I should be careful about being flip on this issue. As recently as the mid aughts (see Mutants) the details of this trait were not entirely understood. Today the nature of inheritance in various populations is well understood, and a substantial proportion of the evolutionary history is also known to a reasonable clarity as far as these things go. The 50,000 foot perspective is this: we lost our fur millions of years ago, and developed dark skin, and many of us lost our pigmentation after we left Africa ~50,000 years ago (in fact, it seems likely that hominins in the northern latitudes were always diverse in their pigmentation)
There is the fact of evolution. And then there is the long-standing debate of how it proceeds. The former is a settled question with little intellectual juice left. The latter is the focus of evolutionary genetics, and evolutionary biology more broadly. The debate is an old one, and goes as far back as the 19th century, where you had arch-selectionists such as Alfred Russel Wallace (see A Reason For Everything) square off against pretty much the whole of the scholarly world (e.g., Thomas Henry Huxely, “Darwin’s Bulldog,” was less than convinced of the power of natural selection as the driving force of evolutionary change). This old disagreement planted the seeds for much more vociferous disputations in the wake of the fusion of evolutionary biology and genetics in the early 20th century. They range from the Wright-Fisher controversies of the early years of evolutionary genetics, to the neutralist vs. selectionist debate of the 1970s (which left bad feelings in some cases). A cartoon-view of the implication of the debates in regards to the power of selection as opposed to stochastic contingency can be found in the works of Stephen Jay Gould (see The Structure of Evolutionary Theory) and Richard Dawkins (see The Ancestor’s Tale): does evolution result in an infinitely creative assortment due to chance events, or does it drive toward a finite set of idealized forms which populate the possible parameter space?*
Like many people I’ve been following the tales of the Hobbits of Flores, H. floresiensis, with some interest since 2004. And, like most people I have no personal expertise or skill which is relevant to evaluating whether this putative hominin species actually is a new species (as opposed to a pathological modern human). So how are we to evaluate a new PLOS ONE article which comes down on the side that it is a new species? First, my very vague impression is that over the past ~10 years the new-species camp has been gaining ground on the pathological-modern-human set. But setting all that aside perhaps the critical issue for me is that the likely reality of archaic human admixture into our own lineage means that the world is far stranger than we had thought in 2004. For various anatomical and paleoanthropological reasons H. floresiensiswas implausible. But as implausible as the idea that the genome of a Siberian hominin would yield admixture in modern Papuans?
Addendum: New York Times on the paper in PLOS ONE.
As recently as 10 years ago one could plausibly talk about mtDNA Eve and Y chromosomal Adam. The “Human Story” might then be stylized into a rapid expansion from a small core East African population which flourished ~100,000 years ago, and engaged in a jailbreak sweep out of Africa and across the rest of the World Island, and beyond, to Oceania and the New World. In the process all other human lineages extirpated, marginalized, and eliminated, their culture and genes consigned to oblivion. No longer, the origin of our species may have been characterized by several admixture events with “other” lineages, both within, and outside of, Africa. Instead of a bifurcating tree, imagine a graph with reticulation. A phylogenetic tree with a light, but noticeable lattice scaffold, tying together disparate branches.
There’s an excellent paper up at Cell right now, Modeling Recent Human Evolution in Mice by Expression of a Selected EDAR Variant. It synthesizes genomics, computational modeling, as well as the effective execution of mouse models to explore non-pathological phenotypic variation in humans. It was likely due the last element that this paper, which pushes the boundary on human evolutionary genomics, found its way to Cell (and the “impact factor” of course).
The focus here is on EDAR, a locus you may have heard of before. By fiddling with the EDAR locus researchers had earlier created “Asian mice.” More specifically, mice which exhibit a set of phenotypes which are known to distinguish East Asians from other populations, specifically around hair form and skin gland development. More generally EDAR is implicated in development of ectodermal tissues. That’s a very broad purview, so it isn’t surprising that modifying this locus results in a host of phenotypic changes. The figure above illustrates the modern distribution of the mutation which is found in East Asians in HGDP populations.
One thing to note is that the derived East Asian form of EDAR is found in Amerindian populations which certainly diverged from East Asians > 10,000 years before the present (more likely 15-20,000 years before the present). The two populations in West Eurasia where you find the derived East Asian EDAR variant are Hazaras and Uyghurs, both likely the products of recent admixture between East and West Eurasian populations. In Melanesia the EDAR frequency is correlated with Austronesian admixture. Not on the map, but also known, is that the Munda (Austro-Asiatic) tribal populations of South Asia also have low, but non-trivial, frequencies of East Asian EDAR. In this they are exceptional among South Asian groups without recent East Asian admixture. This lends credence to the idea that the Munda are descendants in part of Austro-Asiatic peoples intrusive from Southeast Asia, where most Austro-Asiatic languages are present.
