The Milk Revolution When a Single Genetic Mutation First Let Ancient Europeans Drink Milk, It Set the Stage for a Continental Upheaval
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The milk revolution When a single genetic mutation first let ancient Europeans drink milk, it set the stage for a continental upheaval. BY ANDREW CURRY n the 1970s, archaeologist Peter Bogucki farmers had used the pottery as sieves to sepa- that gave people the ability to produce lactase was excavating a Stone Age site in the fer- rate fatty milk solids from liquid whey. That — and drink milk — throughout their lives. tile plains of central Poland when he came makes the Polish relics the oldest known evi- That adaptation opened up a rich new source I 1 across an assortment of odd artefacts. The dence of cheese-making in the world . of nutrition that could have sustained commu- people who had lived there around 7,000 years Roffet-Salque’s sleuthing is part of a wave of nities when harvests failed. ago were among central Europe’s first farmers, discoveries about the history of milk in Europe. This two-step milk revolution may have and they had left behind fragments of pottery Many of them have come from a €3.3-million been a prime factor in allowing bands of dotted with tiny holes. It looked as though the (US$4.4-million) project that started in 2009 farmers and herders from the south to sweep coarse red clay had been baked while pierced and has involved archaeologists, chemists and through Europe and displace the hunter-gath- with pieces of straw. geneticists. The findings from this group illumi- erer cultures that had lived there for millen- Looking back through the archaeologi- nate the profound ways that dairy products have nia. “They spread really rapidly into northern cal literature, Bogucki found other examples shaped human settlement on the continent. Europe from an archaeological point of view,” of ancient perforated pottery. “They were so During the most recent ice age, milk was says Mark Thomas, a population geneticist at unusual — people would almost always include essentially a toxin to adults because — unlike University College London. That wave of emi- them in publications,” says Bogucki, now at children — they could not produce the lactase gration left an enduring imprint on Europe, Princeton University in New Jersey. He had seen enzyme required to break down lactose, the where, unlike in many regions of the world, something similar at a friend’s house that was main sugar in milk. But as farming started to most people can now tolerate milk. “It could used for straining cheese, so he speculated that replace hunting and gathering in the Middle be that a large proportion of Europeans are the pottery might be connected with cheese- East around 11,000 years ago, cattle herders descended from the first lactase-persistent making. But he had no way to test his idea. learned how to reduce lactose in dairy prod- dairy farmers in Europe,” says Thomas. The mystery potsherds sat in storage until ucts to tolerable levels 2011, when Mélanie Roffet-Salque pulled NATURE.COM by fermenting milk to STRONG STOMACHS them out and analysed fatty residues preserved To hear Mark make cheese or yogurt. Young children almost universally produce in the clay. Roffet-Salque, a geochemist at the Thomas discuss the Several thousand years lactase and can digest the lactose in their University of Bristol, UK, found signatures of milk revolution, visit: later, a genetic mutation mother’s milk. But as they mature, most switch abundant milk fats — evidence that the early go.nature.com/aleyte spread through Europe off the lactase gene. Only 35% of the human 20 | NATURE | VOL 500 | 1 AUGUST 2013 © 2013 Macmillan Publishers Limited. All rights reserved FEATURE NEWS population can digest lactose beyond the age of One strand of evidence came from studies of that dairying in the Middle East may go all the about seven or eight (ref. 2). “If you’re lactose animal bones found at archaeological sites. If way back to when humans first started domes- intolerant and you drink half a pint of milk, cattle are raised primarily for dairying, calves ticating animals there, about 10,500 years ago6. you’re going to be really ill. Explosive diarrhoea are generally slaughtered before their first birth- That would place it just after the Middle East- — dysentery essentially,” says Oliver Craig, an day so that their mothers can be milked. But cat- ern Neolithic transition — when an economy archaeologist at the University of York, UK. “I’m tle raised mainly for meat are killed later, when based on hunter-gathering gave way to one not saying it’s lethal, but it’s quite unpleasant.” they have reached their full size. (The pattern, devoted to agriculture. Dairying, says Roz Most people who retain the ability to digest if not the ages, is similar for sheep and goats, Gillis, also an