How some populations adapt to vitamin D scarcity

 

Vitamin D metabolism varies from one human population to another, as do most heritable traits. This is the subject of a review article I’ve recently published in the journal Nutrients. Here is the abstract:

 

 

Vitamin D metabolism differs among human populations because our species has adapted to different natural and cultural environments. Two environments are particularly difficult for the production of vitamin D by the skin: the Arctic, where the skin receives little solar UVB over the year; and the Tropics, where the skin is highly melanized and blocks UVB. In both cases, natural selection has favored the survival of those individuals who use vitamin D more efficiently or have some kind of workaround that ensures sufficient uptake of calcium and other essential minerals from food passing through the intestines. Vitamin D scarcity has either cultural or genetic solutions. Cultural solutions include consumption of meat in a raw or boiled state and extended breastfeeding of children. Genetic solutions include higher uptake of calcium from the intestines, higher rate of conversion of vitamin D to its most active form, stronger binding of vitamin D to carrier proteins in the bloodstream, and greater use of alternative metabolic pathways for calcium uptake. Because their bodies use vitamin D more sparingly, indigenous Arctic and Tropical peoples can be misdiagnosed with vitamin D deficiency and wrongly prescribed dietary supplements that may push their vitamin D level over the threshold of toxicity.

 

 

Reference

 

Frost P. (2022) The Problem of Vitamin D Scarcity: Cultural and Genetic Solutions by Indigenous Arctic and Tropical Peoples. Nutrients 14(19):4071. https://doi.org/10.3390/nu14194071

 

Extreme founder events among ancestral Europeans

 

 

Expansion of steppe pastoralists (Narasimhan et al. 2019)

 

How much of the present-day European gene pool comes from the indigenous hunter-gatherers? How much from Neolithic farmers of Anatolian origin? And how much from steppe pastoralists of the Don-Volga area? There is no easy answer.

 

 

A “founder event” results when a few people split off from their original population and found a new one. The fewer they are, the likelier they will differ genetically, on average, from the original population. The founder event is a “bottleneck” through which only a small fraction of the original genetic diversity can pass into the new population.

 

A founder event is one of three reasons why adjacent populations may differ from each other genetically. The other two are:

 

Natural selection – The boundary between two adjacent populations often corresponds to a change in the natural environment (vegetation, climate, etc.) or the cultural environment (diet, way of life, rules and prohibitions, sexual division of labor, etc.). The two populations are thus subjected to different regimes of natural selection.

 

Population admixture or replacement – One of the two adjacent populations has admixed with or been replaced by a population that has moved into the area.

 

In practice, a founder event overlaps with differences in natural selection. When pioneers move into a new area, they tend to be better suited to the local conditions than the people they left behind. The less suited are less likely to go, and if they do go they are more likely to go back … or die. So, from the outset, there already is some selection.

 

A new study of ancient DNA has shown that founder effects have been more frequent and more “extreme” than previously thought: “In humans, we find that over half of the analyzed populations have evidence for recent founder events, associated with geographic isolation, modes of sustenance, or cultural practices such as endogamy” (Tournebize et al. 2022, p. 1)

 

Contrary to popular belief, Ashkenazi Jews are not the outcome of a particularly extreme founder event:

 

Across worldwide populations, we identified 53 groups that have experienced more extreme founder events (with significantly higher founder intensity) than AJs [Ashkenazi Jews], who have high rates of recessive diseases due to their history of founder events (Tournebize et al. 2022, p. 7)

 

Perhaps those recessive diseases are not due to a founder event. Perhaps they are a side-effect of selection for an adaptive trait. If a founder effect had been the cause, those diseases would be distributed randomly over different metabolic pathways. Actually, they are all associated with excessive storage of sphingolipids, a key component of neural tissue (Cochran et al. 2006; Diamond 1994).

 

Founder events seem to have been frequent among ancestral Europeans, regardless of whether they were hunter-gatherers, farmers, or pastoralists. But those events seem to have been more “intense” among European hunter-gatherers. In other words, founder groups were smaller and spent more time passing through the population bottleneck.

 

Recent analysis has shown that present-day Europeans are a mixture of three major ancestry groups related to ancient European hunter-gatherers, Anatolian farmers, and Eurasian Steppe pastoralists. […] Across the three groups, we found that the frequency of founder events was similar, ranging between 90–100%. However, the average founder intensity was significantly higher in European hunter-gatherers […] compared to the Near Eastern farmers […] or the Steppe pastoralists. (Tournebize et al. 2022, p. 11)

 

Hunter-gatherers had more intense founder events because they had a lower population density. Founder groups were thus smaller and less representative of the original population from which they came.

 

… we found local hunter-gatherer groups had more extreme founder events than the Neolithic farmers or Bronze Age individuals. This suggests that population sizes in Europe have increased over time, coupled with changes in ancestry and transitions in lifestyle. Our results are consistent with a recent study that measured short runs of homozygosity in ancient Europeans and found a similar increase in population size during the Neolithic period. Our results are also in agreement with archeological evidence for increased population size during the Neolithic transition. (Tournebize et al. 2022, p. 14)

 

This takes us back to the previous quote: Europeans are a mix of indigenous hunter-gatherers, Anatolian farmers, and steppe pastoralists. These three groups, and their roles in European prehistory, can be summarized as follows:

 

·         Farmers began to move into Europe from present-day Turkey about 10,000 years ago. Initially, they advanced rapidly through territory inhabited by small nomadic bands.