I have mentioned the PLoS Genetics paper, The Date of Interbreeding between Neandertals and Modern Humans, before because a version of it was put up on arXiv. The final paper has a few additions. For example, it mentions the generally panned (at least in the circles I run in) PNAS paper which suggested that ancient population structure could produce the same patterns which were earlier used to infer admixture with Neandertals (the authors also point to Yang et al. as a support for the proposition of admixture rather than structure). The primary result, dating the admixture between Neandertals and anatomically modern humans ~40-80,000 years before the present, is reiterated.
An interesting aspect is that their method is to utilize linkage disequilibrium (LD) decay. It’s interesting because tens of thousands of years is a hell of a long time to be able to detect an admixture event via LD! In particular because there’s likely a palimpsest effect where there are intervening admixtures and other assorted demographic events (e.g., bottlenecks and selective sweeps can also generate LD). So how’d they do it? Basically the authors figured out a way to ascertain which pairs of SNPs may have introgressed from Neandertals by comparing the frequency in modern humans to Neandertals at those given SNPs (in particular, by looking at variants at low frequency in Africans and derived in Neandertals). A major technical problem here is the “genetic map” which allows one to assess what the nature of recombination over time is going to be which breaks apart the associations which are the hallmark of LD is not particular precise enough to robustly allow them to make the inferences that they want.
If you have a hard time following all the Neandertal genomics findings from the last few years, and their implications, National Geographic has a really thorough piece up. It’s a good digest of all the news you can use. One thing I would like to add: from what I can tell the probability of the signals of admixture in non-Africans being genuinely Neandertal seem to be increasing as we progress. In other words, you should weight the “other side” (ancient population structure, where some African populations were closer to Neandertals before they left Africa) less than you did in 2010.
Of course one of the more inevitable aspects of the admixture story has been the humanization of Neandertals. I don’t know how I feel about this. Should our own affinity to Neandertals alter our view of their behavior or anatomy? Plenty of behaviorally anatomically modern humans were beastly after all.
Who to trust? That is the question when you don’t know very much (all of us). Trust is precious, and to some extent sacred. That’s why I can flip out when I realize after the fact that someone more informed than me in field X sampled biased their argument in a way they knew was shady to support a proposition they were forwarding. What’s the point of that? Who cares if you win at a particular bull-session? You’re burning through cultural capital. And not that most of my interlocutors care, but I’m likely to never trust them again on anything.
In any case, this came to mind when I ran across a James Fallows’ post at The Atlantic. Here’s a screenshot of the appropriate section, with my underlines:
Well, not really…but in some ways close enough judged against the initial reference point of where I started on certain questions. Dienekes contends:
This will help us understand both: the ancestors of non-Africans did not come forth fully formed, like Athena from Zeus’s head, having spent millennia of perfecting their craft and honing their minds by perforating shells and scratching lines in some South African cave. Instead, they may been plain old-style hunter-gatherers who stumbled into Asia by doing what they always did: following the food. At the same time, the UP/LSA revolution may not have been effected by a new and improved type of human bursting into the scene and replacing Neandertals and assorted dummies, but rather as a cultural revolution that spread across a species that already had the genetic potential for it, and was already firmly established in both Africa and Asia.
The former position, that the Out-of-Africa population were genetically endowed supermen who blitzkrieged other humans ~50,000 years ago was probably the most common position ~10 years ago. It’s outlined by Richard Klein in The Dawn of Human Culture. A contrasting argument was put forth at about the same time by Stephen Oppenheimer in The Real Eve. With 10 years of hindsight much of Oppenheimer’s model leaves much to be desired, but the one aspect which I laughed at at the time, but now give much more credit to, is the proposition that the Out-of-Africa migration was an expression of a cultural revolution in a proximate sense, rather than a biological revolution.
The always informative Ann Gibbons has a piece in Slate, The Neanderthal in My Family Tree. There is almost nothing new for regular readers of this weblog, but it’s rather awesome that Slate is now publishing stuff like this. Many people are simply unaware of the new paleogenomics. Case in point, a good friend who has a doctorate in chemical physics, and was totally unaware a year after the seminal Science paper on Neandertal admixture of the likelihood of Neandertal admixture!
