Category: Evolution

The human extended phenotype

Posted on by Razib Khan


I think there is something to the hypothesis that we as a species are self-domesticated, but a new preprint really doesn’t change my probability up or down, Comparative Genomic Evidence for Self-Domestication in Homo sapiens. Notwithstanding my own participation in some comparative genomic work, a lot of the conclusions from this field are as clear and obvious to me as the above figure, not very.

To be fair at least the authors of the preprint have a hypothesis they’re testing, the “domestication syndrome” as cause by the neural crest gene modification. Two major issues I’d bring up: it’s comparative genomic because of a paucity of samples, and, tidy explanations often don’t pan out.

Genomic analysis of ancient genomes is very preliminary. Phylogenomic work, which establishes relationships between lineages, can accept a noisy and poor marker set with only a few representative samples. But when looking at population genomics one should at least have either really good data on a small number of individuals, or, more preferable, good-enough-data on lots of individuals. The ancient genomic data set for hominins is not rich enough that I’m confident about any but the most obvious and clear differences between our closest relations and ourselves. The reality of gene flow across populations also adds a confounding element, because it might not be implausible that “modern” alleles actually derive from another ancient lineage, and our modern forebears exhibited the ancestral state.

Second, the neural crest hypothesis and a general model of domestication is rather attractive. I myself find it intriguing, and am curious from a professional scientific perspective. But, attractive hypotheses often do not pan out, and gain early attention because scientists are human, and exhibit some bias and hope. A case in point, mirror neurons has stalled as a silver bullet to explain all sorts of unique aspects of human cognition. Neural crest models are part of the long quest to establish the genes which make us unique and human, even though I’m not even sure this is a wrong question.

The preprint did remind me of an excellent book I read over 10 years ago, The Cultural Origins of Human Cognition. I am much more well disposed toward the thesis now than I was then, in large part because I now longer hold to a “big bang” theory of the origin of modern humanity due to a behavioral revolution triggered by a rapid suite of genetic changes. Rather, I suspect a cultural model where there is reciprocal feedback with genetic changes in a sort of ratchet has a lot more utility, in part because the gap between “archaic” H. sapiens and our own ancestors was I believe much smaller in many ways in relation to behavior than we’ve assumed until lately. Finally, the genetic evidence of lots of lateral gene flow across these distinct branches is indicative of more complexity in the origin of humanity than we had previously understood.

There is also the whole idea of “self-domestication.” I think perhaps it needs to be more explicitly formulated in an ecological sense. Rather than self-domestication, what occurred is that a host of species began to inhabit an evolving “extended phenotype” which humans were a motive engine within. But we need to be cautious about overemphasizing our agency. Once human societies became agricultural beyond a certain point it is not not possible to revert back to hunter-gathering lifestyles without migration or mass die off. In some ways we are as much pawns in the forces unleashed by our original choices and actions as the domestic animals and plants and parasites which have come along for the ride.

Citation: Comparative Genomic Evidence for Self-Domestication in Homo sapiens, Constantina Theofanopoulou, Simone Gastaldon, Thomas O’Rourke, Bridget D Samuels, Angela Messner, Pedro Tiago Martins, Francesco Delogu, Saleh Alamri, Cedric Boeckx, doi: https://doi.org/10.1101/125799

Why humans have so many pulse admixtures

Posted on by Razib Khan

The Blank Slate is one of my favorite books (though I’d say The Language Instinct is unjustly overshadowed by it). There is obviously a substantial biological basis in human behavior which is mediated by genetics. When The Blank Slate came out in the early 2000s one could envisage a situation in 2017 when empirically informed realism dominated the intellectual landscape. But that was not to be. In many ways, for example in sex differences, we’ve gone backward, while there is still undue overemphasis in our society on the environmental impact parents have on children (as opposed to society more broadly).