·         About 7,000 years ago, the wave of advance stalled along a line running from the Low Countries to the Black Sea. To the north, along the North Sea and the Baltic, were large semi-sedentary communities of hunter-fisher-gatherers who could less easily be replaced because they were so numerous.

·         About a thousand years later, farming resumed its northward advance, although the advance was now much more a matter of people adopting farming rather than being replaced by farmers.

·         Meanwhile, around 5,400 years ago, some hunter-gatherers in the Don-Volga area adopted pastoralism and began to expand westward into Europe and southeastward into the Middle East, Central Asia, and South Asia. They may have been ancestral Indo-Europeans.

 

How much did each of the three groups contribute to the European gene pool? Which group contributed the most and which the least? The question is hard to answer, for three reasons:

 

Double counting

 

The hunter-gatherers of Mesolithic Europe contributed to the present European gene pool both directly and indirectly. The steppe pastoralists were themselves indigenous hunter-gatherers who had adopted pastoralism, plus an admixture of up to 18% from Anatolian farmers. As the Anatolian farmers pushed into Europe, they became gradually “Europeanized” through intermixture with local hunter-gatherers. It is also possible that the Anatolian farmers were themselves the product of an earlier expansion of European hunter-gatherers into the Middle East (Frost 2014).

 

Founder events

 

We measure population replacement by measuring the degree of genetic difference between the original group and the one that replaced it. Is that a valid method? Let’s take the replacement of hunter-gatherers by farmers, and let’s assume that all of the farmers were descended from hunter-gatherers who had adopted farming. The two groups would still be genetically different. The farmers would have been the product of a founder event—a small and genetically unrepresentative group of hunter-gatherers who had decided to take up farming.

 

Differences in natural selection

 

Population replacement is hard to measure for another reason: hunter-gatherers and farmers lived under different regimes of natural selection. They were selected for their ability to adapt to different diets, types of shelter, and means of subsistence. To go from one way of life to the other required not only cultural change but also genetic change.

 

For instance, the population frequency of haplogroup U shows a sharp break at the time boundary between late hunter-gatherers and early farmers (Bramanti et al. 2009). That break strongly suggests that the original Europeans were largely replaced by farmers spreading into Europe from the Middle East. Yet haplogroup U would persist in Denmark at high frequencies long after the transition to farming (Melchior et al. 2010). In Latvia and Ukraine it would persist into Neolithic times (Jones et al. 2017). Haplogroup U probably disappeared from the European gene pool because it ceased to be adaptive. It has been shown to shift the energy balance away from ATP synthesis and toward production of body heat, a useful adaptation if you sleep in makeshift shelters and pursue game in all kinds of weather (Balloux et al. 2009; Montiel-Sosa et al. 2006). It’s less useful if you sleep in a warmer environment and can plan your outdoor activities.

 

Conclusion

 

Whenever I make this argument, the counter-argument is that founder events and natural selection could not possibly explain all of the genetic difference we see between late hunter-gatherers and early farmers in Europe. I agree. I’m just saying that the magnitude of the demographic replacement has been overestimated.

 

References

 

Balloux F., L.J. Handley, T. Jombart, H. Liu, and A. Manica. (2009). Climate shaped the worldwide distribution of human mitochondrial DNA sequence variation. Proceedings of the Royal Society B. Biological Sciences 276: 3447-3455.

https://doi.org/10.1098/rspb.2009.0752

 

Bramanti, B., M.G. Thomas, W. Haak, M. Unterlaender, P. Jores, K. Tambets, I. Antanaitis-Jacobs, M.N. Haidle, R. Jankauskas, C.J. Kind, et al. (2009). Genetic discontinuity between local hunter-gatherers and Central Europe's first farmers. Science 326: 137-140. https://doi.org/10.1126/science.1176869

 

Cochran, G., J. Hardy, and H. Harpending. (2006). Natural history of Ashkenazi intelligence. Journal of Biosocial Science 38(5): 659-693. https://doi.org/10.1017/S0021932005027069

 

Diamond, J.M. (1994). Jewish Lysosomes. Nature 368: 291-292. https://doi.org/10.1038/368291a0

 

Frost, P. (2014). The new European phenotype: expansion into the Middle East. Evo and Proud, January 25. https://evoandproud.blogspot.com/2014/01/the-new-european-phenotype-expansion.html

 

Jones, E.R., G. Zarina, V. Moiseyev, E. Lightfoot, P.R. Nigst, A. Manica, et al. (2017). The Neolithic transition in the Baltic was not driven by admixture with early European farmers, Current Biology 27(4): 576-582.

https://doi.org/10.1016/j.cub.2016.12.060

 

