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The Origins of Lactase Persistence in Europe
Open accessAbstract
Lactase persistence (LP) is common among people of European ancestry, but with the exception of some African, Middle Eastern and southern Asian groups, is rare or absent elsewhere in the world. Lactase gene haplotype conservation around a polymorphism strongly associated with LP in Europeans (-13,910 C/T) indicates that the derived allele is recent in origin and has been subject to strong positive selection. Furthermore, ancient DNA work has shown that the--13,910*T (derived) allele was very rare or absent in early Neolithic central Europeans. It is unlikely that LP would provide a selective advantage without a supply of fresh milk, and this has lead to a gene-culture coevolutionary model where lactase persistence is only favoured in cultures practicing dairying, and dairying is more favoured in lactase persistent populations. We have developed a flexible demic computer simulation model to explore the spread of lactase persistence, dairying, other subsistence practices and unlinked genetic markers in Europe and western Asia's geographic space. Using data on--13,910*T allele frequency and farming arrival dates across Europe, and approximate Bayesian computation to estimate parameters of interest, we infer that the--13,910*T allele first underwent selection among dairying farmers around 7,500 years ago in a region between the central Balkans and central Europe, possibly in association with the dissemination of the Neolithic Linearbandkeramik culture over Central Europe. Furthermore, our results suggest that natural selection favouring a lactase persistence allele was not higher in northern latitudes through an increased requirement for dietary vitamin D. Our results provide a coherent and spatially explicit picture of the coevolution of lactase persistence and dairying in Europe.
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“although the selective sweep has been modelled as originating between Central Europe and the Balkans ~4–6,000 years BC (ref. 34).”
From Genome flux and stasis in a five millennium transect of European prehistory (2014) · cites this paper as [34]
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The History and Geography of Human Genes
Cavalli-Sforza, L. L., Menozzi, P., & Piazza, A. (2018) · Princeton University Press eBooks · doi:10.2307/j.ctv301gjp · Cited by 3,175
Approximate Bayesian computation in population genetics
Beaumont, M. A., Zhang, W., & Balding, D. J. (2002) · Genetics · doi:10.1093/genetics/162.4.2025 · Cited by 2,932
Self-citationHistory and Geography of Human Genes
Piazza, A. (1994) · Advances in forensic haemogenetics · doi:10.1007/978-3-642-78782-9_1 · Cited by 1,639
Convergent adaptation of human lactase persistence in Africa and Europe
Tishkoff, S. A., Reed, F. A., Ranciaro, A., Voight, B. F., Babbitt, C. C., Silverman, J. S., Powell, K., Mortensen, H. M., Hirbo, J. B., Osman, M., et al. (2007) · Nature Genetics · doi:10.1038/ng1946 · Cited by 1,615 · cited 1×
“In Africa there are at least four known LP-associated alleles, including three that are likely to be of African origin [2,4] as well as 213,910*T, which is likely to be of European origin [3,12].”
BackgroundA Mathematical Theory of Natural and Artificial Selection, Part V: Selection and Mutation
Haldane, J. B. S. (1927) · Mathematical Proceedings of the Cambridge Philosophical Society · doi:10.1017/s0305004100015644 · Cited by 1,326 · cited 1×
“While we would expect any de novo mutation to always have an initial frequency of 1/2N, we also expect that it will have a high probability of extinction unless selection is very strong [79].”
BackgroundGenetic Signatures of Strong Recent Positive Selection at the Lactase Gene
Bersaglieri, T., Sabeti, P. C., Patterson, N. J., Vanderploeg, T. N., Schaffner, S. F., Drake, J. A., Rhodes, M. E., Reich, D., & Hirschhorn, J. N. (2004) · The American Journal of Human Genetics · doi:10.1086/421051 · Cited by 1,169 · cited 15×
“063 16 [8] 1699 7274 (69) 7112 (76) 43.”
BackgroundResultInfluentialIdentification of a variant associated with adult-type hypolactasia
Enattah, N. S., Sahi, T., Savilahti, E., Terwilliger, J. D., Peltonen, L., & Järvelä, I. E. (2002) · Nature Genetics · doi:10.1038/ng826 · Cited by 1,029 · cited 1×
“91 kb upstream from the lactase gene [5].”
BackgroundEarliest Date for Milk Use in the Near East and Southeastern Europe Linked to Cattle Herding
Evershed, R. P., Payne, S., Sherratt, A. G., Copley, M. S., Coolidge, J., Urem-Kotsu, D., Kotsakis, K., Özdoğan, M., Özdoğan, A. E., Nieuwenhuyse, O., et al. (2008) · Nature · doi:10.1038/nature07180 · Cited by 681 · cited 4×
“Recent carbon isotope ratios from lipids extracted from archaeological sherds show the presence of milk fats in present-day western Turkey and connect these findings to an increased importance of cattle herding [26,45–48].”