But genes do not determine everything, obviously. Several years after reading The Blank Slate I read Not by Genes Alone: How Culture Transformed Human Evolution. In this work Peter Richerson and Robert Boyd outline their decades long project of modeling cultural variation and evolution formally in a manner reminiscent of biological evolution. Richerson and Boyd’s program does not start from a “blank slate” assumption. Rather, it is focused on broad macro-social dynamics where cultural variation “swamps” out biological variation.

Recall that in classic population genetic theory a major problem with group level selection is that gene flow between adjacent groups quickly removes between group variation. One migrant between two groups per generation is enough for them not to diverge genetically. For group selection to occur the selective effect has to be very strong or the between group difference has to be very high. Rather than talking about genetics though, where the debate is still live, and the majority consensus is still that biological group selection is not that common (depending on how you define it), let’s talk about human culture.

Here the group level differences are extreme and the boundaries can be sharp. Historically it seems likely that most groups which were adjacent to each other looked rather similar because of gene flow and similar selective pressures. Even though in medieval Spain there was a generality, probably true, that Muslims were swarthier than Christians*, there was a palpable danger in battle of identifying friend from foe because the two groups overlapped too much in appearance.

This brings up how one might delineate differences culturally. In battle opposing armies wear distinct uniforms and colors so that the distinction can be made. But obviously one change uniform surreptitiously (perhaps taking the garb from the enemy dead). This is why physical adornment such as tattoos are useful, as they are “hard to fake.” Perhaps the most clear illustration of this dynamic is the Biblical story for the origin of the term shibboleth. Even slight differences in accent are clear to all, and, often difficult to mimic once in adulthood.

Biological evolution mediated through genes is relatively slow and constrained compared to cultural evolution. Whole regions of central and northern Europe shifted from adherence to Roman Catholicism to forms of Protestantism on the order of 10 years. Of course religion is an aspect of culture where change can happen very rapidly, but even language shifts can occur in only a few generations (e.g., the decline of regional German and Italian dialects in the face of standard forms of the language).

Cultural evolution as a formally modeled neofunctionalism is credibly outlined in works such as Peter Turchin’s Ultrasociety: How 10,000 Years of War Made Humans the Greatest Cooperators on Earth. That’s not what I want to focus on here. Rather, I contend that the reality of massive pulse admixtures evident in the human genome over the past 10,000 years, at minimum, is a function of the fact that human cultural evolutionary processes result in winner-take-all genetic consequences.

A concrete example of what I’m talking about would compare the peoples of the Italian peninsula and the Iberian peninsula around 1500. The two populations are not that different genetically, and up to that point shared many cultural traits (and continue to do so). But, a combination of geography and history resulted in Iberian demographic expansion in the several hundred years after 1500, whereby today there are probably many more descendants of Iberians than Italians. This is not a function of any deep genetic difference between the two groups. There aren’t deep genetic differences in fact. Rather, the social and demographic forces which propelled Iberia to imperial status redounded upon the demographic production of Iberians in the future. In addition, the New World underwent a massive pulse admixture between Iberians, and native Amerindians, as well as Africans, usually brought over as slaves, due the cultural and political history of the period.

The pulse admixture question is rather interesting academically. To some extent current methods are biased toward detection of pulse admixtures, and even fit continuous gene flow as pulse admixtures. A quick rapid exchange of gene flow and then recombination breaking apart associations of markers which are ancestrally informative haplotypes is something you can test for. But I think we can agree that the gene flow triggered by the Columbian Exchange was a pulse admixture, and there’s too much concurrent evidence from uniparental lineage turnover in the ancient DNA to dismiss the non-historically corroborated signatures of pulses as simply artifacts.

Nevertheless continuous gene flow does occur. That is, normal exchange of individuals between neighboring demes as a slow simmer over time. But the idea that we are a clinal ring species or something like that isn’t right in my opinion. Part of the story are strong geographical barriers. But another major part is that cultural revolutions and advantages introduce huge short-term demographic advantages to particular groups, and the shake out of inter-group competition can be dramatic.

Therefore, I make a prediction: the more cultural evolutionary dynamics a species is subject to, the more pulse admixture you’ll be able to detect. For example, pulse admixture should be more important in social insects than their solitary relatives.

