Project Outline

Research Background & Aim

Milk is a fraught food, deeply entangled with politics, culture, economics, and history. Seen a universal food since the 1960s, Western medical profession considered the inability to digest milk to be an unfortunate, but uncommon, disease alternately known as primary acquired lactase deficiency, adult hypolactasia, and lactose intolerance. Decades of subsequent research have shown that the ability to digest milk in adulthood is actually a derived trait found in only a few human populations (notably Europeans) with long histories of dairy pastoralism.

In recent years, numerous media stories and organizations started to claim that milk is an unnatural and harmful product with potential links to gastrointestinal illness, cancer, and cardiovascular disease. The growing public scepticism regarding milk as a dietary component relies in part on poorly defined assumptions about the nature of digestion, the role of microbes in human health, and the perceived “naturalness” of dairy as a human food.
Importantly, what is generally missing entirely from public debate is an evidence-based accounting of the context and process by which dairying arose as a human food in the first place and the role it has subsequently played in the long arc of human history.

The DAIRY CULTURES project seeks to enrich scientific and public understanding of dairy foods by systematically investigating the deep history of the biological and cultural relationships between humans, livestock and microbes in a “gene-culture-microbiome coevolution” framework.

The Research Problem – A MILK PARADOX

Worldwide distribution of lactose intolerance

Milk is a nutrient-dense food produced by mammals to feed their young. The main carbohydrate in milk is lactose, a disaccharide of glucose and galactose that requires the action of a specific enzyme, lactase, to digest.
Lactose consumption in the absence of lactase production generally results in lactose passing undigested through the small intestine into the large intestine, where a massive community of more than 30 trillion bacterial cells, collectively known as the gut microbiome, either metabolize it as a food source, or fail to metabolize it due to pH-induced enzyme inactivity.

Either case can produce the symptoms of lactose intolerance, namely cramping, bloating, and diarrhoea. Among humans, populations with long histories of dairying in East Africa, the Levant, Saudi Arabia, Europe, South Asia , and possibly Tibet have been found to have genetic alleles (specific mutations) that enable the continued intestinal production of lactase after infancy and into adulthood. Individuals with these alleles are able to digest lactose in the small intestine and thereby utilize milk as a food resource without developing the symptoms of lactose intolerance.

Adult milk consumption and associated genetic adaptations for lactase persistence have been hailed as the clearest example of gene-culture coevolution. However, how lactase persistence (LP) actually works at a mechanistic level remains unclear, the association between LP genotypes and lactose malabsorption phenotypes and lactose intolerance symptoms is variable, and there is a growing body of evidence that microbes – through culinary fermentation and the action of the human microbiome – assist with lactose digestion and may have played important, yet overlooked, roles in the successful establishment of prehistoric dairying economies. Early manipulation of microbes and control of dairy fermentation, for example, may help explain why humans were able to both invent and subsist on dairy products for more than 5,000 years before the first ancient DNA evidence of LP appears in the archaeological record.

This has left archaeologists with a puzzling problem, a “milk paradox,” regarding how and why ancient peoples developed milk into a dietary resource and what other factors besides lactase persistence may have been involved in this process.

To date, pasteurization and strict control of European dairies has greatly altered the microbial content and functionality of European dairy products. Likewise, recent biodiversity studies of the human microbiome have shown that industrialized European populations have highly altered and simplified gut microbiomes that diverge from the ancestral human state. Thus, investigating the deep relationships between genes, culture, and microbes in a European dairy context is complicated by two centuries of successful industrialization, sanitation, medical modernization, and pasteurization efforts.

Therefore, we focus our attention on Mongolia, a country in which a third of the population pursues a pastoralist lifestyle and where as much as 80% of the rural diet derives from dairy products.
In rural Mongolia, fresh milk and fermented dairy products are basic foods, of which some are consumed year-round. Specific dairy practices exhibit remarkable continuity through time, with relatively few changes compared to early 20th century ethnographic accounts. Today, tradition, cultural heritage, and a strong connection to the past is highly valued by Mongolian dairy herders. In addition to its rich dairying traditions today, Mongolia also has a long recorded history of dairying, including numerous references to dairy livestock (sheep, goat, cattle, and horses) and specific dairy products (milk, aarts, aaruul, öröm, and airag) dating as far back as the 13th century in the Secret History of the Mongols (Монголын нууц товчоо). Recognizable dairying equipment (horse milk cauldrons and fermentation plungers) and dairy livestock (sheep, goats, cattle, yaks, and camels) are depicted in rock art dated to the Late Bronze and Iron Ages throughout Mongolia.
Nevertheless, horse, cow/yak, and sheep/goat skeletal remains are widely attested in Mongolia after 1300 BC and possibly earlier. However, how these animals arrived there, what breeds they are, and where they came from remains uncertain and largely untested. Additionally, all humans we have genetically analyzed from this period (n=20) lack all known LP alleles, and therefore it is important to note that the early adoption of dairying in Mongolia almost certainly occurred in the absence of LP.