Melchior, L., N. Lynnerup, H.R. Siegismund, T. Kivisild, and J. Dissing. (2010). Genetic diversity among ancient Nordic populations. PLoS One 5(7): e11898

https://doi.org/10.1371/journal.pone.0011898

 

Montiel-Sosa, F., E. Ruiz-Pesini, J.A. Enriquez, A. Marcuello, C. Diez-Sanchez, J. Montoya, D.J. Wallace, and M.J. López-Pérez, (2006). Differences of sperm motility in mitochondrial DNA haplogroup U sublineages. Gene 368: 21-27.

https://doi.org/10.1016/j.gene.2005.09.015

 

Narasimhan, V.M., N. Patterson, P. Moorjani, N. Rohland, R. Bernardos, S. Mallick, I. Lazaridis, et al. (2019). The formation of human populations in South and Central Asia. Science 6: 365(6457): eaat7487. https://doi.org/10.1126/science.aat7487  

 

Tournebize, R., G. Chu, and P. Moorjani. (2022). Reconstructing the history of founder events using genome-wide patterns of allele sharing across individuals. PLoS Genet 18(6): e1010243. https://doi.org/10.1371/journal.pgen.1010243

Declining intelligence in the 20th century: the case of Estonia

Soviet-era stamp. In Estonia, cranial volume shrank between the cohort of girls born in 1937 and those born in 1962, apparently because the intellectually gifted were more likely to pursue higher education and postpone childbearing.

 

Is the genetic basis for intelligence declining from one generation to the next? That’s the conclusion of several recent studies on alleles associated with high educational attainment. By adding up such alleles over the genome, we can get a person's "polygenic score." By calculating the mean polygenic score for each generation, we can then find out whether this genetic basis is declining.

The polygenic score has declined among Icelanders since the cohort born in 1910 and among Euro Americans between the 1931 and 1953 cohorts (Beauchamp 2016; Kong et al. 2017). The Icelandic study is especially interesting because that country took in very few immigrants during the period under study. The decline was thus driven by internal factors. One reason seems to be the tendency of university-educated people to delay reproduction and have fewer children. But that's not the whole story. Even among Icelanders who didn’t pursue higher education, fertility was lower among the intellectually gifted, apparently because their intelligence was associated with a desire to plan for the future and delay gratification.

Before the twentieth century, such forward-looking people were reproductively successful. They were the ones who had enough resources to survive disasters of one sort or another: famine, disease, the Little Ice Age, etc. Today, such disasters are a lot less deadly, and it no longer matters so much whether one is a grasshopper or an ant.

Moreover, because of demographic and cultural changes during the twentieth century, it’s no longer possible to count on the same degree of assistance for child-raising from relatives and grandparents. With childbearing at later ages, grandparents are either dead or too frail to help. With people moving around more, not all relatives live nearby. If you’re the sort of person who plans for the future and delays gratification, you may be a lot more intimidated than your forbears by the costs of raising a family.

Shrinking cranial volume in Estonians

Cranial volume correlates with IQ and with educational attainment, albeit imperfectly (see Frost 2020). Has it been declining in tandem with the decline in alleles for educational attainment?

In Soviet-era Estonia, cranial volume was one of several anthropometric traits that were measured in girls born between 1937 and 1962. Because the measurements were mandatory, there was no volunteer basis; mortality bias was minimal because all the participants were younger than 20. In this respect, the study is better than Western biobank studies. On the other hand, the results may be less applicable to Western populations, given the differences in demographic history. Estonia had no postwar baby boom. Fertility then rose from the late 1960s until the breakup of the Soviet Union. By the late 1980s, fertility was actually higher in Estonia than in any other major region of Europe.

Nonetheless, there were demographic similarities between Soviet Estonia and the West, particularly the rising prevalence of single mothers and the influence of education on fertility:

- Divorce rates began to rise during the interwar years, equalling or exceeding those of Scandinavia from the 1970s onward.

- Throughout the twentieth century, Estonian women with only primary education bore 0.5 to 0.75 more children on average than women with tertiary education. In the population under study, taller children and those with larger crania were more likely to go on to secondary and/or tertiary education, independently of sex, socioeconomic position, and rural vs urban origin (Valge et al. 2019).

The second factor seems to explain why cranial volume declined from the older cohorts to the younger ones:

[...] the majority of selection for smaller cranial volume acted indirectly via educational attainment, whereas the direct path of selection in the SEM model was non-significant (Figs. 2 and 4). In other words, consistent with our prior expectations, girls with larger heads were selected against because they were more likely to obtain higher education than girls with smaller heads. Lower education (Tiit, 2013) and rural origin (Kulu, 2005) have been independently and additively associated with higher fertility in Estonia throughout the past century. The reason for the link between education and fertility is that early reproduction, a major determinant of LRS, is not compatible with schooling for both cultural and genetic reasons. (Valge 2020)

 It is doubtful that this decline is due to ethnic change. All of the girls were from Estonian schools (Russian-speakers had their own schools). Nonetheless some of them were of mixed background. According to a personal communication from the corresponding author, 84% of the fathers and 93% of the mothers were Estonian. Ideally, the study should be redone without individuals of mixed parentage. The problem here is not only that one of the parents was non-Estonian but also that such individuals were disproportionately economic migrants who had trouble finding suitable work elsewhere in the Soviet Union.

