Debate over recent human evolution: pros and cons

Acceleration of recent human evolution. Age distribution of alleles under selection (Hawks et al. 2007)

A decade has passed since a research team led by John Hawks published a strange finding: human genetic evolution accelerated more than a hundred-fold some 10,000 years ago. This was when hunting and gathering began to give way to farming, which in turn brought other changes, all of which required adjustments to mind and body. All in all, new cultural and natural environments have reshaped 7% of the human genome over the last 40,000 years:

Some of the most radical new selective pressures have been associated with the transition to agriculture. For example, genes related to disease resistance are among the inferred functional classes most likely to show evidence of recent positive selection. Virulent epidemic diseases, including smallpox, malaria, yellow fever, typhus, and cholera, became important causes of mortality after the origin and spread of agriculture. Likewise, subsistence and dietary changes have led to selection on genes such as lactase. (Hawks et al. 2007)

Instead of adapting only to the natural environment, humans have adapted to cultural creations of their own making, things like prepared food, clothing, shelter, way of life, social organization, sedentary versus nomadic living, religious strictures, and so on.

This finding may come as a surprise. As a university student I learned that culture has greatly reduced the importance of natural selection in our species. Instead of adapting genetically to our environment, we adapt culturally. That was, and still is, the normative view.

Debates in the scientific literature: 2008 to 2010

So what are we to believe? Perhaps there have been other findings over the last decade, either pro or con.

In 2008, a research team led by Matthieu Foll and Oscar Gaggiotti calculated a higher estimate of recent human evolution: over 23% of the human genome. By using an FST test and data from 53 human populations, they found evidence for selection at 131 out of 560 random loci. When this methodology was repeated with other random loci, the same estimate of 23% came up.

A review paper by Joshua Akey notes, however, that these genome-wide scans are problematic in two ways. On the one hand, they miss genes that are known to have contributed to recent human evolution. On the other, these different scans disagree on the regions of the human genome that have been evolving rapidly:

Strikingly, only 722 regions (14.1%) were identified in two or more studies, 271 regions (5.3%) were identified in three or more studies, and 129 regions (2.5%) were identified in four or more studies (Fig. 1). Furthermore, the integrated map of positive selection does not include several of the most compelling genes with well-substantiated claims of positive selection, such as G6PD and DARC. (Akey 2009)

A closer look at the data suggests that recent evolution is highly localized on the human genome. If the size of the region is decreased, the probability increases of that region containing either no genes at all under selection or several under selection. Making the regions smaller makes it easier, strangely enough, to find regions with multiple genes under selection. "This paradoxical observation [...] is due to the marked difference in the average size of regions identified in single versus multiple studies (~80 kb and 300 kb, respectively)" (Akey 2009).

So estimates of recent human evolution seem to range from a low of 7% of the genome (Hawks et al. 2007) to a high of 23% (Foll and Gaggiotti 2008). Even the 7% estimate, however, has been criticized in the literature, specifically by two papers. The first one was Pickrell et al. (2009):

We find that putatively selected haplotypes tend to be shared among geographically close populations. [...]. This suggests that distinguishing true cases of selection from the tails of the neutral distribution may be more difficult than sometimes assumed, and raises the possibility that many loci identified as being under selection in genome scans of this kind may be false positives. Reports of ubiquitous strong (s = 1 - 5%) positive selection in the human genome (Hawks et al. 2007) may be considerably overstated. (Pickrell et al. 2009)

The argument here is that a genetic variant with high selective value should spread beyond its area of origin, instead of remaining bottled up there. Yet this is unlikely for two reasons. First, recent variants, by definition, have little time to spread very far. Second, and more importantly, the selective value of a genetic variant is a function of its natural and cultural environment. A variant that succeeds in one environment will be less successful in another.