This combination of a rich dairy prehistory and a robust contemporary dairy tradition makes Mongolia an ideal biocultural laboratory in which to investigate “gene-culture-microbiome” coevolution. However, many questions remain.

First, the origin of dairy domesticates in Mongolia is poorly understood. With the exception of the Bactrian camel and possibly the reindeer, none of the other five Mongolian dairy livestock species (sheep, goat, cattle, yak, horse) were likely domesticated in or near Mongolia; instead these domesticates appear to have been brought to Mongolia in prehistory through processes that are currently not well understood.

Second, although recent advances have been made in the detection of milk proteins from dental calculus and archaeological food containers, current databases are patchy and incomplete in their coverage of milk protein sequences from various dairy species, making the identification of archaeological milk proteins challenging.

Third, relatively little is known regarding the relationship between the gut microbiome and dairy digestion in Mongolian populations. Specifically, few data are available that examine LP genotypes, lactose malabsorption phenotypes, and lactose intolerance symptoms in parallel, and no studies have investigated Mongolian gut microbiomes together with these clinical measures. To date, only two related studies have examined gut microbiome structure and diversity in Mongolian populations, and one major finding from this research is that certain groups of bacteria, such as dairy-associated Lactobacillus spp., are statistically elevated in Mongolian populations. A contextualized study of Mongolian gut microbiomes that includes measurement of milk digestion-related measures, and which takes into account specific dairy dietary components, is needed to begin to tease apart the digestive role of microbes in the dairy-based subsistence of Mongolian pastoralist herders.