BackgroundInfluentialExcoffier, L. (2003) · Molecular Ecology · doi:10.1046/j.1365-294x.2003.02004.x · Cited by 663 · cited 3×
“related studies [33–36] the one we present is stochastic and more parameter-heavy.”
BackgroundMethodThe Fate of Mutations Surfing on the Wave of a Range Expansion
Klopfstein, S., Currat, M., & Excoffier, L. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msj057 · Cited by 641 · cited 2×
“However, previous simulations have shown that the geographic centroid of allele can be offset from its location of origin, particularly when it occurs on the wave front of a demographic expansion [29,30].”
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Research works printed but not linked: 2
- CJ Ingram, 2008, Population and molecular genetics of lactase persistence., Journal of Human Genetics In Press
- JD Vigne, 2007, Was milk a “secondary product” in the Old World Neolithisation process? Its role in the domestication of cattle, sheep and goats., Anthropozoologica, 42, 9
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Yi, X., Liang, Y., Huerta-Sanchez, E., Jin, X., Cuo, Z. X. P., Pool, J. E., Xu, X., Jiang, H., Vinckenbosch, N., Korneliussen, T. S., et al. (2010) · Science · doi:10.1126/science.1190371 · Cited by 1,611
Population genomics of Bronze Age Eurasia
Allentoft, M. E., Sikora, M., Sjögren, K.-G., Rasmussen, S., Rasmussen, M., Stenderup, J., Damgaard, P. B., Schroeder, H., Ahlström, T., Vinner, L., et al. (2015) · Nature · doi:10.1038/nature14507 · Cited by 1,550
Approximate Bayesian Computation (ABC) in practice
Csilléry, K., Blum, M. G. B., Gaggiotti, O. E., & François, O. (2010) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2010.04.001 · Cited by 1,302
Ancient human genomes suggest three ancestral populations for present-day Europeans
Lazaridis, I., Patterson, N., Mittnik, A., Renaud, G., Mallick, S., Kirsanow, K., Sudmant, P. H., Schraiber, J. G., Castellano, S., Lipson, M., et al. (2014) · Nature · doi:10.1038/nature13673 · Cited by 1,357
Self-citationApproximate Bayesian Computation in Evolution and Ecology
Beaumont, M. (2010) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-102209-144621 · Cited by 1,117
“ABC has also been used to model parameters relating to selection on lactase persistence in a spatially explicit modelling framework (Itan et al., 2009; Gerbault et al., 2009).”
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Gligorijević, V., Renfrew, P. D., Kościółek, T., Leman, J. K., Berenberg, D., Vatanen, T., Chandler, C., Taylor, B. C., Fisk, I., Vlamakis, H. C., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23303-9 · Cited by 984
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Laland, K. N., Odling‐Smee, J., & Myles, S. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2734 · Cited by 891
“One prominent example is the co-evolution of dairy farming and lactose toleranc”
BackgroundRegional population collapse followed initial agriculture booms in mid-Holocene Europe
Shennan, S. J., Downey, S. S., Timpson, A., Edinborough, K., Colledge, S., Kerig, T., Manning, K., & Thomas, M. (2013) · Nature Communications · doi:10.1038/ncomms3486 · Cited by 751
Self-citationCrop manuring and intensive land management by Europe’s first farmers
Bogaard, A., Fraser, R., Heaton, T. H. E., Wallace, M. P., Vaiglova, P., Charles, M., Jones, G., Evershed, R. P., Styring, A., Andersen, N. H., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305918110 · Cited by 698
“…curds from the Kuyavia region of Poland dating back to the sixth mil-lennium cal B.C. (36), and simulation modeling of the emergence of lactase persistence, which points to origins in Neolithic central Europe (37), although crops may often have remained the predominant protein source (38).”
Genome flux and stasis in a five millennium transect of European prehistory
Gamba, C., Jones, E. R., Teasdale, M. D., McLaughlin, R. L., Gonzalez-Fortes, G., Mattiangeli, V., Domboróczki, L., Kővári, I., Pap, I., Anders, A., et al. (2014) · Nature Communications · doi:10.1038/ncomms6257 · Cited by 667
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InfluentialRicherson, P., Baldini, R., Bell, A. V., Demps, K., Frost, K., Hillis, V., Mathew, S., Newton, E. K., Naar, N., Newson, L., et al. (2016) · Behavioral and Brain Sciences · doi:10.1017/s0140525x1400106x · Cited by 639
Fearnhead, P., & Prangle, D. (2012) · Journal of the Royal Statistical Society Series B (Statistical Methodology) · doi:10.1111/j.1467-9868.2011.01010.x · Cited by 550
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Karlsson, E. K., Kwiatkowski, D. P., & Sabeti, P. C. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3734 · Cited by 546
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Roffet‐Salque, M., Bogucki, P., Pyzel, J., Sobkowiak‐Tabaka, I., Grygiel, R., Szmyt, M., & Evershed, R. P. (2012) · Nature · doi:10.1038/nature11698 · Cited by 545
Evolution of lactase persistence: an example of human niche construction
Gerbault, P., Liebert, A., Itan, Y., Powell, A., Currat, M., Bürger, J., Swallow, D. M., & Thomas, M. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0268 · Cited by 546
Self-citationDid Our Species Evolve in Subdivided Populations across Africa, and Why Does It Matter?
