A variety of researchers are converging on the view that human evolution has been shaped by gene–culture interactions. Theoretical biologists use models to demonstrate that cultural processes can affect human evolution, anthropologists are investigating cultural practices that modify current selection, and geneticists are uncovering alleles that have been subject to recent selection because of human activities.
Theoretical population genetics models are used to explore how genes and culture interact over evolutionary time, including how and why culture can affect evolutionary rates.
Niche-construction theory is a branch of evolutionary biology that emphasizes the capacity of organisms to modify natural selection and thereby act as co-directors of their own, and other species', evolution. Humans are the ultimate niche-constructing species. We specify how variation in buffering through cultural niche construction could explain geographical variation in human genes.
A further source of evidence for gene–culture co-evolution comes from anthropological studies of contemporary human populations, which demonstrate gene–culture co-evolution in action. Examples include Kwa-speaking yam cultivators in West Africa whose agriculture favoured the haemoglobin S (HbS) 'sickle-cell' allele, and Polynesian voyages that led to positive selection for thrifty metabolism, leading to type 2 diabetes susceptibility.
Geneticists have recently developed methods to identify alleles that have been favoured by recent selection, many of which seem to have been favoured because of cultural activities. Overrepresented categories of genes that have been subject to positive selection include those related to recent changes in human diet and human-induced disease.
The well-researched example of co-evolution of dairy farming and the lactase gene shows the range of methods used to investigate gene–culture co-evolution.
We end by asking how prevalent gene–culture co-evolution is, and how researchers can differentiate between a molecular signature of selection generated by gene–culture co-evolution and one generated from a non-cultural aspect of the environment.
Researchers from diverse backgrounds are converging on the view that human evolution has been shaped by gene–culture interactions. Theoretical biologists have used population genetic models to demonstrate that cultural processes can have a profound effect on human evolution, and anthropologists are investigating cultural practices that modify current selection. These findings are supported by recent analyses of human genetic variation, which reveal that hundreds of genes have been subject to recent positive selection, often in response to human activities. Here, we collate these data, highlighting the considerable potential for cross-disciplinary exchange to provide novel insights into how culture has shaped the human genome.
Your institute does not have access to this article
Open Access articles citing this article.
Scientific Reports Open Access 12 July 2022
Philosophy & Technology Open Access 27 May 2022
Human Genomics Open Access 29 January 2022
Subscribe to Journal
Get full journal access for 1 year
only $4.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Klein, R. G. The Human Career: Human Biological and Cultural Origins (Univ. of Chicago Press, 1999).
Wheeler, P. E. The thermoregulatory advantages of hominid bipedalism in open equatorial environments: the contribution of increased convective heat loss and cutaneous evaporative cooling. J. Hum. Evol. 21, 107–115 (1991).
Boyd, R. & Silk, J. How Humans Evolved 3rd edn (Norton & Co., New York, 2003).
Kingdon, J. Lowly Origins (Princeton Univ. Press, 2003).
Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001).
Voight, B. F., Kudaravalli, S., Wen, X. & Pritchard, J. K. A map of recent positive selection in the human genome. PLoS. Biol. 4, e72 (2006).
Wang, E. T., Kodama, G., Baldi, P. & Moyzis, R. K. Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc. Natl Acad. Sci. USA 103, 135–140 (2006). References 6 and 7 describe alleles that have been subject to recent rapid selection and posit a role for cultural practices.
Sabeti, P. C. et al. Positive natural selection in the human lineage. Science 312, 1614–1620 (2006).
Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913–918 (2007).
Nielsen, R., Hellmann, I., Hubisz, M., Bustamante, C. & Clark, A. G. Recent and ongoing selection in the human genome. Nature Rev. Genet. 8, 857–868 (2007).
Tang, K., Thornton, K. R. & Stoneking, M. A new approach for using genome scans to detect recent positive selection in the human genome. PLoS. Biol. 5, e171 (2007).
Durham, W. H. Co-evolution: Genes, Culture and Human Diversity (Stanford Univ. Press, 1991). A classic anthropological text that investigates the relationship between genes and culture.
Holden, C. & Mace, R. Phylogenetic analysis of the evolution of lactose digestion in adults. Hum. Biol. 69, 605–628 (1997). A comparative statistical model that was used to test hypotheses about the evolution of lactose absorption in humans.
Williamson, S. H. et al. Localizing recent adaptive evolution in the human genome. PLoS. Genet. 3, e90 (2007).
Burger, J., Kirchner, M., Bramanti, B., Haak, W. & Thomas, M. G. Absence of the lactase-persistence-associated allele in early Neolithic Europeans. Proc. Natl Acad. Sci. USA 104, 3736–3741 (2007).