Nevertheless, I think it is important for me to be repetitive and highlight a disagreement I have with the Gibbons’ piece. She says:
John Hawks prompts to reemphasize an aspect of my thinking which has undergone a revolution over the past 10 years. I pointed to it in my post on the Khoe-San. In short, the common anatomically modern human ancestors of Khoe-San and non-Khoe-San may not have been people. Rather, people may have evolved over the past 100-200,000 years ago. Of course the term “people” is not quite as scientific as you might like. In philosophy and law you have debates about “personhood”. Granting the utility of these debates I am basically saying that the common ancestor of Khoe-San and non-Khoe-San may not have been persons, as well understand them. Though, as a person myself, I do think they were persons. At this point I am willing to push the class “person” rather far back in time.
As I suggested earlier there is an implicit assumption that personhood is a shared derived trait of our species. Or at least it is a consensus today that all extant members of H. sapiens are persons. Since Khoe-San are persons, the common ancestor of Khoe-San and non-Khoe-San must also be persons if personhood is a shared derived trait. But, we also know that there are many aspects of realized personhood on a sociological or cultural scale which seem to diminish the further back in time you go. For example, the Oldowan lithic technology persisted for ~1 million years. A common modern conception of persons is that persons in the aggregate are simply never so static. Persons have culture, and culture is protean. Therefore, one might infer from the nature of Oldowan technological torpor that the producers of that technology were not persons.
Over at Haldane’s Sieve there are more than preprints posted, there are commentaries from the authors as well. For example, for The genetic prehistory of southern Africa, the first author, Dr. Joseph K. Pickrell, has a extended comment up.
But occasionally you get contributions & perspectives from non-authors which are very interesting. And it is to one of these I want to draw your attention, Thoughts on: The date of interbreeding between Neandertals and modern humans. It’s a comment on The date of interbreeding between Neandertals and modern humans. In the post Dr. Graham Coop contends:
At this point you are likely saying: well we know that Neandertals existed as a [somewhat] separate population/species who are these population X you keep talking about and where are their remains? Population X could easily be a subset of what we call Neandertals, in which case you’ve been reading this all for no reason [if you only want to know if we interbred with Neandertals]. However, my view is that in the next decade of ancient human population history things are going to get really interesting. We have already seen this from the Denisovian papers [1,2], and the work of ancient admixture in Africa (e.g. Hammer et al. 2011, Lachance et al. 2012). We will likely discover a bunch of cryptic somewhat distinct ancient populations, that we’ve previously [rightly] grouped into a relatively small number of labels based on their morphology and timing in the fossil record. We are not going to have names for many of these groups, but with large amounts of genomic data [ancient and modern] we are going to find all sorts of population structure. The question then becomes not an issue of naming these populations, but understanding the divergence and population genetic relationship among them.
This is a bold contention, and I suspect some physical anthropologists will take issue with it. But it’s a testable prediction. We’ll know if it’s panned out in 2020. I may still be blogging between now and then, and so I will now self-importantly label this “Coop’s Conjecture.” Is there anyone who wants to wager some money on Coop’s Conjecture? Any side of the bet you think is a sure thing?
The map to the right shows the frequencies of HGDP populations on SLC45A2, which is a locus that has been implicated in skin color variation in humans. It’s for the SNP rs16891982, and I yanked the figure from IrisPlex: A sensitive DNA tool for accurate prediction of blue and brown eye colour in the absence of ancestry information. Brown represents the genotype CC, green CG, and blue, GG. Europeans who have olive skin often carry the minor allele, C. While SLC24A5 is really bad at distinguishing West Eurasians from each other, SLC45A2 is better. Though both are fixed in Northern Europe, the former stays operationally fixed in frequency outside of Europe, in the Near East. As I stated earlier the proportions of the ancestral SNP in the Middle Eastern populations in the HGDP seem to be easily explained by the Sub-Saharan admixture you can find in these groups.
In contrast major SNPs in SLC45A2 are closer to disjoint between Europeans and South Asians. For example I’m a homozygote for the C allele. And yet even here we need to be careful. I want in particular to draw your attention to the frequencies in the Middle Eastern populations, the Sardinians, and the Kalash of Pakistan.
The Kalash, and their Nuristani cousins, have often been observed to have “European” physical features. These populations even trade in legends of descent from the Macedonians of Alexander. And the genetics here shows why. Though the Kalash far are more closely related to other Northwest South Asians than to Europeans, on the subset of genes which are implicated in pigmentation many of them could actually “pass” for Europeans. In fact, it is interesting to me that by these measures the Sardinians are no more European than groups like the Kalash and the Druze (in contrast to the total genome, where Sardinians may be the best reference for Western Europeans). They have a lower frequency of the SNP strongly associated with blue eyes than either of these groups, for example.