Scerri, E. M. L., Thomas, M., Manica, A., Gunz, P., Stock, J. T., Stringer, C. B., Grove, M. L., Groucutt, H. S., Timmermann, A., Rightmire, G. P., et al. (2018) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2018.05.005 · Cited by 514
“More complex models allow demographic expansions or contractions in space, often based on simulations [71,72].”
BackgroundSelf-citationABC as a flexible framework to estimate demography over space and time: some cons, many pros
Bertorelle, G., Benazzo, A., & Mona, S. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04690.x · Cited by 465
“Forward genetic simulations have the advantage to substantially simplify the implementation of natural selection and for this reason they may spread for specific ABC implementations (e.g. Itan et al. 2009).”
BackgroundStorhaug, C. L., Fosse, S., & Fadnes, L. (2017) · The Lancet Gastroenterology and Hepatology · doi:10.1016/s2468-1253(17)30154-1 · Cited by 343
RetractedDetection of human adaptation during the past 2000 years
Field, Y., Boyle, E. A., Telis, N., Gao, Z., Gaulton, K. J., Golan, D., Yengo, L., Rocheleau, G., Froguel, P., McCarthy, M. I., et al. (2016) · Science · doi:10.1126/science.aag0776 · Cited by 383
On the Evolution of Lactase Persistence in Humans
Ségurel, L., & Bon, C. (2017) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-091416-035340 · Cited by 387
A worldwide correlation of lactase persistence phenotype and genotypes
Itan, Y., Jones, B. L., Ingram, C. J. E., Swallow, D. M., & Thomas, M. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-36 · Cited by 352
“Furthermore, a simulation model of the origins and evolution of lactase persistence and dairying in Europe has inferred that natural selection started to act on an initially small number of lactase persistent dairyers around 7,500 BP in a region between Central Europe and the northern Balkans, possibly in association…”
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Larson, G., & Bürger, J. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.01.003 · Cited by 309
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Garrett, D. D., Kovacevic, N., McIntosh, A. R., & Grady, C. L. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs055 · Cited by 276
Deschamps, M., Laval, G., Fagny, M., Itan, Y., Abel, L., Casanova, J.-L., Patin, E., & Quintana-Murci, L. (2016) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2015.11.014 · Cited by 257
Self-citationModeling Recent Human Evolution in Mice by Expression of a Selected EDAR Variant
Kamberov, Y. G., Wang, S., Tan, J., Gerbault, P., Wark, A. R., Tan, L., Yang, Y., Li, S., Tang, K., Chen, H., et al. (2013) · Cell · doi:10.1016/j.cell.2013.01.016 · Cited by 277
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BackgroundMethodInfluentialSelf-citationThe future of ancient DNA: Technical advances and conceptual shifts
Hofreiter, M., Paijmans, J. L. A., Goodchild, H., Speller, C., Barlow, A., Fortes, G. G., Thomas, J. A., Ludwig, A., & Collins, M. J. (2014) · BioEssays · doi:10.1002/bies.201400160 · Cited by 275
“A well-known example is the development of lactase persistence in Europe concurrent with the introduction of dairy products [106, 107].”
BackgroundWilde, S., Timpson, A., Kirsanow, K., Kaiser, E., Kayser, M., Unterländer, M., Hollfelder, N., Potekhina, I. D., Schier, W., Thomas, M. G., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1316513111 · Cited by 257
“0795 and to have begun around 7,500 y ago in the region between the Balkans and central Europe (37).”
BackgroundSelf-citationDirect evidence of milk consumption from ancient human dental calculus
Warinner, C., Hendy, J., Speller, C., Cappellini, E., Fischer, R., Trachsel, C., Arneborg, J., Lynnerup, N., Craig, O. E., Swallow, D. M., et al. (2014) · Scientific Reports · doi:10.1038/srep07104 · Cited by 216
Genes, Culture, and Agriculture
O’Brien, M. J., & Laland, K. N. (2012) · Current Anthropology · doi:10.1086/666585 · Cited by 254
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BackgroundMethodResultInfluentialDarwin in Mind: New Opportunities for Evolutionary Psychology
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“In addition to these established tools, researchers can also exploit modern comparative statistical methods applied to cultural and behavioural variation [85] and gene-culture coevolutionary theory [22,58,83,86] to reconstruct human evolutionary histories.”
BackgroundReconstructing the origin and spread of horse domestication in the Eurasian steppe
Warmuth, V. M., Eriksson, A., Bower, M. A., Barker, G., Barrett, E., Hanks, B. K., Li, S., Lomitashvili, D., Ochir-Goryaeva, M. A., Sizonov, G. V., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111122109 · Cited by 232
“(24) used a demic computer model to trace the spread of lactase persistence and therefore dairying in Europe.”