Other anthropomorphic changes

Height also declined. Unlike cranial volume, this decline was not wholly explained by educational/socioeconomic differences:

Notably, higher reproductive success of shorter girls in Estonia could not be entirely ascribed to indirect selection via educational attainment, nor via other measured socioeconomic variables such as rural/urban origin, although indirect selection via education did account for a large portion of total selection (Fig. 4). The finding that selection against height remains after controlling for education or income (that favours less-educated individuals who are generally shorter than highly-educated ones) is consistent with findings of studies reviewed by Stulp and Barrett (2016).

 

Female hips and female jaws became narrower even after controlling for educational/socioeconomic differences. There seems to have been selection for rounder female faces, but this selection is significant only if one allows for nonlinear effects. Finally, there was no direct selection on two markers of overall health and nutritional status: handgrip strength and lung capacity.

In general, "direct selection favoured shorter, slimmer and lighter girls with smaller heads, more masculine facial and body shapes and slower rates of sexual maturation."

Conclusion

The genetic basis for intelligence has declined in European populations, apparently since the early twentieth century. This decline is attested by two "hard" measures: 1) alleles associated with educational attainment; and 2) cranial volume. Furthermore, it is attested in two relatively homogenous societies, i.e., Iceland and Estonia.

In Estonia, the decline seems entirely due to the intellectually gifted going to university and postponing family formation. In Iceland, this factor explains only part of the decline: the intellectually gifted chose to postpone family formation even when they didn't go to university. Perhaps the Soviet system was better at steering gifted individuals into higher education.

On a final note, this problem will not go away on its own. If we wish to have large numbers of intellectually gifted people who plan for the future and delay gratification, we will need to reverse certain social and cultural changes of the twentieth century.

Comments by Peeter Horak

In an email, Peeter pointed out that the decrease in height due to natural selection might be offset by an increase in height due to lower pathogen load (as a result of vaccination and antibiotics, see Hõrak and Valge 2015). In addition, we currently don't know the direction of selection on boys. It may entirely cancel out natural selection on girls if men's income and education correlate positively with their reproductive success. In the sample under study, taller boys and those with larger heads went on to obtain more education; if they were reproductively successful, there would be sexually antagonistic selection: selection would favor larger boys and smaller girls at the same time.

References

Beauchamp, J.P. (2016). Genetic evidence for natural selection in humans in the contemporary United States. Proceedings of the National Academy of Sciences 113(28): 7774-7779 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4948342/

Frost, P. (2020). Did women jumpstart recent cognitive evolution? Evo and Proud, July 1 https://evoandproud.blogspot.com/2020/07/did-women-jumpstart-recent-cognitive.html

Hõrak, P., and M. Valge. (2015). Why did children grow so well at hard times? The ultimate importance of pathogen control during puberty, Evolution, Medicine, and Public Health, 2015 (1): 167–178, https://doi.org/10.1093/emph/eov017

Kong, A., M.L. Frigge, G. Thorleifsson, H. Stefansson, A.I. Young, F. Zink, G.A. Jonsdottir, A. Okbay, P. Sulem, G. Masson, D.F. Gudbjartsson, A. Helgason, G. Bjornsdottir, U. Thorsteinsdottir, and K. Stefansson. (2017). Selection against variants in the genome associated with educational attainment. Proceedings of the National Academy of Sciences 114(5): E727-E732 https://core.ac.uk/download/pdf/154416179.pdf

Valge, M., P. Horak, and J.M. Henshaw. (2020). Natural selection on anthropometric traits of Estonian girls. Evolution and Human Behavior in press. https://doi.org/10.1016/j.evolhumbehav.2020.07.013

Valge, M, R. Meitern, and P. Horak. (2019). Morphometric traits predict educational attainment independently of socioeconomic background. BMC Public Health 19: 1696. https://link.springer.com/article/10.1186/s12889-019-8072-7

Replacement or continuity?

 

Inuit meat cache, Kazan River (source: Library and Archives Canada / PA-101294). Because of their high meat diet, hunters produce more body heat than farmers do. Natural selection has thus favored certain mtDNA sequences over others in humans with this profile of heat production. A change in selection pressure may therefore explain, at least in part, the genetic divide between late hunter-gatherers and early farmers in Europe.

 

Who were the ancestors of present-day Europeans? The hunter-gatherers of the Paleolithic and the Mesolithic? Or the Neolithic farmers who began to spread out of the Middle East some 10,000 years ago?

This debate has teetered back and forth for the past thirty years. On the basis of various genetic polymorphisms, L.L. Cavalli-Sforza and his students argued that Europeans are largely descended from Middle Eastern farmers (Ammerman and Cavalli-Sforza, 1984; Cavalli-Sforza et al., 1994). On the basis of mtDNA and Y chromosomal data, two other research teams, one led by Martin Richards and the other by Ornella Semino, maintained that the European gene pool is over 75% of native hunter-gatherer origin (Richards et al., 2000; Semino et al., 2000). If we look only at the present-day gene pool, Europeans seem far too differentiated to be the descendants of Neolithic farmers from the Middle East.