In the above paper they also produced a chart which illustrated the relationships of HGDP populations as a measure only of the six SNPs they used in their prediction method. These are markers which distinguish blue and brown eye color in Europeans efficiently.
A new paper in Molecular Biology and Evolution, The timing of pigmentation lightening in Europeans, is rather interesting. It’s important because skin pigmentation has been one of the major successes of the first age of human genomics. In 2002 we really didn’t know the nature of normal human variation in skin color in terms of specific genes (basically, we knew about MC1R). This is what Armand Leroi observed in Mutants in 2005, wondering about our ignorance of such a salient trait. Within a few years though Leroi’s contention was out of date (in fact, while Mutants was going to press it became out of date) . Today we do know the genetic architecture of pigmentation. This is why GEDmatch can predict that my daughter’s eyes will be light brown from just her SNPs (they are currently hazel). This genomic yield was facilitated by the fact that pigmentation seems to be a trait where most human variation is controlled by half a dozen genes. In contrast, height or I.Q. are controlled by innumerable genes.
There have been several recent studies reemphasizing diet over exercise (timely because Americans are kind of fat, on average). A new piece in The New York Times looking at the Hadza of Tanzania, who are hunter-gatherers, seems to reiterate this point, Debunking the Hunter-Gatherer Workout:
We found that despite all this physical activity, the number of calories that the Hadza burned per day was indistinguishable from that of typical adults in Europe and the United States. We ran a number of statistical tests, accounting for body mass, lean body mass, age, sex and fat mass, and still found no difference in daily energy expenditure between the Hadza and their Western counterparts.
How can the Hadza be more active than we are without burning more calories? It’s not that their bodies are more efficient, allowing them to do more with less: separate measurements showed that the Hadza burn just as many calories while walking or resting as Westerners do.
We think that the Hadzas’ bodies have adjusted to the higher activity levels required for hunting and gathering by spending less energy elsewhere. Even for very active people, physical activity accounts for only a small portion of daily energy expenditure; most energy is spent behind the scenes on the myriad unseen tasks that keep our cells humming and our support systems working. If the Hadza’s bodies somehow manage to spend less energy in those areas, they could easily accommodate the elevated energy demands of hunting and gathering. And indeed, studies reporting differences in metabolic-hormone profiles between traditional and Western populations support this idea (though more work is needed).
As noted in the paper the researchers used urine samples to ascertain caloric expenditure. I’ve seen this in surveys of overweight people. One result was that many overweight people inadvertently under report their consumption (e.g., not writing down snacks that they ate) by as much as 1/3, so this is an essential check on self-reports. A reader brings up this relevant point:
ADMIXTURE and STRUCTURE tests aren’t formal mixture tests. Yes! In fact, in the “open science” community this issue is repeated over and over and over, because people routinely get confused (our audience does not consist of population geneticists and phylogeneticists by and large). So sometimes it is necessary to lay it out in detail as in the post above. The key point to always remember is that population genetic & phylogenetic statistics and visualizations are a reduction and summary of reality in human palatable form. They tell us something, but they do not tell us everything. A common issue is that for purposes of mental digestion it is useful to label ancestral elements “European,” or on PCA refer to a “European-Asian” cline, as if the population genetic abstractions themselves are the measure of what European or Asian is. But European and Asian are themselves human constructions, and subject to debate (e.g., do Turks count as Europeans? Indians as Asians?) The population genetic statistics are not themselves subjective, but the meanings we give them are.
Yesterday I pointed out that David Reich had a moderately dismissive attitude toward the new paper in PNAS, Effect of ancient population structure on the degree of polymorphism shared between modern human populations and ancient hominins. Here’s what Reich said:
…But Reich believes that the discussion would have been different if it had happened in the open. The PNAS paper questioning the Neanderthal admixture addresses issues swirling around two years ago, but not Reich and Slatkin’s latest work. “It’s been an issue for several years. They were right to work on this,” says Reich. But now, “it’s kind of an obsolete paper,” he says.
Here’s what Nick Patterson, Reich’s colleague told me via email:
Ancient structure in Africa was considered when we wrote the Green et al. paper, and we were aware that this could explain D-statistics. But the hypothesis is no longer viable as the major explanation of Neandertal genetics in Eurasia. This was discussed in the recent paper of Yang et al. (MBE, 2012). (Not referenced by the PNAS paper).