MethodThe Importance of Dietary Carbohydrate in Human Evolution
Hardy, K., Brand-Miller, J. C., Brown, K. D., Thomas, M., & Copeland, L. (2015) · The Quarterly Review of Biology · doi:10.1086/682587 · Cited by 230
“…the case of milk consumption (Holden and Mace 1997), whereby the development of dairying practices during the early Neolithic led to increased milk consumption (Evershed et al. 2008), and the evolution and spread of lactase persistence (Swallow 2003; Itan et al. 2009, 2010; Gerbault et al. 2011).”
BackgroundSelf-citationDairying, diseases and the evolution of lactase persistence in Europe
Evershed, R. P., Smith, G. D., Roffet‐Salque, M., Timpson, A., Diekmann, Y., Lyon, M., Cramp, L., Casanova, E., Smyth, J., Whelton, H. L., et al. (2022) · Nature · doi:10.1038/s41586-022-05010-7 · Cited by 242
Fundamentals and Recent Developments in Approximate Bayesian Computation
Lintusaari, J., Gutmann, M. U., Dutta, R., Samuel Kaski, A., & Corander, J. (2016) · Systematic Biology · doi:10.1093/sysbio/syw077 · Cited by 220
“2009), or the demographic spread of a species (Currat and Excoffier 2004; Fagundes et al. 2007; Itan et al. 2009; Excoffier et al. 2013).”
BackgroundDomesticating animals in Africa: implications of genetic and archaeological findings
Gifford-Gonzalez, D., & Hanotte, O. (2011) · Journal of World Prehistory · doi:10.1007/s10963-010-9042-2 · Cited by 274
“This inference of an early and independent ‘secondary products’ economy is rendered more plausible by what is now known of the early appearance of dairying in Eurasia (Evershed et al. 2008; Ingram et al. 2009; Itan et al. 2009; see also Linseele 2010).”
BackgroundOlalde, I., Schroeder, H., Sandoval-Velasco, M., Vinner, L., Lobón, I., Ramirez, O., Civit, S., García Borja, P., Salazar-García, D. C., Talamo, S., et al. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv181 · Cited by 207
“At the rs4988235 site (which has a regulatory effect on the LCT gene), CB13 shows the ancestral variant associated with the inability to digest milk during adulthood (Itan et al. 2009), sharing this trait with all Neolithic individuals analyzed to date (Gamba et al.”
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Peter, B. M., Huerta-Sanchez, E., & Nielsen, R. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003011 · Cited by 193
In defence of model-based inference in phylogeography
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“…on allele frequencies (e.g. Guillot et al. 2005; Novembre et al. 2005; Francois et al. 2006; Corander et al. 2008), coalescent-based approaches seem in an ideal position to enable us to integrate molecular information into phylogeographic inferences (see e.g. Manolopoulou 2008; Itan et al. 2009;).”
Self-citationMace, R. H., & Jordan, F. M. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0238 · Cited by 188
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Modern taurine cattle descended from small number of near-eastern founders
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Underhill, P. A., Myres, N. M., Rootsi, S., Metspalu, M., Анатольевич, Ж. Л., King, R., Lin, A. A., Chow, C.-E. T., Semino, O., Battaglia, V., et al. (2009) · European Journal of Human Genetics · doi:10.1038/ejhg.2009.194 · Cited by 191
“51 However, computer simulations have shown that its increased frequency particularly in North Europe does not necessarily imply stronger effect of positive selection there than in other parts of Europe”
BackgroundArchaeology: The milk revolution
Curry, A. (2013) · Nature · doi:10.1038/500020a · Cited by 185
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“To build a global model, we had to leave out several region-specific factors, such as local adaptation to new climatic conditions (32, 33), the depletion of important food sources such as megafauna (34), the advent of new techniques such as agriculture (35) and domestication (36, 37), or the possible competition with…”
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Lacan, M., Keyser, C., Ricaut, F., Brucato, N., Duranthon, F., Guilaine, J., Crubézy, É., & Ludes, B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100723108 · Cited by 178
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BackgroundOn the History of Cattle Genetic Resources
Felius, M., Beerling, M.-L., Buchanan, D., Theunissen, B., Koolmees, P., & Lenstra, J. (2014) · Diversity · doi:10.3390/d6040705 · Cited by 176
“Roman cattle were not milked [64], but Columella and Pliny praised the dairy qualities of the Alpine cows [64,90,91].”
BackgroundCramp, L., Jones, J. R., Sheridan, A., Smyth, J., Whelton, H. L., Mulville, J., Sharples, N., & Evershed, R. P. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.2372 · Cited by 187
How evolutionary principles improve the understanding of human health and disease
Gluckman, P. D., Low, F. M., Buklijaš, T., Hanson, M. A., & Beedle, A. S. (2011) · Evolutionary Applications · doi:10.1111/j.1752-4571.2010.00164.x · Cited by 166
“Evidence to support this hypothesis includes epidemiological studies on humans prenatally exposed to famine, who have a higher risk of coronary heart disease and obesity in adulthood (Painter et al. 2005).”