Allentoft ME, Sikora M, Sjögren K-G, Rasmussen S, Rasmussen M, Stenderup J, et al. Population genomics of Bronze Age Eurasia. Nature. nature.com; 2015;522: 167–172.
Azcarate-Peril MA, Ritter AJ, Savaiano D, Monteagudo-Mera A, Anderson C, Magness ST, et al. Impact of short-chain galactooligosaccharides on the gut microbiome of lactose-intolerant individuals. Proc Natl Acad Sci U S A. 2017;114: E367–E375.
Bolin TD, Davis AE. Primary lactase deficiency: genetic or acquired? Am J Dig Dis. Springer; 1970;15: 679–692. Haemmerli UP, Kistler H, Ammann R, Marthaler T, Semenza G, Auricchio S, et al. Acquired Milk Intolerance in the Adult caused by Lactose Malabsorption. Am J Med. Elsevier; 1965;38: 7–30.
Broderick LG, Houle J-L. More than just horse: dietary breadth and subsistence in Bronze Age Central Mongolia. Mongolian Journal of Archaeology, Anthropology and Ethnology. 2013;7: 149–157.
Burger J, Kirchner M, Bramanti B, Haak W, Thomas MG. Absence of the lactase-persistence-associated allele in early Neolithic Europeans. Proc Natl Acad Sci U S A. 2007;104: 3736–3741.
Claeys WL, Cardoen S, Daube G, De Block J, Dewettinck K, Dierick K, et al. Raw or heated cow milk consumption: Review of risks and benefits. Food Control. 2013;31: 251–262.
Clark J. Modeling Late Prehistoric and Early Historic Pastoral Adaptations in Northern Mongolia’s Darkhad Depression [Internet]. dissertation, University of Pittsburgh. 2015. Available: http://d-scholarship.pitt.edu/id/eprint/23838
Colonese AC, Hendy J, Lucquin A, Speller CF, Collins MJ, Carrer F, et al. New criteria for the molecular identification of cereal grains associated with archaeological artefacts. Sci Rep. 2017;7: 6633.
Davlet MA. Rock engravings in the Middle Yenisei Basin. Наука Публ; 1976.
Gamba C, Jones ER, Teasdale MD, McLaughlin RL, Gonzalez-Fortes G, Mattiangeli V, et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat Commun. 2014;5: 5257.
Gerbault P, Liebert A, Itan Y, Powell A, Currat M, Burger J, et al. Evolution of lactase persistence: an example of human niche construction. Philos Trans R Soc Lond B Biol Sci. rstb.royalsocietypublishing.org; 2011;366: 863–877.
He T, Venema K, Priebe MG, Welling GW, Brummer R-JM, Vonk RJ. The role of colonic metabolism in lactose intolerance. Eur J Clin Invest. 2008;38: 541–547.
Hendy J, Warinner C, Bouwman A, Collins MJ, Fiddyment S, Fischer R, et al. Proteomic evidence of dietary sources in ancient dental calculus. Proc Biol Sci. 2018;285. doi:10.1098/rspb.2018.0977
Hertzler SR, Savaiano DA. Colonic adaptation to daily lactose feeding in lactose maldigesters reduces lactose intolerance. Am J Clin Nutr. 1996;64: 232–236.
Hertzler SR, Clancy SM. Kefir improves lactose digestion and tolerance in adults with lactose maldigestion. J Am Diet Assoc. 2003;103: 582–587.
Jacobson-Tepfer E, Meacham JE, Tepfer G. Archaeology and landscape in the Mongolian Altai: an atlas. ESRI Press Redlands; 2010.Kolars JC, Levitt MD, Aouji M, Savaiano DA. Yogurt–an autodigesting source of lactose. N Engl J Med. 1984;310: 1–3.
Leonardi M, Gerbault P, Thomas MG, Burger J. The evolution of lactase persistence in Europe. A synthesis of archaeological and genetic evidence. Int Dairy J. 2012;22: 88–97.
Lomer MCE, Parkes GC. lactose intolerance in clinical practice–myths and realities. Aliment Pharmacol Ther. Wiley Online Library; 2008; Available: https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-2036.2007.03557.x
Makarewicz C. Xiongnu pastoral systems: Integrating economies of subsistence and scale. Xiongnu archaeology: Multidisciplinary perspective on the first steppe empire in Central Asia. 2011; 181–192.
Mathieson I, Lazaridis I, Rohland N, Mallick S, Patterson N, Roodenberg SA, et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature. 2015;528: 499–503.Peng M-S, He J-D, Zhu C-L, Wu S-F, Jin J-Q, Zhang Y-P. Lactase persistence may have an independent origin in Tibetan populations from Tibet, China. J Hum Genet. 2012;57: 394–397.
Obregon-Tito AJ, Tito RY, Metcalf J, Sankaranarayanan K, Clemente JC, Ursell LK, et al. Subsistence strategies in traditional societies distinguish gut microbiomes. Nat Commun. 2015;6: 6505.
Marton A, Xue X, Szilagyi A. Meta-analysis: the diagnostic accuracy of lactose breath hydrogen or lactose tolerance tests for predicting the North European lactase polymorphism C/T-13910. Aliment Pharmacol Ther. 2012;35: 429–440.
Montell G. Distilling in Mongolia. Ethnos. Routledge; 1937;2: 321–332.
de Rachewiltz I. The Secret History of the Mongols: A Mongolian Epic Chronicle of the Thirteenth Century. Igor de Rachewiltz; 2015; Available: https://cedar.wwu.edu/cedarbooks/4/
Rampelli S, Schnorr SL, Consolandi C, Turroni S, Severgnini M, Peano C, et al. Metagenome Sequencing of the Hadza Hunter-Gatherer Gut Microbiota. Curr Biol. doi:10.1016/j.cub.2015.04.055
Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G, et al. Gut microbiome of the Hadza hunter-gatherers. Nat Commun. 2014;5: 3654.
Schnorr SL, Sankaranarayanan K, Lewis CM Jr, Warinner C. Insights into human evolution from ancient and contemporary microbiome studies. Curr Opin Genet Dev. Elsevier; 2016;41: 14–26.
Sender R, Fuchs S, Milo R. Revised Estimates for the Number of Human and Bacteria Cells in the Body. PLoS Biol. journals.plos.org; 2016;14: e1002533.
Ségurel L, Bon C. On the Evolution of Lactase Persistence in Humans. Annu Rev Genomics Hum Genet. 2017;18: 297–319.
Swallow DM. Genetics of lactase persistence and lactose intolerance. Annu Rev Genet. 2003;37: 197–219.
Thorning TK, Raben A, Tholstrup T, Soedamah-Muthu SS, Givens I, Astrup A. Milk and dairy products: good or bad for human health? An assessment of the totality of scientific evidence. Food Nutr Res. Taylor & Francis; 2016;60: 32527.
Warinner C, Rodrigues JFM, Vyas R, Trachsel C, Shved N, Grossmann J, et al. Pathogens and host immunity in the ancient human oral cavity. Nat Genet. 2014;46: 336–344.
Warinner C, Hendy J, Speller C, Cappellini E, Fischer R, Trachsel C, et al. Direct evidence of milk consumption from ancient human dental calculus. Sci Rep. 2014;4: 7104.
Welsh JD. Isolated lactase deficiency in humans: report on 100 patients. Medicine . journals.lww.com; 1970;49: 257–277.
Worrying About Milk | DiscoverMagazine.com. In: Discover Magazine [Internet]. [cited 12 Mar 2019]. Available: http://discovermagazine.com/2000/aug/featmilk

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