Over the last few years, new evidence has swung the debate back to the model of population replacement. By retrieving DNA from ancient skeletal remains, we can now compare the latest hunter-gatherers with the earliest farmers, and what we see is a sharp genetic divide between the two (Bramanti et al., 2009). The farmers seem to have been immigrants who replaced the hunter-gatherers. This is direct evidence, so what more is there to say? Facts are facts.

Yet there is always more to say. Facts may be illusory or, if real, wrongly interpreted. For one thing, wherever we have a fairly continuous time series of ancient DNA, the genetic divide no longer appears between the latest hunter-gatherers and the earliest farmers. It appears between the earliest farmers and somewhat later farmers. This is particularly so when we examine haplogroup U lineages, whose disappearance is widely seen as evidence for population replacement. According to a study of 92 Danish remains, these lineages remained common after the Neolithic and reached their current low prevalence only during the Early Iron Age (Melchior et al., 2010).

If this genetic divide is not solely due to population replacement, what else might be responsible? Mishmar et al. (2003) were the first to suggest natural selection:

Thus, extensive global population studies have shown that there are striking differences in the nature of the mtDNAs found in different geographic regions. Previously, these marked differences in mtDNA haplogroup distribution were attributed to founder effects, specifically the colonizing of new geographic regions by only a few immigrants that contributed a limited number of mtDNAs. However, this model is difficult to reconcile with the fact that northeastern Africa harbors all of the African-specific mtDNA lineages as well as the progenitors of the Eurasia radiation, yet only two mtDNA lineages (macrohaplogroups M and N) left northeastern Africa to colonize all of Eurasia (1, 2) and also that there is a striking discontinuity in the frequency of haplogroups A, C, D, and G between central Asia and Siberia, regions that are contiguous over thousands of kilometers. Rather than Eurasia and Siberia being colonized by a limited number of founders, it seems more likely that environmental factors enriched for certain mtDNA lineages as humans moved to the more northern latitudes.

[...] We now hypothesize that natural selection may have influenced the regional differences between mtDNA lineages. This hypothesis is supported by our demonstration of striking differences in the ratio of nonsynonymous (nsyn)/synonymous (syn) nucleotide changes in mtDNA genes between geographic regions in different latitudes. We speculate that these differences may reflect the ancient adaptation of our ancestors to increasingly colder climates as Homo sapiens migrated out of Africa and into Europe and northeastern Asia.

This hypothesis has since received support from Balloux et al. (2009):

We show that populations living in colder environments have lower mitochondrial diversity and that the genetic differentiation between pairs of populations correlates with difference in temperature. These associations were unique to mtDNA; we could not find a similar pattern in any other genetic marker. We were able to identify two correlated non-synonymous point mutations in the ND₃ and ATP6 genes characterized by a clear association with temperature, which appear to be plausible targets of natural selection producing the association with climate. The same mutations have been previously shown to be associated with variation in mitochondrial pH and calcium dynamics. Our results indicate that natural selection mediated by climate has contributed to shape the current distribution of mtDNA sequences in humans.

Humans have to adapt to two sources of warmth: climate and internal body heat, which in turn varies with lifestyle and diet. Diet in particular results in different patterns of body heat production between hunter-gatherers and farmers, as explained by Speth (1983):

One aspect of protein metabolism relevant to this issue concerns the high "specific dynamic action" (SDA) of protein ingestion. The SDA of food refers to the rise in metabolism or heat production (diet-induced thermogenesis) resulting from the ingestion of food [...] The SDA of a diet consisting largely of fat is about 6- 14%, while that of a diet high in carbohydrates is about 6%. In striking contrast, the SDA of a diet consisting almost entirely of protein may be as high as 30%; or, in other words, for every 100 calories of protein ingested, up to 30 calories are needed to compensate for the increase in metabolism. Thus, persons whose diets are high in protein experience higher metabolic rates than those whose diets are composed largely of carbohydrate. For example, members of Eskimo populations, at least 90% of whose caloric needs were traditionally met by meat and fat (cf. Draper 1980:263; Hoygaard 1941), had basal metabolic rates 13 to 33% above the DuBois standard, which is based on the metabolic rates of populations consuming western diets (Itoh 1980:285).

Conclusion

Before ancient DNA became available, the prehistory of populations had to be inferred. The age of a genetic lineage was inferred from the degree of differentiation divided by the mutation rate. Since both variables could be known only approximately, the time depths of Europe's genetic lineages were likewise known only approximately.

Ancient DNA seems to promise a clearer picture because the only source of uncertainty is the age of the skeletal material. Unfortunately, this new method is more sensitive to uncertainty from another source: natural selection. Late hunter-gatherers and early farmers had to adapt to different environments. There certainly was a genetic divide between the two, but did it result from differences in origin or from differences in natural selection?