The criticism made by Pickrell et al. (2009) was repeated by Hermisson (2009). If the data are controlled for geographic region, the evidence for recent human evolution virtually disappears:

[...] introduction of hierarchical structure based on five previously established geographic regions reduces the frequency of selection candidates from 23% (Foll and Gaggiotti, 2008) to no more than expected by chance (that is, comparable with the 1% significance level applied). (Hermisson 2009)

The implication is that recent human evolution is largely due to founder effects and other forms of genetic drift. Genetic drift, however, would not produce the observed signatures of natural selection, as Nicholas Wade noted in a review of this research the following year:

One of the signatures of natural selection is that it disturbs the undergrowth of mutations that are always accumulating along the genome. As a favored version of a gene becomes more common in a population, genomes will look increasingly alike in and around the gene. Because variation is brushed away, the favored gene's rise in popularity is called a sweep. Geneticists have developed several statistical methods for detecting sweeps, and hence of natural selection in action. (Wade 2010).

Moreover, this signature is much stronger in some geographic regions than in others:

A new approach to identifying selected genes has been developed by Anna Di Rienzo at the University of Chicago. Instead of looking at the genome and seeing what turns up, Dr. Di Rienzo and colleagues have started with genes that would be likely to change as people adopted different environments, modes of subsistence and diets, and then checked to see if different populations have responded accordingly.

She found particularly strong signals of selection in populations that live in polar regions, in people who live by foraging, and in people whose diets are rich in roots and tubers. [..] The fewest signals of selection were seen among people who live in the humid tropics, the ecoregion where the ancestral human population evolved. [...] there seem to be more genes under recent selection in East Asians and Europeans than in Africans, possibly because the people who left Africa were then forced to adapt to different environments. "It's a reasonable inference that non-Africans were becoming exposed to a wide variety of novel climates," says Dr. Stoneking of the Max Planck Institute. (Wade 2010)

Joshua Akey remains cautious on this point:

A specific example of the difficulties in interpreting signatures of spatially varying selection is the observation that non-African populations tend to show more evidence for recent positive selection relative to African populations (Akey et al. 2004; Storz et al. 2004; Williamson et al. 2007; but see Voight et al. 2006). While this may be due to increased selection as humans migrated out of Africa and were confronted with new environmental pressures (such as novel climates, diets, and pathogens), differences in demographic history or rates of recombination and mutation between African and non-African populations may obscure the relationship between signatures of selection across populations. (Akey 2009)

Since 2010: consensus among some, skepticism and hostility among others

After 2010, Google Scholar turns up only brief references to the original paper by John Hawks et al., most of them favorable or neutral in tone. If one judges by the scientific literature alone, there seems to be broad support for the notion that recent evolution has accelerated in our species. And the original estimate of 7% recent evolutionary change may err on the low side

Yet many people remain unconvinced. Last week Razib Khan reproached me: "you take the accelerationist hypothesis as a given. it's not. at least at that magnitude (i think most ppl agree holocene resulted in faster rate of change)." Indeed, most people seem to view these findings with incredulity, to put it mildly, as a journalist from Discover magazine found:

Not surprisingly, the new findings have raised hackles. Some scientists are alarmed by claims of ethnic differences in temperament and intelligence, fearing that they will inflame racial sensitivities. Other researchers point to limitations in the data. Yet even skeptics now admit that some human traits, at least, are evolving rapidly, challenging yesterday's hallowed beliefs. (McAuliffe 2009)

A decade later, the barriers to acceptance are still considerable. Chen et al. (2016) identifies four sources of opposition:

- Evolutionary psychologists, who believe that human nature took shape in the Pleistocene. According to this view, genetic influences on behavior are too complex to have changed much since then.

- Cultural determinists, who believe that "once humans invented culture, natural selection was halted because humans could overcome nature through culture."

- People who point out that we are all 99.9% genetically alike. So there is little room for genetic differences within our species.

- People who believe that genetic differences are inconsequential to human behavior.

There are counter-arguments to the above. Genetic influences on existing behaviors can evolve very fast (Harpending and Cochran 2002). And that figure of 99.9% genetic identity is an over-estimate, the best estimate being 99%. Even if we assume that this 1% difference is spread evenly across the genome, that tiny difference could significantly alter the way each and every gene works.

Nonetheless, such counter-arguments would still leave many unconvinced. And others wouldn't even listen. Some beliefs are foundational, being difficult to challenge without seeming to attack an entire worldview. In such cases, reactions can be nasty.