Tishkoff, S. A. et al. Convergent adaptation of human lactase persistence in Africa and Europe. Nature Genet. 39, 31–40 (2007).
Hawks, J., Wang, E. T., Cochran, G. M., Harpending, H. C. & Moyzis, R. K. Recent acceleration of human adaptive evolution. Proc. Natl Acad. Sci. USA 104, 20753–20758 (2007).
Varki, A., Geschwind, D. H. & Eichler, E. E. Explaining human uniqueness: genome interactions with environment, behaviour and culture. Nature Rev. Genet. 9, 749–763 (2008).
Feldman, M. W. & Cavalli-Sforza, L. L. Cultural and biological evolutionary processes, selection for a trait under complex transmission. Theor. Popul. Biol. 9, 238–259 (1976).
Cavalli-Sforza, L.L. & Feldman, M. W. Cultural Transmission and Evolution: A Quantitative Approach (Princeton Univ. Press, 1981). A classic book that describes the mathematical modelling of human culture and its co-evolution with genes using theoretical population genetics.
Boyd, R. & Richerson, P. J. Culture and the Evolutionary Process (Univ. of Chicago Press, 1985). Another classic book on the mathematical modelling of human culture and its co-evolution with genes, but with a more anthropological perspective.
Feldman, M. W. & Laland, K. N. Gene–culture co-evolutionary theory. Trends Ecol. Evol. 11, 453–457 (1996).
Enquist, M., Eriksson, K. & Ghirlanda, S. Critical social learning: a solution to Roger's paradox of nonadaptive culture. Am. Anthropol. 109, 727–734 (2007).
Odling-Smee, F. J., Laland, K. N. & Feldman, M. W. Niche Construction: The Neglected Process in Evolution. Monographs in Population Biology 37 (Princeton Univ. Press, 2003). The major book on niche-construction theory.
Kylafis, G. & Loreau, M. Ecological and evolutionary consequences of niche construction for its agent. Ecol. Lett. 11, 1072–1081 (2008).
Laland, K. N., Odling-Smee, F. J. & Feldman, M. W. On the evolutionary consequences of niche construction. J. Evol. Biol. 9, 293–316 (1996).
Laland, K. N., Odling-Smee, F. J. & Feldman, M. W. Evolutionary consequences of niche construction and their implications for ecology. Proc. Natl Acad. Sci. USA 96, 10242–10247 (1999). A key paper on niche-construction theory.
Boni, M. F. & Feldman, M. W. Evolution of antibiotic resistance by human and bacterial niche construction. Evolution 59, 477–491 (2005).
Lehmann, L. The adaptive dynamics of niche constructing traits in spatially subdivided populations: evolving posthumous extended phenotypes. Evolution 62, 549–566 (2008).
Silver, M. & Di Paolo, E. Spatial effects favour the evolution of niche construction. Theor. Popul. Biol. 20, 387–400 (2006).
Feldman, M. W. & Cavalli-Sforza, L. L. in Mathematical Evolutionary Theory (ed. Feldman, M. W.) 145–173 (Princeton Univ. Press, 1989).
Ehrlich, P. R. Human Natures: Genes, Cultures, and the Human Prospect (Island Press, Washington DC, 2000).
Richerson, P. J. & Boyd, R. Not By Genes Alone: How Culture Transformed Human Evolution (Univ. of Chicago Press, 2005).
Laland, K. N. Exploring gene–culture interactions: insights from handedness, sexual selection and niche-construction case studies. Phil. Trans. R. Soc. Lond. B 363, 3577–3589 (2008).
Laland, K. N. & Brown, G. R. Sense and Nonsense: Evolutionary Perspectives on Human Behaviour (Oxford Univ. Press, 2002).
Rogers, A. Does biology constrain culture? Am. Anthropol. 90, 819–813 (1988).
Laland, K. N., Kumm, J., Van Horn, J. D. & Feldman, M. W. A gene–culture model of handedness. Behav. Genet. 25, 433–445 (1995).
Cavalli-Sforza, L. L. & Feldman, M. W. Models for cultural inheritance I: group mean and within-group variation. Theor. Popul. Biol. 4, 42–55 (1973).
Otto, S. P., Christiansen, F. B. & Feldman, M. W. Genetic and Cultural Inheritance of Continuous Traits. Morrison Institute for Population and Resource Studies Paper Number 0064 (Stanford Univ. Press, 1995).
Bersaglieri, T. et al. Genetic signatures of strong recent positive selection at the lactase gene. Am. J. Hum. Genet. 74, 1111–1120 (2004).
