the special character of classic Neanderthal morphology (Howell 1957:332-333).

The early Neandertals were those from the third interglacial, which during the 1950's would have included those from Krapina, Ehringsdorf, and Saccopastore. Howell's description highlights the most common hypothesis: classic Neanderthals had evolved toward greater and greater specialization over time.

Weckler took a different approach: for him, the fourth glaciation Neandertals descended from already-specialized ancestors, who had existed in Central Asia:

The Asiatic migrants, probably already mixed with Homo sapiens in central Asia in the Middle East, pushed on to central Europe during the third interglacial. They may have moved northwestward from Palestine or directly westward along the north face of the barrier. In the zone of contact in western Asia and eastern Europe further miscegenation and cultural exchange probably occurred. Then, when the climate deteriorated with the onset of the fourth glaciation, the bulk of the Homo sapiens population retreated south as was its wont. This left Europe open to further Neanderthal invasion and set the stage for the modern misconception that classic Neanderthals evolved rapidly (and in a curiously regressive fashion) in western Europe during Würm I. Probably all that actually happened was that additional Neanderthals of more classic type, adjusted by previous experience to life in a cold climate, kept pushing in behind the advance guard and, by weight of numbers, blotted out the neanthropic traits the earlier migrants had acquired along the way.

Weckler proposed this scenario not long after F. Clark Howell's 1952 paper [8], in which Howell had proposed that climate isolated Neandertals within Europe during the last glaciation, leading to their increasing specialization. According to Weckler, the glaciations had not isolated Europe so much as they had wiped clean the evolutionary slate within Europe. After the last interglacial, migration from a central Asian source brought back a purer strain of Neandertal.

Out of this welter of fact and interpretation emerge the few concepts necessary to the hypothesis supported in this paper. By the end of third glacial times Neanderthal had probably developed in eastern Asia to something approximating the classic form. His numbers had probably always been small compared to developing Homo sapiens: his range was incomparably smaller, and in part of this range he had no easy retreat from glacial conditions such as Homo sapiens enjoyed. His restricted range (and possibly his sometimes severe habitat) had militated against the racial diversification that characterized the development of Homo sapiens. In spite of his cultural advances his range and numbers were probably sharply reduced during every glacial episode he had to endure. This may be why, although he stood athwart the entrance to the New World, he never expanded his range sufficiently to explore that territory. But as the climate ameliorated after the rigors of the third glaciation, his numbers increased and he did finally expand his range. For reasons not as yet ascertained he looked westward, and the lowlands north of the barrier afforded him a route to Europe.

Several strains of contemporary thought emerge in Weckler's formulation. Neandertals were always on the edge of extinction, being repeatedly driven to low numbers by deteriorating climate. Their tenuous existence did not allow them to disperse more broadly.

That old Neandertal magic

Where Weckler differed from the received view is in the way he accentuated the Neandertal positives. He wrote that the diversification of humans and Neandertals presented an opportunity to the evolution of our species. From their central Asian source, the Neandertals had acquired innovations necessary for existence in the cold north. Human colonization of these regions might be impossible without the adoption of Neandertal cultural and behavioral innovations:

The Homo sapiens groups that retreated south from Europe and perhaps from central Asia [during the glaciation] had been touched by Neanderthal magic. They may have acquired some Neanderthal physical traits, but, more important, they had achieved a new cultural outlook. They had perhaps learned the use of fire, clothing and specialized hunting techniques, and possibly of cave dwelling -- accomplishments that freed man from dependence on a mild climate and from a grubbing existence (emphasis added).

I find myself reading this on two levels. On the concrete, empirical side, Weckler would soon be proven wrong. Neandertals didn't invent fire; that was much older and more broadly shared by Middle and Late Pleistocene humans. They may have had better clothes for cold weather than contemporaries who lived further south, but the innovations of woven cloth, sewn garments, and shoes happened later. They certainly had specialized hunting techniques, but these were linked to a particular kind of social organization and technology. Later developments in both would have required new hunting (and gathering) methods. None of them lived in caves very often; their experience must have been fairly "grubbing" in either event.

But on the abstract, Weckler presents a scenario where Neandertals had something of value, cultural or physical, without which later humans would have been as successful. He had already posited biological hybridization; here he suggests a kind of "cultural hybridization" as well.

The essential idea I am suggesting is that the contact of Homo sapiens groups with "Neanderthal culture" in Asia and in Europe during the third interglacial resulted in an efflorescence of "Homo sapiens cultures" that gave rise to the Upper Paleolithic. There is general agreement, I think, that a sudden enrichment of culture is evident at the beginning of the Upper Paleolithic in Europe and that these richer and more varied cultures seem to have originated, for the most part, outside of Europe. Movius, discussing the European Upper Paleolithic (1953:171ff.), follows M. Denis Peyrony, Dorothy Garrod, and others in suggesting that different European cultures of that time may have originated in Palestine, Iran, the plains of southern Russia, and possibly Africa. All but the latter are areas where indigenous Homo sapiens was probably directly stimulated during the third interglacial by invading Neanderthal man (Weckler 1954:1016).