Natural selection distorts the picture if either method is used, since both assume that mtDNA is selectively neutral. The distortion is more serious, however, with the new method, which assumes selective neutrality across the genetic divide between late hunter-gatherers and early farmers—the very moment in prehistory when this assumption is most likely to fail. The old method assumes selective neutrality throughout the entire time depth of Europe’s genetic lineages—an assumption that may indeed be true over most of that time.

Even if the lineage has no selective value in and of itself, natural selection can still distort the picture. This is especially so for mtDNA:

Selection can change allele frequency even at a locus not responsible for fitness differences. Because there is little or no recombination in mitochondrial DNA, selection at one nucleotide affects the frequencies of all other variable nucleotides for the whole molecule. Selection on the nuclear genome, particularly nuclear-encoded proteins that are imported into the mitochondrion and X-linked markers that can have a high effective linkage to mtDNA, can also cause changes in the frequencies of mtDNA haplotypes. Equally importantly, selection on any other cytoplasmically inherited traits will directly affect the frequencies of mtDNA. (Ballard and Whitlock, 2004)

This is less of a problem with nuclear DNA because of recombination, but the problem remains if the presumably neutral gene is close to another gene of high selective value.

In raising these points, I am not trying to argue that Middle Eastern farmers made no contribution to the European gene pool. There is good archaeological evidence of these farmers pushing up the Danube and into central Europe. Elsewhere, however, the evidence for population replacement becomes weaker and the evidence for continuity correspondingly stronger. This is the conclusion that Zvelebil and Dolukhanov (1991) make with respect to northern and eastern Europe:

The transition to farming occurred very slowly and took a long time to complete, the whole process lasting 1500-4000 years. In the far north and northeast of Europe, the process was never completed. [...] Local hunter-gatherer societies played a significant role in the transition. There is strong evidence for continuity in material culture in most regions throughout the transition. Although this neither proves nor disproves the case for population movement associated with the transition (small groups of people could have migrated, leaving little or no trace in the archaeological record), such evidence does not support the colonization model for the transition to farming and it does indicate that local hunter-gatherer traditions were passed on from generation to generation during the long period of the adoption of farming.

And yet the advent of farming brought massive genetic change to northern and eastern Europe, including widespread decline of haplogroup U—the sort of change that is supposed to mean massive population replacement. Since farming began to spread to this region only 6,000 years ago, even later among the Finnish and Baltic peoples, there is only a very narrow time frame in which northern and eastern Europeans could have evolved their characteristic physical appearance, assuming of course that population replacement had actually happened.

Even in central Europe, where population replacement is well documented, we are still unsure whether it was permanent or temporary. Indeed, we see evidence of the replacers being later replaced, perhaps by natives who had never disappeared from the vicinity of the farming settlements (Haak et al., 2005; Rowley-Conwy, 2011).

 

References

Ammerman, A.J. and L.L. Cavalli-Sforza. (1984). The Neolithic Transition and the Genetics of Populations in Europe, New Jersey: Princeton University Press.

Ballard, J.W.O. and M.C. Whitlock. (2004). The incomplete natural history of mitochondria, Molecular Ecology, 13, 729-744.

http://dna.ac/filogeografia/PDFs/Ballard%26Whitlock_04_MTrev.pdf

Balloux F., L.J. Handley, T. Jombart, H. Liu, and A. Manica (2009). Climate shaped the worldwide distribution of human mitochondrial DNA sequence variation. Proceedings. Biological Sciences, 276 (1672), 3447-55.

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2817182/?tool=pmcentrez

Bramanti, B., M. G. Thomas, W. Haak, M. Unterlaender, P. Jores, K. Tambets, I. Antanaitis-Jacobs, M.N. Haidle, R. Jankauskas, C.-J. Kind, F. Lueth, T. Terberger, J. Hiller, S. Matsumura, P. Forster, and J. Burger. (2009). Genetic discontinuity between local hunter-gatherers and Central Europe's first farmers, Science, 326 (5949), 137-140.

http://jsarf.free.fr/palanthsci/Europe's%20First%20Farmers%20Were%20Immigrants.pdf

Cavalli-Sforza, L.L., P. Menozzi, and A. Piazza. (1994). The History and Geography of Human Genes, New Jersey: Princeton University Press.

Haak, W., P. Forster, B. Bramanti, S. Matsumura, G. Brandt, M. Tänzer, R. Villems, C. Renfrew, D. Gronenborn, K.W. Alt, and J. Burger. (2005). Ancient DNA from the first European farmers in 7500-year-old Neolithic sites, Science, 310 (5750), 1016-1018.

http://www.sciencemag.org/content/310/5750/1016.short

Melchior, L., N. Lynnerup, H.R. Siegismund, T. Kivisild, J. Dissing. (2010). Genetic diversity among ancient Nordic populations, PLoS ONE, 5(7): e11898

http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0011898#pone-0011898-g002