* Not only was some of the ancestry of Muslims North African, Muslim rule was longest in the southern and southeastern regions, where people were not as fair as in the north.

How Tibetans can function at high altitudes

Posted on by Razib Khan


About seven years ago I wrote two posts about how Tibetans manage to function at very high altitudes. And it’s not just physiological functioning, that is, fitness straightforwardly understood. High altitudes can cause a sharp reduction in reproductive fitness because women can not carry pregnancies to term. In other words, high altitude is a very strong selection pressure. You adapt, or you die off.

For me there have been two things of note since those original papers came out. First, one of those loci seem to have been introgressed from a Denisovan genetic background. I want to be careful here, because the initial admixture event may not have been into the Tibetans proper, but earlier hunter-gatherers who descend from Out of Africa groups, who were assimilated into the Tibetans as they expanded 5-10,000 years ago. Second, it turns out that dogs have been targeted for selection on EPAS1 as well (the “Denisovan” introgression) for altitude adaptation as well.

This shows that in mammals at least there’s a few genes which show up again and again. The fact that EPAS1 and EGLN1 were hits on relatively small sample sizes also reinforces their powerful effect. When the EPAS1 results initially came out they were highlighted as the strongest and fastest instance of natural selection in human evolutionary history. One can quibble about the details about whether this was literally true, but that it was a powerful selective event no one could deny.

A new paper in PNAS, Genetic signatures of high-altitude adaptation in Tibetans, revisits the earlier results with a much larger sample size (the research group is in China) comparing Han Chinese and Tibetans. They confirm the earlier results, but, they also find other loci which seem likely targets of selection in Tibetans. Below is the list:

SNPA1A2Frequency of A1P valueFSTNearest gene
TibetanEAS (Han)
rs1801133AG0.2380.3336.30E-090.021MTHFR
rs71673426CT0.1020.0131.50E-080.1RAP1A
rs78720557AT0.4980.2014.70E-080.191NEK7
rs78561501AG0.5990.1356.10E-150.414EGLN1
rs116611511GA0.4470.0033.60E-190.57EPAS1
rs2584462GA0.2110.5493.90E-090.203ADH7
rs4498258TA0.5860.2871.70E-080.171FGF10
rs9275281GA0.0950.3651.10E-100.162HLA-DQB1
rs139129572GAG0.3160.4495.80E-090.036HCAR2
P value indicates the P value from the MLMA-LOCO analysis. FST is the FST value between Tibetans and EASs. Nearest gene indicates the nearest annotated gene to the top differentiated SNP at each locus except EGLN1, which is known to be associated with high-altitude adaptation; rs139129572 is an insertion SNP with two alleles: GA and G. A1, allele 1; A2, allele 2.

Many of these genes are familiar. Observe the allele frequency differences between the Tibetans and other East Asians (mostly Han). The sample sizes are on the order of thousands, and the SNP-chip had nearly 300,000 markers. What they found was that the between population Fst of Han to Tibetan was ~0.01. So only 1% of the SNP variance in their data was partitioned between the two groups. These alleles are huge outliers.

The authors used some sophisticated statistical methods to correct for exigencies of population structure, drift, admixture, etc., to converge upon these hits, but even through inspection the deviation on these alleles is clear. And as they note in the paper it isn’t clear all of these genes are selected simply for hypoxia adaptation. MTFHR, which is quite often a signal of selection, may have something to due to folate production (higher altitudes have more UV). ADH7 is part of a set of genes which always seem to be under selection, and HLA is never a surprise.

Rather than get caught up in the details it is important to note here that expansion into novel habitats results in lots of changes in populations, so that two groups can diverge quite fast on functional characteristics.  The PCA makes it clear that Tibetans and Hans have very little West Eurasian admixture, and the Fst based analysis puts their divergence on the order of 5,000 years before the present. The authors admit honestly that this is probably a lower bound value, but I also think it is quite likely that Tibetans, and probably Han too, are compound populations, and a simple bifurcation model from a common ancestral population is probably shaving away too many realistic edges. In plainer language, there has been gene flow between Han and Tibetans probably <5,000 years ago, and Tibetans themselves probably assimilated more deeply diverged populations in the highlands as they expanded as agriculturalists. An estimate of a single divergence fits a complex history to too simple of a model quite often.

