A mitochondrion (source). Is mitochondrial DNA selectively neutral?
Were Ice Age Europeans a dead end, like the Neanderthals before them? Did Middle Eastern farmers replace indigenous hunter-gatherers, just as Europeans would later replace native Indians in North America?
This debate has been raging back and forth for some time, but it has now entered a new phase with retrieval of mtDNA from ancient European skeletons. We can now genetically compare late hunter-gatherers with early farmers. We can now ask the question: Which of them were the ancestors of modern Europeans?
This kind of comparison has recently been made in Sweden, where farming replaced hunting/gathering/fishing some 5,000 years ago. This is the time depth for mtDNA retrieved from two burial sites: a farming community in Gökhem parish (one individual) and a hunter-gatherer community on the island of Gotland (three individuals). The results?
The Neolithic hunter-gatherers shared most alleles with northern Europeans, and the lowest allele sharing was with populations from southeastern Europe. In contrast, the Neolithic farmer shared the greatest fraction of alleles with southeastern European populations (Cypriots and Greeks) and showed a pattern of decreasing genetic similarity to populations from the northwest and northeast extremes of Europe (Skoglund etal., 2012)
The authors then went on to estimate the degree of admixture from Middle Eastern farmers in present-day Europeans:
We estimated that people of southern, central and northern Swedish descent are, on average, of 41 ± 8%, 36 ± 7%, and 31 ± 6% Neolithic farmer–related ancestry, respectively (±1 SE). Across Europe, this fraction decreases from 95 ± 13% in Sardinians to 52 ± 8% in the CEU population (individuals of northwestern European descent) and 11 ± 4% in Russians (Skoglund et al., 2012)
So, according to this study, northern Europeans are mainly descended from the hunter-gatherers of Ice Age Europe. But there is also substantial admixture from those Middle Eastern farmers—roughly a third of the present-day Swedish gene pool.
Is this the last word? No, the debate will surely continue. For one thing, the sample sizes are still small. For another, the replacement of hunter-gatherers by farmers may have played out differently in different places.
But there is a more fundamental objection. All of this assumes that we have a reliable yardstick for measuring admixture. For this to be so, mtDNA must not be influenced by natural selection. In particular, it must not be influenced by the change in selection pressures that occurs when hunting and gathering give way to farming. Is this assumption valid?
When we compare late hunter-gatherers with present-day Europeans, the main change to mtDNA is the loss of haplogroup U. Indeed, if this haplogroup had not declined to its current low levels, the above admixture estimates would be minimal.
Today, haplogroup U reaches high levels only among the Saami of Finland and the Mansi of northwestern Siberia, both of whom were hunter-gatherers until recently (Derbeneva et al, 2002). Did something about that lifestyle favor this haplogroup?
Balloux et al. (2009) have argued that some haplogroups create different trade-offs between thermogenesis and ATP synthesis. In particular, haplogroup U is associated with reduced sperm motility—an indication that the energy balance is shifted from producing ATP to producing heat:
The ATP that drives the sperm flagella is derived from the mitochondria located in the midpiece. Therefore, mutations in the mtDNA which increase or decrease ATP production will be reflected in increased or decreased sperm motility.
[…] Therefore, shifting the energy balance from primarily ATP production to increased heat production could explain the lower sperm motility and the predilection of these sublineages U to reside in colder climates and their northern distribution. (Montiel-Sosa et al., 2006)
Being nomadic, hunter-gatherers spent more time in the cold, especially when sleeping in temporary shelters. Farming brought more sedentary living and a generally warmer sleeping environment. There would thus have been weaker natural selection for genetic variants, like haplogroup U, that maintain a higher body temperature at the expense of lower ATP production.
This hypothesis is testable. If haplogroup U disappeared because Middle Eastern farmers partially replaced native hunter-gatherers, this genetic change should largely coincide with the time boundary between late hunter-gatherers and early farmers. If this haplogroup disappeared through natural selection, the change should have occurred gradually over a longer period.
The second scenario seems closer to the truth. In a study of 92 Danish human remains that ranged in time from the Mesolithic to the Middle Ages, Melchior et al. (2010) found that high incidences of haplogroup U persisted long after the advent of farming and apparently as late as the Early Iron Age.
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.
Derbeneva, O.A., E.B. Starikovskaya, D.C. Wallace, & R.I. Sukernik. (2002). Traces of early Eurasians in the Mansi of Northwest Siberia revealed by mitochondrial DNA analysis, Am. J. Hum. Genet. 70:1009–1014.
Melchior, L., N. Lynnerup, H.R. Siegismund, T. Kivisild, J. Dissing. (2010). Genetic diversity among ancient Nordic populations, PLoS ONE, 5(7): e11898
Montiel-Sosa, F., E. Ruiz-Pesini, J.A. Enríquez, A. Marcuello, C. Díez-Sánchez, J. Montoya, D.C. Wallace, & M.J. López-Pérez. (2006). Differences of sperm motility in mitochondrial DNA haplogroup U sublineages, Gene, 368, 21–27.
Skoglund, P., H. Malmström, M. Raghavan, J. Storå, P. Hall, E. Willerslev, M.T. Gilbert, A. Götherström, & M. Jakobsson. (2012). Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe, Science, 336, 466-469.