Mishmar, D., E. Ruiz-Pesini, P. Golik, V. Macaulay, A.G. Clark, S. Hosseini, M. Brandon, K. Easley, E. Chen, M.D. Brown, R.I. Sukernik, A. Olckers, and D.C. Wallace. (2003). Natural selection shaped regional mtDNA variation in humans, Proceedings of the National Academy of Sciences (USA), 100 (1), 171-176.

http://www.pnas.org/content/100/1/171.full

Richards, M., V. Macaulay, E. Hickey, E. Vega, B. Sykes, et al. (2000). Tracing European founder lineages in the Near Eastern mtDNA pool, American Journal of Human Genetics, 67, 1251-1276.

http://www.sciencedirect.com/science/article/pii/S0002929707629541

Rowley-Conwy, P. (2011). Westward ho! The spread of agriculturalism from Central Europe to the Atlantic, Current Anthropology, 52 (S4), S431-S451.

http://arkeobotanika.pbworks.com/w/file/fetch/48307263/Rowley-Conwy%2011%20CA%20Farming%20westward.pdf

Semino, O., G. Passarino, P.J. Oefner, A.A. Lin, S. Arbuzova, et al. (2000). The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: A Y chromosome perspective, Science, 290, 1155-1159.

http://fboekelo.tripod.com/boekelo/GP/semino.pdf

Speth, J.D. (1983). Energy source, protein metabolism, and hunter-gatherer subsistence strategies, Journal of Anthropological Archaeology, 2, 1-31.

http://faculty.ksu.edu.sa/archaeology/Publications/Hearths/Energy%20source,%20protein%20metabolism,%20and%20hunter-gatherer%20subsistence%20strategies.pdf

Zvelebil, M. and P. Dolukhanov. (1991). The transition to farming in Eastern and Northern Europe, Journal of World Prehistory, 5, 233-278.

http://link.springer.com/article/10.1007/BF00974991

Apples, oranges, and genes

Publicly funded misinformation. Source: PBS website

In human genetics, a ‘population’ is a group of individuals who share ancestry and hence genes. This sharing is not absolute. There is always some gene flow from outside, and sometimes “outside” means another species. We humans, for example, have received genes not only from Neanderthals and Denisovans but also from … viruses.

In addition, new gene variants are constantly arising through mutation. Most of them are harmful or useless. But some are useful and will thus spread through the population.

So below the species level, and often even at the species level, population boundaries tend to be fuzzy. Genes vary both between and within populations.

You’ve undoubtedly heard that there is much more genetic variation within human populations than between them, this being true even for the large continental populations we used to call ‘races.’ This was the finding of the geneticist Richard Lewontin (1972), and others have concluded likewise. You’ve probably not heard, however, that the same kind of genetic overlap exists between many sibling species that are nonetheless distinct in anatomy and behavior (Frost, 2011).

How come? First, keep in mind that genes vary a lot in adaptive value. Some are little more than ‘junk DNA.’ Others code for structural proteins that form the building blocks of flesh and blood. Others still are very important because they code for regulatory proteins that control how other genes behave and, hence, the way an organism grows and develops. The last kind of gene accounts for only a tiny fraction of the genome. Most genes have modest effects, or none at all.

Second, keep in mind that different populations occupy different environments and are thus exposed to differences in natural selection. In most species, these differences are due to physical environments that differ in climate, vegetation, and wildlife. Humans also have to adapt to cultural environments that differ in social structure, belief systems, and technology. In either case, when a gene varies between two populations the cause is probably a difference in natural selection, since the population boundary also separates different selection pressures. Conversely, when a gene varies within a population this variation is less likely to have adaptive significance. It hasn’t been flattened out by the steamroller of similar selection pressures.

This is one aspect of “Lewontin’s fallacy.” Within-population variation isn’t comparable to between-population variation. It’s like comparing apples and oranges.

Another aspect of Lewontin’s fallacy is that natural selection within a population exercises a leveling effect only on phenotypes, and not on genotypes. If two gene variants have a similar phenotypic effect, natural selection will take longer to replace one with the other. Sometimes, this sort of diversity will persist indefinitely because epidemics often spare individuals whose surface proteins are somewhat different from those of their neighbors.

Thus, within-population variation tends to consist of different gene variants at different loci whose effects nonetheless point in the same general direction. To some degree, these variants can stand in for each other. If one is absent, another one might do the trick. This is probably why population differences are more sharply defined if several gene loci are compared simultaneously. If we chart how each gene varies geographically and then superimpose these maps on top of each other, the resulting composite map will show population differences in sharper relief (Edwards, 2003; Mitton, 1977; Mitton, 1978; Sesardic, 2010).

This point has been made by Emmanuel Milot, the principal author of the paper I reviewed in my last post. His research team found that the time between marriage and first birth steadily shrank among succeeding generations of French Canadians on Île aux Coudres (Milot et al., 2011). In the land-rich environment of the New World, there was strong selection for married women to get pregnant faster. A genetic difference has thus developed between French Canadians and the French who remained in France.