BackgroundResultThe selection landscape and genetic legacy of ancient Eurasians
Irving-Pease, E. K., Refoyo-Martínez, A., Barrie, W., Ingason, A., Pearson, A., Fischer, A., Sjögren, K.-G., Halgren, A. S., Macleod, R., Demeter, F., et al. (2024) · Nature · doi:10.1038/s41586-023-06705-1 · Cited by 126
Review article: the aetiology, diagnosis, mechanisms and clinical evidence for food intolerance
Lomer, M. C. E. (2014) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.13041 · Cited by 152
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BackgroundElevated genetic risk for multiple sclerosis emerged in steppe pastoralist populations
Barrie, W., Yang, Y., Irving-Pease, E. K., Attfield, K. E., Scorrano, G., Jensen, L. T., Armen, A. P., Dimopoulos, E. A., Stern, A., Refoyo-Martinez, A., et al. (2024) · Nature · doi:10.1038/s41586-023-06618-z · Cited by 161
“2a): the LCT / MCM6 region on chromosome 2, which is well established as regulating lactase persistence 11,12 , and the HLA region on chromosome 6.”
BackgroundEvolutionary Patterns and Processes: Lessons from Ancient DNA
Leonardi, M., Librado, P., Sarkissian, C. S. I. D., Schubert, M., Alfarhan, A., Alquraishi, S. A., Al‐Rasheid, K. A. S., Gamba, C., Willerslev, E., & Orlando, L. (2016) · Systematic Biology · doi:10.1093/sysbio/syw059 · Cited by 157
“This suggests that European LP possibly originated on the steppes (Allentoft et al. 2015), and not from Central Europe, as previously proposed based on patterns of genetic variation observed in living European populations (Itan et al. 2009).”
BackgroundInfluentialDebono Spiteri, C., Gillis, R. E., Roffet-Salque, M., Castells Navarro, L., Guilaine, J., Manen, C., Muntoni, I. M., Saña Segui, M., Urem-Kotsou, D., Whelton, H. L., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1607810113 · Cited by 142
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BackgroundFraser, R., Bogaard, A., Schäfer, M., Arbogast, R., & Heaton, T. H. E. (2013) · World Archaeology · doi:10.1080/00438243.2013.820649 · Cited by 145
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Anguita‐Ruiz, A., Aguilera, C. M., & Gil, Á. (2020) · Nutrients · doi:10.3390/nu12092689 · Cited by 157
Genetic ancestry changes in Stone to Bronze Age transition in the East European plain
Saag, L., Vasilyev, S. V., Varul, L., Kosorukova, N. V., Gerasimov, D. V., Oshibkina, S. V., Griffith, S. J., Solnik, A., Saag, L., D’Atanasio, E., et al. (2021) · Science Advances · doi:10.1126/sciadv.abd6535 · Cited by 139
The genetic prehistory of domesticated cattle from their origin to the spread across Europe
Scheu, A., Powell, A., Bollongino, R., Vigne, J., Tresset, A., Çakırlar, C., Benecke, N., & Bürger, J. (2015) · BMC Genetics · doi:10.1186/s12863-015-0203-2 · Cited by 139
“the ability to digest milk sugar as an adult), point to this area as where positive selection started affecting the frequency of this allele in dairying cultures [59].”
Self-citationMajor correlates of male height: A study of 105 countries
Grasgruber, P., Sebera, M., Hrazdíra, E., Cacek, J., & Kalina, T. (2016) · Economics & Human Biology · doi:10.1016/j.ehb.2016.01.005 · Cited by 130
He, Q., Edwards, D. L., & Knowles, L. L. (2013) · Evolution · doi:10.1111/evo.12159 · Cited by 130
“Moreover, the flexibility and versatility of tools for evaluating and interpreting models (e.g., with ABC: Neuenschwander et al. 2008; Itan et al. 2009; Jaquiéry et al. 2011) can expand the repertoire of biological models that might be considered.”
MethodLiebert, A., López, S., Jones, B. L., Montalva, N., Gerbault, P., Lau, W., Thomas, M., Bradman, N., Maniatis, N., & Swallow, D. M. (2017) · Human Genetics · doi:10.1007/s00439-017-1847-y · Cited by 127
“While strong selection for LP has been supported by various studies (Aoki 1986; Coelho et al. 2005; Gerbault et al. 2009; Holden and Mace 1997; Itan et al. 2009; Mathieson et al. 2015; Schlebusch et al. 2013; Sverrisdottir et al. 2014), the features of the chromosomal region highlighted here show that other processes,…”
BackgroundSelf-citationAncient DNA suggests the leading role played by men in the Neolithic dissemination
Lacan, M., Keyser, C., Ricaut, F., Brucato, N., Tarrús, J., Bosch, À., Guilaine, J., Crubézy, É., & Ludes, B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113061108 · Cited by 118
“The mutated position would have appeared during the dissemination of the Linear pottery culture in central Europe (15).”