That's normal. Strong disagreement is the stuff of scientific debate. What's less normal is that some people will seek not to debate but to judge and punish. That fate befell a coauthor of the 2007 paper on recent human evolution. In 2015, the Southern Poverty Law Center (SPLC) prepared and published a file on Henry Harpending ... under the heading "Extremist Info." The opening words sounded no less ominous:

Henry Harpending is a controversial anthropologist at the University of Utah who studies human evolution and, in his words, "genetic diversity within and between human populations."

The file went on to state:

Harpending is most famous for his book, co-authored with frequent collaborator Gregory Cochran, The 10,000 Year Explosion: How Civilization Accelerated Human Evolution, which argues that humans are evolving at an accelerating rate, and that this began when the ancestors of modern Europeans and Asians left Africa. (SPLC 2015)

One wonders what exactly is intended by this public naming and shaming. After all, the SPLC has no legal mandate to judge and punish, although it seems to think so. Indeed, it acts like a law-enforcement agency without being constrained by the law and without being answerable to an elected body.

Henry Harpending died scarcely a year later, yet his file is still there on the SPLC website. Even in death he's still a grave threat … as is apparently anyone else who believes in the evidence for recent human evolution.

References

Akey, J.M. (2009). Constructing genomic maps of positive selection in humans: Where do we go from here? Genome Research 19: 711-722.

https://pdfs.semanticscholar.org/9199/dab2542982e282eaf28fc303008c20583db7.pdf

Chen, C., R.K. Moyzis, X. Lei, C. Chen, and Q. Dong. (2016). "The enculturated genome: Molecular evidence for recent divergent evolution in human neurotransmitter genes." In Joan Y. Chiao, Shu-Chen Li, Rebecca Seligman, Robert Turner (eds). The Oxford Handbook of Cultural Neuroscience. Oxford.

https://books.google.ca/books?id=rtbiCgAAQBAJ&printsec=frontcover&hl=fr&source=gbs_ge_summary_r&cad=0#v=onepage&q&f=false

Cochran, G. and H. Harpending. (2010). The 10,000 Year Explosion: How Civilization Accelerated Human Evolution, New York: Basic Books.

Foll, M., and O. Gaggiotti. (2008). A Genome-Scan Method to Identify Selected Loci Appropriate for Both Dominant and Codominant Markers: A Bayesian Perspective. Genetics 180(2):977-993.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2567396/

Harpending, H., and G. Cochran, (2002). In our genes, Proceedings of the National Academy of Science. USA. 99(1):10-12.

https://s3.amazonaws.com/academia.edu.documents/43528175/In_our_genes20160308-5744-8wzdxj.pdf?AWSAccessKeyId=AKIAIWOWYYGZ2Y53UL3A&Expires=1524495810&Signature=XEX4Jqbe%2FAD3Faud9Re0M1ECEys%3D&response-content-disposition=inline%3B%20filename%3DIn_our_genes.pdf

Hawks, J., E.T. Wang, G.M. Cochran, H.C. Harpending, and R.K. Moyzis. (2007). Recent acceleration of human adaptive evolution, Proceedings of the National Academy of Science USA 104:20753-20758.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2410101/

Hermisson, J. (2009). Who believes in whole-genome scans for selection? Heredity 103, 283-284

https://www.nature.com/articles/hdy2009101  

McAuliffe K. (2009). They don't make Homo sapiens like they used to. Our species-and individual races-have recently made big evolutionary changes to adjust to new pressures. Discover February 9

http://discovermagazine.com/2009/mar/09-they-dont-make-homo-sapiens-like-they-used-to

Pickrell, J.K., G. Coop, J. Novembre, S. Kudaravalli, J.Z. Li, D. Absher, B.S. Srinivasan, G.S. Barsh, R.M. Myers, M.W. Feldman, and J.K. Pritchard. (2009). Signals of recent positive selection in a worldwide sample of human populations. Genome Research 19(5): 826-837

http://europepmc.org/articles/pmc2675971  

SPLC. (2015). Henry Harpending. Extremist Info

https://www.splcenter.org/fighting-hate/extremist-files/individual/henry-harpending

Wade, N. (2010). Adventures in very recent evolution. The New York Times, July 19

https://www.nytimes.com/2010/07/20/science/20adapt.html