So why has this idea been largely forgotten? The failure of the particulars was almost complete:

Leakey claimed in the 1930's that Lower Aurignacian techniques of stone chipping were older in Africa than in Europe (1931:237-39; 1936:54-60, 161). Movius seems ready to dismiss Africa as a source of European Aurignacian (1953:171), but he doesn't dispose of Africa's claim to temporal priority. The sudden new competence Leakey claims for African Aurignacian cultures early in the fourth glaciation (1936:161) may have been the consequence of contact with Neanderthal. The stimulation may have come secondhand from Homo sapiens wanderers returning from Europe or may have resulted directly via diffusion or migration from the Middle East.

He was overreaching here. He didn't overestimate the cultural sophistication of Neandertals, although he did accentuate behaviors, like fire, that would turn out to be less special than he assumed -- older than Neandertals and more broadly shared. More critically, Weckler rested his argument on the absence of evidence for cultural sophistication in the African contemporaries of the Neandertals. But Louis Leakey's earlier claims about an "African Aurignacian" also overreached, supported by a mistaken chronology. A better understanding of the Late Pleistocene African cultural sequence would emerge only later.

When Homo sapiens had thoroughly assimilated and improved on the ideas he got from Neanderthal, he took advantage of the first interstadial of the Würm glaciation to launch forth on his initial conquest of the world. He overran Europe and pushed around the barrier into eastern Asia.... One might even hazard the guess that the reason Africa south of the Mediterranean littoral remained so backward during the Upper Paleolithic was because the Homo sapiens groups there had not had the full benefit of Neanderthal stimulation. In the new dynamics of cultural enrichment and sapiens migrations the hinterlands of Africa had become a dead end, far removed from the centers of rapid development.

I find myself wondering about the nature of "Neanderthal stimulation"....

This passage is worth examination. Most of the details have changed radically since 1954. We now know that MSA Africans had most of the tricks that Neandertals did, and vice-versa. Many MSA industrial innovations predate Mousterian or Middle Paleolithic occurrences. The complexity within Africa may itself represent a vastness of population history that we now can only guess at.

Yet the development of Upper Paleolithic cultural complexity still wants some explanation. The biological innovation of "anatomical modernity" is not sufficient to explain the cultural evolution of the Late Pleistocene -- it does not match the pattern of cultural innovation in time or space.

Bottom line

I think there was some "Neandertal magic." Middle Pleistocene humans were more isolated than present-day populations, for a longer period of time. Less gene flow made it less likely for adaptive traits to spread beyond the population where they originated. Not impossible, just less likely. So any surge of population contact caused by migration would have been accompanied by a surge of introgression of adaptive genes. The evidence for Neandertal contribution to the later gene pool of non-Africans documents one such surge of population contact, but there may well have been others.

Where genes are concerned, this is a simple matter of mathematics, discussed more fully by Greg Cochran and I in our 2006 paper [9]. Simply put, Neandertals and modern humans had comparable selection pressures for many aspects of their biology, similar adaptive responses, and the same time to adapt. Adaptive mutations are chance events, governed by demography and time. If the evolving African MSA population got many new adaptive mutations, Neandertals would have gotten nearly as many (possibly constrained by smaller population size). In a few cases, the same variants would occur in both populations by chance, but in most they would be different. These alleles should still be with us, as the extent of Neandertal contribution to our population was great enough to pick up almost all of them.

But what about Neandertal cultural traits? These were the real focus of Weckler's argument, and here I think the question is very difficult to resolve today. Cultures are ephemeral. As we know from history, if we choose a beginning and end point a few hundred years apart, it can be difficult to show the continuity of cultural information even within a single place.

With the transition from Mousterian, through Châtelperronian into Aurignacian in France and northern Spain -- a place where we have relatively dense archaeological documentation -- we are nevertheless talking about time gaps of hundreds of years. I'm skeptical that we're in a position to test the hypothesis of cultural exchanges across these time periods.

We're in a better position to test the hypothesis of stasis. If genetic exchanges happened in the absence of culture change, that would tell us something very relevant to the relation between gene flow and demographic contact. Likewise, persistent stasis of different cultures in adjacent areas tells us something about the absence of information flow. A kind of regional stasis, over thousands of years, seems to have been the norm in MSA and Middle Paleolithic contexts, and it's not a pattern that we are well-placed to understand without a better understanding of the limits on information exchange. Some of those limits may, in these ancient populations, have been biological constraints. So I'm less confident that we will be able to understand the cultural consequences of Neandertal contact.

References