But this difference is not due to a few genes. As Milot points out, natural selection tends to produce effects at many different genes:

“We should not think that there are genes that code specifically for age at first reproduction. In fact, this type of trait is probably influenced by hundreds, even thousands, of genes. These genes act on other characteristics, like body weight at birth, age at first menstruation, or even personality traits, which impact on age at first birth” (Bourdon, 2011)

This point is important. If two populations differ at one gene, and if the difference is sensitive to natural selection, they probably also differ at many other genes. The same selection pressure that caused one difference has almost certainly caused others. Typically, we see only the tip of the iceberg—a gene variant that produces an obvious effect in affected individuals, such as illness. Most gene variants, however, don’t cause medically recognized illnesses, and their effects also tend to be subtler.

References

Bourdon, M-C. (2011). L’espèce humaine. Toujours en évolution. UQAM. Entrevues
http://www.uqam.ca/entrevues/entrevue.php?id=965

Edwards, A.W.F. (2003). Human genetic diversity: Lewontin’s fallacy. BioEssays, 25, 798-801.

Frost, P. (2011). Human nature or human natures? Futures, 43, 740-748. http://dx.doi.org/10.1016/j.futures.2011.05.017

Lewontin, R.C. (1972). The apportionment of human diversity. Evolutionary Biology, 6, 381-398.

Milot, E., F.M. Mayer, D.H. Nussey, M. Boisvert, F. Pelletier, and D. Réale. (2011). Evidence for evolution in response to natural selection in a contemporary human population, Proceedings of the National Academy of Sciences (USA), early view

Mitton, J.B. (1977). Genetic differentiation of races of man as judged by single-locus and multilocus analyses, American Naturalist, 111, 203-212.

Mitton, J.B. (1978). Measurement of differentiation: reply to Lewontin, Powell, and Taylor, American Naturalist, 112, 1142-1144.

Sesardic, N. (2010). Race: a social destruction of a biological concept, Biology and Philosophy, 25(2), 143-162.

The rising curve

It was long thought that human genetic evolution pretty much ended with the advent of culture. As Paul Ehrlich (2000, p. 63) wrote:

The evolution of that body of extragenetic information—cultural evolution—has been centrally important in making us the unique beasts we are. Cultural evolution rests on a foundation of genetic (or biological) evolution—especially that of our brains and tongues—but can proceed at what by comparison is a lightning pace. … cultural evolution can vastly outpace genetic evolution because it’s not constrained by generation time. Our genes are passed only from one generation to relatives in succeeding generations. In contrast, the units of culture—ideas, basically—are passed among both relatives and nonrelatives not only between generations (in both
directions) but also within generations.

So did cultural evolution make genetic evolution obsolete? Paul Ehrlich seemed to draw this conclusion … only to pull himself back. “There are many ways in which culture can alter selection pressures,” he says, noting that genes have co-evolved with changes to diet, farming practices, and shelter (Ehrlich, 2000, p. 64). Indeed, the same properties that make cultural evolution so fast have also been diversifying the adaptive landscape at an unparalleled rate. Whenever our species came up with a cultural innovation—a new technology, domestication of a plant or animal, or the advent of agriculture itself—our environment changed as fundamentally as if we had moved to a new ecosystem.

So which factor has mattered most in determining the pace of human genetic evolution? Has cultural evolution been resolving more and more adaptive problems that were formerly resolved by genetic evolution? Or has genetic evolution been resolving more and more adaptive problems because human environments have been diversifying more and more?

The second factor, apparently. A recent study has concluded that genetic evolution has actually accelerated over the past 40,000 years and even more over the past 10,000-15,000. This is partly because there are many more of us and partly because we are spread over an increasingly diverse range of natural and man-made environments. At least 7% of the human genome appears to have changed since the advent of Homo sapiens. And the rate of change has increased a 100-fold since the advent of agriculture (Hawks et al., 2007).

These are high numbers. As one of the study’s authors observes:

Personally, I can't believe that nobody noticed how extreme these estimates of recent selection really are. I guess that folks doing genomics just weren't as primed in evolutionary theory to perceive how weird the human estimates looked compared to what is measured in the wild on other species, or even over the span of human evolution!

In the earliest studies, when people were finding that 3 or 4 percent of a sample of genes had signs of recent selection, those numbers were already extremely high. They got even higher, as more and more powerful methods of detecting selection came online. Our current estimate is the highest yet, but even this very high number is perfectly consistent with theoretical predictions coming from human population numbers.

These figures, if anything, err on the low side. They do not capture recent selective pressures that are just emerging above noise in the data. Nor do they capture older selective pressures that have already pushed many alleles to fixation. The real figures won’t become known until we’ve retrieved the human genome that existed 40,000 years ago—something that is certainly within the realm of possibility.

All this underlines a point I made in an earlier post: human evolution is not a straight line. It’s a logarithmic curve with most of the evolutionary change in the recent past. If we met a Homo erectus face to face, or even a Neanderthal (who was probably just an arctic-adapted Homo erectus), we wouldn’t consider it to be human. It would look to us like an overgrown ape. Nor would its behavior reassure us otherwise.


References

Ehrlich, P.R. (2000). Human Natures. Genes, Cultures, and the Human Prospect. Penguin: New York.

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 Sciences (USA), 104(52), 20753-20758.