The take home: understanding population history is probably important to get a better sense of the dynamics of adaptation.

Citation: Jian Yang, Zi-Bing Jin, Jie Chen, Xiu-Feng Huang, Xiao-Man Li, Yuan-Bo Liang, Jian-Yang Mao, Xin Chen, Zhili Zheng, Andrew Bakshi, Dong-Dong Zheng, Mei-Qin Zheng, Naomi R. Wray, Peter M. Visscher, Fan Lu, and Jia Qu, Genetic signatures of high-altitude adaptation in Tibetans, PNAS 2017 ; published ahead of print April 3, 2017, doi:10.1073/pnas.1617042114

Jeepers creepers…those eyes

Posted on by Razib Khan

I take some interest in the old debate about contingency and some aspect of determinism in evolutionary processes. Basically the debate is whether the basic morphology and mechanism of life on earth would exhibit the same patterns we see around us today if we rewound the clock. Stephen Jay Gould, most extensively in The Structure of Evolutionary Theory, argued for radical contingency. In Life’s Solution Simon Conway Morris takes a very different view. From what I can tell Richard Dawkins actually takes a somewhat middle perspective, though generally he is chalked up in the anti-Gouldian position (see The Ancestor’s Tale).

But ultimately this is all jaw-jaw. Real science deals in facts adduced and theories propounded. The great “debates” between “schools” of thought in the natural sciences usually suggests to me a paucity of data and method for the purposes of analysis. When it comes to contingency and inevitability that’s changing. Though I usually focus on the molecular evolutionary aspects of the scholarship (see Joe Thornton’s work), a new preprint in biorxiv utilizes phylogenetic reconstruction to indirectly addresses this question, Temporal Niche Expansion In Mammals From A Nocturnal Ancestor After Dinosaur Extinction:

Most modern mammals, including strictly diurnal species, exhibit sensory adaptations to nocturnal activity, thought to be the result of a prolonged nocturnal phase or ‘bottleneck’ during early mammalian evolution. Nocturnality may have allowed mammals to avoid antagonistic interactions with diurnal dinosaurs during the Mesozoic. However, understanding the evolution of mammalian activity patterns is hindered by scant and ambiguous fossil evidence. While ancestral reconstructions of behavioural traits from extant species have the potential to elucidate these patterns, existing studies have been limited in taxonomic scope. Here, we use an extensive behavioural dataset for 2415 species from all extant orders to reconstruct ancestral activity patterns across Mammalia. We find strong support for the nocturnal origin of mammals and the Cenozoic appearance of diurnality, although cathemerality (mixed diel periodicity) may have appeared in the late Cretaceous. Simian primates are among the earliest mammals to exhibit strict diurnal activity, some 52-33Mya. Our study is consistent with the hypothesis that temporal partitioning between early mammals and dinosaurs during the Mesozoic led to a mammalian nocturnal bottleneck, but also demonstrates the need for improved phylogenetic estimates for Mammalia.

The results from this analysis aren’t revolutionary. Through fancy rjMCMC they infer a posterior probability of 0.74 for the nocturnal hypothesis. As someone who knows very little about this topic I’d probably have guessed such a number. But at least the discussion is happening on a formal basis.

But first, this analysis highlights the likelihood that the tens of millions of years our mammalian ancestors spent as nocturnal creatures still redound to non-nocturnal lineages today, over 60 millions years beyond the end of the Age of Dinosaurs. Presumably in all this time mutation could have random-walked itself into some other optimum and moved beyond those nocturnal adaptations, but it seems that that legacy is with us still. Strike one for contingency.

Without knowing anything I’d predict birds would be the opposite, with nocturnal lineages derived from diurnal ancestors.