archaeozoologist at the Paris milk can trace their ancestry to Europe, where which were part of the dairying revolution.) museum, “may have been one of the reasons the trait seems to be linked to a single nucleo- On the basis of studies of growth patterns in why human populations began trapping and tide in which the DNA base cytosine changed bones, LeCHE participant Jean-Denis Vigne, keeping ruminants such as cattle, sheep and to thymine in a genomic region not far from an archaeozoologist at the French National goats”. (See ‘Dairy diaspora’.) the lactase gene. There are other pockets of Museum of Natural History in Paris, suggests Dairying then expanded in concert with lactase persistence in West Africa (see Nature 444, 994–996; 2006), the Middle East and DAIRY DIASPORA south Asia that seem to be linked to separate 3 Dairying practices spread from the Middle East to mutations (see ‘Lactase hotspots’). Europe as part of the Neolithic transition from hunting The single-nucleotide switch in Europe and gathering to agriculture. happened relatively recently. Thomas and his colleagues estimated the timing by looking at genetic variations in modern populations and Piece of a roughly 7,000-year-old running computer simulations of how the sieve used to related genetic mutation might have spread make cheese. through ancient populations4. They proposed MAP SOURCE: REF. 2; POT PHOTOGRAPH: REF. 1 REF. PHOTOGRAPH: 2; POT MAP SOURCE: REF. that the trait of lactase persistence, dubbed the LP allele, emerged about 7,500 years ago in the 6,500 YEA S AGO Well-developed dairy 7,500 YEA S AGO Lactase persistence, the ability to drink milk broad, fertile plains of Hungary. economy established in in adulthood, emerges in central Europe. central Europe. POWERFUL GENE 8,000 YEA S AGO Once the LP allele appeared, it offered a major Neolithic reaches the Balkans. selective advantage. In a 2004 study5, researchers estimated that people with the mutation would 8,400 YEA S AGO have produced up to 19% more fertile offspring Neolithic spreads to Greece. than those who lacked it. The researchers called that degree of selection “among the strongest yet seen for any gene in the genome”. Compounded over several hundred gen- ,000–0,000 YEA S AGO Neolithic culture develops in the Middle erations, that advantage could help a popula- East. This is the start of agriculture and tion to take over a continent. But only if “the possibly the domestication of dairy animals. population has a supply of fresh milk and is dairying”, says Thomas. “It’s gene–culture co- evolution. They feed off of each other.” To investigate the history of that interaction, LACTASE HOTSPOTS Thomas teamed up with Joachim Burger, a Only one-third of people produce the lactase enzyme palaeogeneticist at the Johannes Gutenberg during adulthood, which enables them to drink milk. University of Mainz in Germany, and Matthew Collins, a bioarchaeologist at the University of York. They organized a multidisciplinary project called LeCHE (Lactase Persistence in the early Cultural History of Europe), which brought together a dozen early-career researchers from around Europe. By studying human molecular biology and the archaeology and chemistry of ancient pottery, LeCHE participants also hoped to address a key issue about the origins of mod- ern Europeans. “It’s been an enduring question in archaeology — whether we’re descended from Middle Eastern farmers or indigenous hunter-gatherers,” says Thomas. The argument boils down to evolution versus replacement. Did native populations of hunter-gatherers in Europe take up farming and herding? Or was Percentage of adult population that can drink milk there an influx of agricultural colonists who outcompeted the locals, thanks to a combina- 10% 90% tion of genes and technology? 1 AUGUST 2013 | VOL 500 | NATURE | 21 © 2013 Macmillan Publishers Limited. All rights reserved NEWS FEATURE the Neolithic transition, says Gillis, who has to have required the spread of lactase persis- naturally only when exposed to the sun, which looked at bone growth at 150 sites in Europe tence. The LP allele did not become common makes it difficult for northerners to make and Anatolia (modern Turkey). As agriculture in the population until some time after it first enough during winter months. But lactase per- spread from Anatolia to northern Europe over emerged: Burger has looked for the mutation sistence also took root in sunny Spain, casting roughly two millennia, dairying followed a in samples of ancient human DNA and has vitamin D’s role into doubt. similar pattern. found it only as far back as 6,500 years ago in The LeCHE project may offer a model for On their own, the growth patterns do not northern Germany. how archaeological questions can be answered say whether the Neolithic transition in Europe Models created by LeCHE participant using a variety of disciplines and tools.