A very simple argument, that convinces me, is that the allelic frequency spectrum of Neandertal alleles in Eurasia falls off very quickly. A bottleneck flattens out the spectrum, and it turns out that the Neandertal gene flow has to be placed after the out of Africa bottleneck or the spectrum is much too flat.
The paper on the arXiv from the Reich lab (Sankararaman et al.) is trying to do something much more subtle than this and date the flow. I personally am no longer interested in explaining the introgression as ancient structure. That ship has sailed.
Of course the question of what was the genetic structure of Ancient Africa is quite open, and remains very interesting.
If Nick’s explanation is a bit cryptic for you (he was a cryptographer!), figure 2 from the Yang et al. paper lays it out quite clearly:
Dienekes tips me off to the fact that the long-awaited Reich lab paper on Neandertal admixture dating has finally been put on arXiv! The date of interbreeding between Neandertals and modern humans:
Comparisons of DNA sequences between Neandertals and present-day humans have shown that Neandertals share more genetic variants with non-Africans than with Africans. This could be due to interbreeding between Neandertals and modern humans when the two groups met subsequent to the emergence of modern humans outside Africa. However, it could also be due to population structure that antedates the origin of Neandertal ancestors in Africa. We measure the extent of linkage disequilibrium (LD) in the genomes of present-day Europeans and find that the last gene flow from Neandertals (or their relatives) into Europeans likely occurred 37,000-86,000 years before the present (BP), and most likely 47,000-65,000 years ago. This supports the recent interbreeding hypothesis, and suggests that interbreeding may have occurred when modern humans carrying Upper Paleolithic technologies encountered Neandertals as they expanded out of Africa.
This isn’t the only group working on the Neandertal genomic admixture story. From reading his blog you probably know that John Hawks is working in this area, but there are other labs too. I’m hoping that the Reich lab pushing their stuff on arXiv will prompt the other groups to also start moving (instead of just presenting preliminary results to a narrow group of researchers).
As for these results, I’m still amazed that LD based methods can work this far into the deep past. Second, it is nice that the low bound estimate can plausibly predate the arrival of anatomically modern humans to Australia. Also, this admixture date is well after anatomical modern humanity, and well before the classical “Great Leap Forward” of behavioral modernity. Though I think that over the next few years we may start to discard the idea of any such punctuated leap.
And again, it’s on arXiv. As they used to say, read the whole thing!
Dienekes reflects on the seemingly simultaneous appearance of behavioral modernityin South Africa and Europe and Australia, pending the acceptance of the most recent finds. This part is very important in my opinion:
The San people still live in several countries of southern Africa, and until the latter part of the 20th century were still mainly hunter-gatherers. But Dr. Stringer cautioned not to think of them as “living fossils,” unchanged by time. “Their genes, cultures and behaviors have undoubtedly continued to evolve in the intervening millennia,” he said.
I see no reason to think that these were the ancestors of the San. Over 45,000 years I think the most likely option is that genetic and cultural continuity will not be maintained, and these are probably a sister group to the modern peoples of Southern Africa. In any case, to address Dienekes’ confusion, I think this is one case where his non-American background shows. We know exactly what happened so long ago to kick-start modern humanity. The answer has been with us for over 40 years.
If you are interested in genomics and human evolution, a new review paper in PLoS Genetics is a must read, Genomic Data Reveal a Complex Making of Humans. A must read not because you need to agree with the thrust of the authors’ arguments, but because it provides a thorough bibliography for the last 2 to 3 years. Here is the abstract:
In the last few years, two paradigms underlying human evolution have crumbled. Modern humans have not totally replaced previous hominins without any admixture, and the expected signatures of adaptations to new environments are surprisingly lacking at the genomic level. Here we review current evidence about archaic admixture and lack of strong selective sweeps in humans. We underline the need to properly model differential admixture in various populations to correctly reconstruct past demography. We also stress the importance of taking into account the spatial dimension of human evolution, which proceeded by a series of range expansions that could have promoted both the introgression of archaic genes and background selection.
The main problem I have at this point is the general mode of range expansions, whereby population A expands as a demographic wave across a substrate of population B. These sorts of models seem to assume a sort of continuous dynamic process. In contrast, I am beginning to suspect that much of the human demographic past was characterized by discrete events. The closer to the present the more I’m convinced of this, though honestly I am now pushing back my own timing for the origins of many of the human distinctive traits, such as culture, well before behaviorally modern humans.