BackgroundThe genetic history of Europeans
Pinhasi, R., Thomas, M., Hofreiter, M., Currat, M., & Bürger, J. (2012) · Trends in Genetics · doi:10.1016/j.tig.2012.06.006 · Cited by 120
Self-citationKnowles, L. L., & Alvarado‐Serrano, D. F. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04702.x · Cited by 117
“…consequences of climateinduced distributional shifts, as with other parameterrich models (see Currat & Excoffier 2004; Fagundes et al. 2007; Valdiosera et al. 2008; Bramanti et al. 2009; Itan et al. 2009; Malmström et al. 2009), ABC (Beaumont et al. 2002, 2010) is ideal for these applications.”
BackgroundThe evolution of lactase persistence in Europe. A synthesis of archaeological and genetic evidence
Leonardi, M., Gerbault, P., Thomas, M., & Bürger, J. (2011) · International Dairy Journal · doi:10.1016/j.idairyj.2011.10.010 · Cited by 120
Self-citationAdaptation of human skin color in various populations
Deng, L., & Xu, S. (2018) · Hereditas · doi:10.1186/s41065-017-0036-2 · Cited by 89
“08 for LCT, a gene strongly associated with lactase persistence in populations with European ancestry [113, 114], 0.”
BackgroundStaphylococcus aureus and Listeria monocytogenes in Norwegian raw milk cheese production
Jakobsen, R. A., Heggebø, R., Sunde, E. B., & Skjervheim, M. (2010) · Food Microbiology · doi:10.1016/j.fm.2010.10.017 · Cited by 106
Demic and cultural diffusion propagated the Neolithic transition across different regions of Europe
Fort, J. (2015) · Journal of The Royal Society Interface · doi:10.1098/rsif.2015.0166 · Cited by 108
“r 7 the spreads of horse domestication in Eurasia [37], dairying in Europe [38], maize in America [39] and military technologies in the Old World [40].”
BackgroundGenome-wide data from two early Neolithic East Asian individuals dating to 7700 years ago
Siska, V., Jones, E. R., Jeon, S., Bhak, Y., Kim, H., Cho, Y. S., Kim, H., Kyusang, L., Veselovskaya, E. V., Balueva, T. S., et al. (2017) · Science Advances · doi:10.1126/sciadv.1601877 · Cited by 103
“999) (35) and was unlikely to have suffered from alcohol flush (rs671, ALDH2 gene;”
Evolutionary accounts of human behavioural diversity
Brown, G. R., Dickins, T. E., Sear, R., & Laland, K. N. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0267 · Cited by 110
Diversity of Lactase Persistence Alleles in Ethiopia: Signature of a Soft Selective Sweep
Jones, B. L., Oljira, T., Liebert, A., Zmarz, P., Bekele, E., Danielsen, E. T., Olsen, A. K., Bradman, N., Troelsen, J. T., & Swallow, D. M. (2013) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2013.07.008 · Cited by 103
Riede, F. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0266 · Cited by 105
Human evolution: a tale from ancient genomes
Llamas, B., Willerslev, E., & Orlando, L. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0484 · Cited by 100
Understanding rare and common diseases in the context of human evolution
Quintana‐Murci, L. (2016) · Genome biology · doi:10.1186/s13059-016-1093-y · Cited by 103
“Studies aiming to date the lactase persistence allele in Europe have suggested that this allele was selected in farmers some 6000 to 11,000 years ago [79, 81, 95, 129, 130], although estimates based on ancient DNA point to a more recent time [131, 132] (see below).”
BackgroundIngram, C. J. E., Oljira, T., Tarekegn, A., Browning, S. L., Elamin, M. F., Bekele, E., Thomas, M., Weale, M. E., Bradman, N. N., & Swallow, D. M. (2009) · Journal of Molecular Evolution · doi:10.1007/s00239-009-9301-y · Cited by 100
“The calcium assimilation hypothesis, which proposed that the calcium in milk is more advantageous at high latitudes due to reduced incident sunlight and reduced vitamin D synthesis (Flatz and Rotthauwe 1973), was not supported in a recent study (Itan et al. 2009).”
BackgroundSelf-citationPopulation structure and cultural geography of a folktale in Europe
Ross, R. M., Greenhill, S. J., & Atkinson, Q. D. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.3065 · Cited by 105
Burger, J., Link, V., Blöcher, J., Schulz, A., Sell, C., Pochon, Z., Diekmann, Y., Žegarac, A., Hofmanová, Z., Winkelbach, L., et al. (2020) · Current Biology · doi:10.1016/j.cub.2020.08.033 · Cited by 108
“Demography and Selection Aside from strong natural selection, demographic processes, such as migration and population range expansion—leading to allele surfing [59, 60]—will have shaped the distribution of the rs4988235-A allele [61].”