A final gripe about this preprint: data and code are available after publication. This is really a methods based paper and I did toy with the idea of trying to reanalyze the data. Oh well, I guess not.

Citation: Temporal Niche Expansion In Mammals From A Nocturnal Ancestor After Dinosaur Extinction, Roi Maor, Tamar Dayan, Henry Ferguson-Gow, Kate Jones
bioRxiv 123273; doi: https://doi.org/10.1101/123273

List of top 10 evolutionary biologists in history

Posted on by Razib Khan

What is your list of the top 10 evolutionary biologists in history? I’m asking because this came up in a discussion with a friend. Obviously the composition of the list will have to do with disciplinary bias and geography and history (there are Russian population geneticists from the 20th century who should be more famous who aren’t).

Here are my top 10 (with two minutes thought given):

1. Charles Darwin & Alfred Russell Wallace (I’m combining these two)
2. R. A. Fisher
3. Sewall Wright
4. J. B. S. Haldane
5. W. D. Hamilton
6. G. G. Simpson
7. John Maynard Smith
8. August Weismann
9. Motoo Kimura
10. Theodosius Dobzhansky

What’s your list? (in the comments)

10 things about human evolution (genetics) you should know (simpler)

Posted on by Razib Khan

In response to my earlier post some people suggested that the language was impenetrable. Nathan Taylor​ offered to make it more plain spoken, so here is this go at it. I think it’s pretty good.

(text below is from Nathan)  

1) Modern humans stayed in Africa for tens of thousands years of before expanding beyond it. Most of the ancestors of non-African humanity seem to have started expanding rapidly from a small founder group of less than 1,000 people, starting around 50-75 thousand years years ago. African humanity has a more complex pattern. Some groups diverged as early as 200,000 years ago, then mixed back together.


2) Don’t think of humanity as a branching tree. Rather think of humanity as groups of streams. Some streams end, many fold back on one another, and some suddenly have massive expansions. Surprisingly, all major human population groups we know today seem to be the product of relatively recent fusions. Even Africa, the source of modern humanity, has seen streams flow back from Eurasia.


3) Many of the characteristics people focus on today are of recent origin. At least as measured in thousands or tens of thousands of years. 8,000 years ago parts of Europe were populated by brown skinned hunter gatherers with blue eyes. Whiter skin is a (relatively) recent development. And the thick straight hair now common among East Asians is recent as well.

4) The genetic variant which helps Tibetans tolerate very high altitudes comes from a human lineage as divergent from modern humans as Neanderthals are. The Denisovans. This illustrates a general trend: we have adaptations from other very diverged human lineages in our genes today. Even if the genetic percentage is small.


5) The transition to agriculture and complex civilization seems correlated with the explosive growth of a few select male Y chromosomes. Think Genghis Khan.


6) It seems unlikely there is one genetic change which made humans humans. This is less certain than 1-5, but I’m pretty sure it’s true. Researchers have been looking for this for years and haven’t turned up anything definitive. I think the reason is simple enough: many genetic changes came together to make us distinctive.


7) A lot of variation between human groups is not due to novel genes. Rather it comes from increasing the popularity of pre-existing genetic variants. For example, the lightening of skin across parts of Eurasia is due to an increase of genetic variants which are common to many human populations. Height is another example.


8) Cultural flexibility does not means humans are not evolving. On the contrary, strong shifts in cultural norms seem to drive human evolution. Lactase persistence (the ability to drink milk as an adult) is a clear case. But even genetic tolerance to malaria was ultimately driven by human created environmental changes.


9) There are no “most ancient” human group. By definition, we are all equally separated in time from our common ancestors.


10) There are hints of possible new discoveries coming from ancient human DNA.  For example there is evidence of humans leaving Africa ~100,000 years ago into Eurasia in both genetic and fossil data. These earlier humans may have been overrun by a later group. But this is hard to determine with the current data. The DNA of current and ancient humans still has many stories to tell.