BackgroundSelf-citationAntagonistic Pleiotropy in Human Disease
Byars, S., & Voskarides, K. (2019) · Journal of Molecular Evolution · doi:10.1007/s00239-019-09923-2 · Cited by 96
The Importance of Lactose in the Human Diet: Outcomes of a Mexican Consensus Meeting
Romero‐Velarde, E., Delgado‐Franco, D., García-Gutiérrez, M., Gurrola‐Díaz, C. M., Larrosa‐Haro, A., Montijo-Barrios, É., Muskiet, F. A. J., Vargas‐Guerrero, B., & Geurts, J. M. W. (2019) · Nutrients · doi:10.3390/nu11112737 · Cited by 108
A Generic Program for Multistate Protein Design
Leaver‐Fay, A., Jacak, R., Stranges, P. B., & Kuhlman, B. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020937 · Cited by 100
Lactase nonpersistence is directed by DNA-variation-dependent epigenetic aging
Labrie, V., Buske, O. J., Oh, E. S., Jeremian, R., Ptak, C., Gasiūnas, G., Maleckas, A., Petereit, R., Žvirblienė, A., Adamonis, K., et al. (2016) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3227 · Cited by 99
The Evolution of Fermented Milks, from Artisanal to Industrial Products: A Critical Review
Bintsis, Τ., & Papademas, P. (2022) · Fermentation · doi:10.3390/fermentation8120679 · Cited by 109
High frequency of lactose intolerance in a prehistoric hunter-gatherer population in northern Europe
Malmström, H., Linderholm, A. E., Lidén, K., Storå, J., Molnár, P., Holmlund, G., Jakobsson, M., & Götherström, A. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-89 · Cited by 89
“Notably, the allele frequency at the SNP and the extent of haplotype homozygosity around the particular SNP-allele indicate a history of a strong positive selection [5,6,9,10], and it has been suggested that this selective pressure was attributable to the introduction of agriculture and animal domestication [10,11].”
Herders of Indian and European Cattle Share Their Predominant Allele for Lactase Persistence
Romero, I. G., Mallick, C. B., Liebert, A., Crivellaro, F., Chaubey, G., Itan, Y., Metspalu, M., Eaaswarkhanth, M., Pitchappan, R. M., Villems, R., et al. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr190 · Cited by 91
“It is therefore likely that the -13910*T allele was introduced to the subcontinent via a small number of migrants in the wake of the well-documented sweep for lactase persistence in the European middle Neolithic (Bersaglieri et al. 2004; Burger et al. 2007; Ingram, Mulcare, et al. 2009; Itan et al. 2009).”
BackgroundInfluentialSelf-citationEdwards, C. J., Ginja, C., Kantanen, J., Pérez-Pardal, L., Tresset, A., Stock, F., Gama, L. T., Penedo, M. C. T., Bradley, D. G., Lenstra, J. A., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015922 · Cited by 88
“This is consistent with the origin of human lactase tolerance in central Europe [61].”
BackgroundResultSégurel, L., Guarino‐Vignon, P., Marchi, N., Lafosse, S., Laurent, R., Bon, C., Fabre, A., Hegay, T., & Heyer, É. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000742 · Cited by 89
“We don’t see any LP individual among those directly affiliated with Yamnaya-associated cultures, but there are not many of them (48 individuals) compared to non-Yamnaya Europeans (and 0/48 is not significantly different from 3/252, proportion test: p = 1). https://doi.org/10.1371/journal.pbio.3000742.g001 PLOS Biology…”
BackgroundInfluentialStorytelling and story testing in domestication
Gerbault, P., Allaby, R. G., Boivin, N. L., Rudzinski, A., Grimaldi, I. M., Pires, J. C., Vigueira, C. C., Dobney, K. M., Gremillion, K. J., Barton, L., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400425111 · Cited by 85
“In addition, methodologies such as ABC allow for the integration of distinct sources of data (47).”
MethodSelf-citationHarris, A. M., Garud, N. R., & DeGiorgio, M. (2018) · Genetics · doi:10.1534/genetics.118.301502 · Cited by 87
“We scanned all autosomes using nucleotide-delimited genomic windows, proportional to the effective size of the study population, and the interval over which the rate of decay in pairwise LD plateaus empirically [see Jakobsson et al., 2008].”