10 things about human evolution (genetics) you should know

Posted on by Razib Khan

In 2011 I had dinner with a friend of mine from college. He’s a smart guy. Ph.D. in chemistry form M.I.T and all that. I mentioned offhand how it was rather proven to good degree of certainty there was Neanderthal gene flow into modern humans (our lineage)[1]​. He was somewhat surprised by this information, and I was aghast that he didn’t know. 1It was one of the biggest science stories of the year. Right?

What that brought home to me is that something that seems revolutionary near to your heart or field of occupational interest may not be so visible to those who are not similarly situated. My friend is a well educated person with a science Ph.D., but it was just not on his radar. Similarly, I had very smart friends in college who were evangelical Christians who were surprised by the high degree of identity between the chimpanzee and human in regards to our DNA sequence (they were Creationists, and skeptical of any close kinship).

Here’s a final example that might interest readers. I had a long conversation with a relatively prominent journalist a month or so ago. Someone who writes in biology, and in particular genetics (who is not Carl Zimmer). I mentioned offhand to them that the work of various labs utilizing ancient DNA is showing rather conclusively that the vast majority of human populations are relatively recent admixtures between highly diverged lineages. To put it in plainer language: we are all mestizos! This journalist was totally surprised by this fact.

This indicates to me again that facts which are “known” in the “in-group” may be surprising to those who are not as hooked in. It isn’t a matter of being educated, smart, or interested. It’s a matter of narrowly constrained social channels.

Here are 10 facts that we’ve recently discovered about human evolution, with a focus on genetics since that’s what I know best, which you should probably know. Or might find interesting.

1) The expansion/development of modern humans occurred within Africa for tens of thousands of before their expansion “Out of Africa.” Most of the ancestors of non-African humanity seem to have started expanding rapidly from a small founder group of 100-1,000 50-75 thousand years years ago. African humanity has a different and more complex historical pattern, with lineages which began diverging as early as 200,000 years before the present, and then mixing back with each other.

2) Related to #1, we’re one species, so rather than an expanding “tree” from common ancestors, it’s better to think of a mesh which keeps coming back together, as some branches are pruned, and the whole pulses out periodically. All major human populations seem to be the product of relatively recent fusions between diverged branches. Africa was the source of modern humanity, but clearly there has been “back migration” from Eurasia.

3) Many of the phenotypes we define as characteristic of various human populations are relatively recent. E.g., the depigmented look of Northern Europeans, or the thick straight hair of East Asians.

4) The Denisovan version of EPAS1 which is found in Tibetans illustrates a general trend: we have adaptations from other very diverged human lineages through low levels of gene flow[2]​.

5) The transition to agriculture and complex “civilization” seems correlated to pulses of highly fecund male paternal lineages. Many of the common Y chromosomes today exhibit a pattern of diversification indicative of explosive population growth.

6) It seems unlike there is one singular genetic change which makes us sui generis or distinctive in relation to our hominin cousins. This is less certain than 1-5, but I’m pretty sure that this is so. Researchers have been looking for years, and not finding anything definitive, and I think there’s a reason. There isn’t anything definitive. Many genetic changes come together to make our lineage distinctive.

7) A lot of adaptation occurs through reemergence of old variation which is floating around in the human population. For example, the lightening of skin across parts of Eurasia co-opt common mammalian pigmentation pathways.

8) Cultural flexibility does not negate biological evolution. On the contrary, strong shifts in cultural norms seem to drive biology. Lactase persistence is a clear case, but even something like malaria adaptation is ultimately due to anthropogenic environmental changes.

9) We are all equally descended from common ancestors. There are no “most ancient” human lineages. We’re all equally recent by definition.

10) There are evolutionary genetic events in our history which are hinted at in the most recent data, so there are major lacunae in our knowledge. The picture is well formed, but not complete. E.g., there is evidence of pulses out of Africa ~100,000 years ago into Eurasia in both genetic and fossil data. These lineages may have gone extinct, or, their contribution may be difficult to detect with current data sets. But there is clearly more to be told in this story.