MethodThe effective founder effect in a spatially expanding population
Peter, B. M., & Slatkin, M. (2015) · Evolution · doi:10.1111/evo.12609 · Cited by 84
Familial hypercholesterolemia: epidemiology, Neolithic origins and modern geographic distribution
Liyanage, K. E., Burnett, J. R., Hooper, A. J., & BOCKXMEER, F. M. V. (2011) · Critical Reviews in Clinical Laboratory Sciences · doi:10.3109/10408363.2011.565585 · Cited by 82
Recent advances in methods of lexical semantic relatedness – a survey
Zhang, Z., Gentile, A. L., & Ciravegna, F. (2012) · Natural Language Engineering · doi:10.1017/s1351324912000125 · Cited by 81
The genomic history of the Aegean palatial civilizations
Clemente, F., Unterländer, M., Dolgova, O., Amorim, C. E. G., Coroado-Santos, F., Neuenschwander, S., Ganiatsou, E., Dávalos, D. I. C., Anchieri, L., Michaud, F., et al. (2021) · Cell · doi:10.1016/j.cell.2021.03.039 · Cited by 81
Adaptations to local environments in modern human populations
Jeong, C., & Di Rienzo, A. (2014) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2014.06.011 · Cited by 80
A MicroRNA Linking Human Positive Selection and Metabolic Disorders
Wang, L., Sinnott-Armstrong, N., Wagschal, A., Wark, A. R., Camporez, J. P., Perry, R. J., Ji, F., Sohn, Y., Oh, J. D., Wu, S., et al. (2020) · Cell · doi:10.1016/j.cell.2020.09.017 · Cited by 81
“However, other dietary sources might have provided sufficient sources of such nutrients (Itan et al., 2009).”
BackgroundLactase Persistence and Lipid Pathway Selection in the Maasai
Wagh, K., Bhatia, A., Alexe, G., Reddy, A., Ravikumar, V., Seiler, M., Boemo, M. A., Yao, M., Cronk, L., Naqvi, A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044751 · Cited by 78
“For example, many studies have identified polymorphisms conferring lactase persistence in Northern Europeans, which arose with the advent of cattle breeding [26].”
BackgroundLow prevalence of lactase persistence in Neolithic South-West Europe
Plantinga, T. S., Alonso, S., Izagirre, N., Hervella, M., Fregel, R., van der Meer, J. W. M., Netea, M. G., & Vaca, C. D. L. R. (2012) · European Journal of Human Genetics · doi:10.1038/ejhg.2011.254 · Cited by 76
Detecting and Measuring Selection from Gene Frequency Data
Vitalis, R., Gautier, M., Dawson, K. J., & Beaumont, M. (2013) · Genetics · doi:10.1534/genetics.113.152991 · Cited by 80
“Last, using a spatially explicit model and approximate Bayesian computation (Beaumont et al. 2002), Itan et al. (2009) estimated coefficients of selection to lay in the range of 5.2-15.9%.”
MethodInfluentialSelf-citationCharting a Future Course for Organic Residue Analysis in Archaeology
McGovern, P. E., & Hall, G. R. (2015) · Journal of Archaeological Method and Theory · doi:10.1007/s10816-015-9253-z · Cited by 74
“That the modern reference samples from Britain, North Africa, and Central Asia can be combined together for comparison to the ancient Polish samples.”
BackgroundInfluentialOmenn, G. S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906198106 · Cited by 78
“(32) used a simulation model incorporating genetic and archaeological data to conclude that this allele arose and was selected for among dairying farmers in the central Balkans and central Europe.”
Global Distribution and Evolution of Mycobacterium bovis Lineages
Zimpel, C. K., Patané, J. S. L., Guedes, A. C. P., de Souza, R. F., Silva‐Pereira, T. T., Camargo, N., Filho, A. F. D. S., Ikuta, C. Y., Neto, J. S. F., Setúbal, J. C., et al. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00843 · Cited by 72
Metadata
- Authors
- Itan, Y., Powell, A., Beaumont, M. A., Burger, J., & Thomas, M. G.
- Affiliations
- University College London (GB)
- University of Reading (GB)
- Corresponding author
- Thomas, Mark G.
- Venue
- PLoS Computational Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2009-08-28
- Volume
- 5
- Issue
- 8
- Pages
- e1000491
- ISSN
- 1553-734X (ISSN-L)
- 1553-7358
- PMC
- PMC2722739
- OpenAlex
- W2151227169
- Cited by
- 569
- References
- 79
- Citations by year
- 2026: 16 · 2025: 52 · 2024: 18 · 2023: 17 · 2022: 20 · 2021: 31 · 2020: 39 · 2019: 43 · 2018: 26 · 2017: 44 · 2016: 29 · 2015: 46 · 2014: 46 · 2013: 39 · 2012: 41
- FWCI
- 19.89
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Computational Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UCL Discovery (University College London) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Explore Bristol Research (submittedVersion)
- Bristol Research (University of Bristol) (submittedVersion, cc-by)
- Funders
- Arts and Humanities Research Council
- Topics
- Health Sciences › Medicine › Gastroenterology › Digestive system and related health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Forensic and Genetic Research
- Keywords
- lactase persistence, lactase gene, dairy production, gene-culture coevolution, positive selection, Neolithic, demic diffusion, approximate Bayesian computation, vitamin D, European ancestry, ancient DNA, subsistence strategies, West Asia
- MeSH terms
- Alleles, Bayes Theorem, Computer Simulation, Diet, Europe, Gene Frequency, Genetic Markers, Geography, Haplotypes, Humans, Lactose, Polymorphism, Genetic, Vitamin D, Evolution, Molecular, Computational Biology, Lactase
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