Laland, K. N. Sexual selection with a culturally transmitted mating preference. Theor. Popul. Biol. 45, 1–15 (1994).
Laland, K. N., Kumm, J. & Feldman, M. W. Gene–culture co-evolutionary theory: a test case. Curr. Anthropol. 36, 131–156 (1995).
Cochran, G. & Harpending, H. The 10,000 Year Explosion. How Civilization Accelerated Human Evolution (Basic Books, New York, 2009).
Coop, G. et al. 2009. The role of geography in human adaptation. PLoS Genet. 5, e1000500 (2009). This group studied the geographical distribution of recently selected genes and found that strong sustained selection is rare and partial sweeps are common.
Lewontin, R. C. in Evolution From Molecules to Men (ed. Bendall, D. S.) 273–285 (Cambridge Univ. Press, 1983).
Laland, K. N., Odling-Smee, F. J. & Feldman, M. W. Cultural niche construction and human evolution. J. Evol. Biol. 14, 22–33 (2001). A theoretical analysis of human niche construction and its effects on human evolution.
Borenstein, E., Kendal, J. & Feldman, M. W. Cultural niche construction in a metapopulation. Theor. Popul. Biol. 70, 92–104 (2006).
Smith, B. Niche construction and the behavioral context of plant and animal domestication. Evol. Anthropol. 16, 188–199 (2007).
Stringer, C. & Andrews, P. The Complete World of Human Evolution (Thames & Hudson, London, 2005).
Guglielmino, C. R., Viganotti, C., Hewlett, B. & Cavalli-Sforza, L. L. Cultural variation in Africa: role of mechanism of transmission and adaptation. Proc. Natl Acad. Sci. USA 92, 7585–7589 (1995).
Perry, G. H. & Dominy, N. J. Evolution of the human pygmy phenotype. Trends Ecol. Evol. 24, 218–225 (2009).
Fortunato, L. in Early Human Kinship: From Sex To Social Reproduction (eds Allen, N. J., Callan, H., Dunbar, R. & James, W.) 189–199 (Blackwell Publishing, Oxford, 2008).
Mace, R., Holden, C. J. & Shennan, S. (eds) The Evolution Of Cultural Diversity. A Phylogenetic Approach (Left Coast, Walnut Creek, California, 2005).
Balter, M. Are humans still evolving? Science 309, 234–237 (2005).
Hawkes, K., O'Connell, J. F., Blurton-Jones, N. G., Alvarez, H. & Charnov, E. L. Grandmothering, menopause, and the evolution of human life histories. Proc. Natl Acad. Sci. USA 95, 1336–1339 (1998).
Aiello, L. C. & Wheeler, P. The expensive-tissue hypothesis. Curr. Anthropol. 36, 199–221 (1995).
Wrangham, R. W., Jones, J. H., Laden, G., Pilbeam, D. & Conklin-Brittain, N. The raw and the stolen: cooking and the ecology of human origins. Curr. Anthropol. 40, 567–594 (1999).
Sabeti, P. C. et al. Detecting recent positive selection in the human genome from haplotype structure. Nature 419, 832–837 (2002).
Akey, J. M. Constructing genomic maps of positive selection in humans: where do we go from here? Genome Res. 19, 711–722 (2009).
Berglund, J., Pollard, K. S. & Webster, M. T. Hotspots of biased nucleotide substitutions in human genes. PLoS. Biol. 7, e1000026 (2009).
Galtier, N., Duret, L., Glémin, S. & Ranwez, V. GC-biased gene conversion promotes the fixation of deleterious amino acid changes in primates. Trends Genet. 25, 1–5 (2009).
Pickrell, J. K. et al. Signals of recent positive selection in a worldwide sample of human populations. Genome Res. 19, 826–837 (2009).
López Herráez, D. et al. Genetic variation and recent positive selection in worldwide human populations: evidence from nearly 1 million SNPs. PLoS ONE 4, e7888 (2009).
Stefansson, H. et al. A common inversion under selection in Europeans. Nature Genet. 37, 129–137 (2005).
Nguyen, D-Q., Webber, C. & Ponting, C. P. Bias of selection on human copy-number variants. PLoS Genet. 2, e20 (2006).
Prabhakar, S. et al. Human-specific gain of function in a developmental enhancer. Science 321, 1346–1350 (2008).
Quach, H. et al. Signatures of purifying and local positive selection in human miRNAs. Am. J. Hum. Genet. 84, 316–327 (2009).
Evans, P. D. et al. Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science 309, 1717–1720 (2005).
Mekel-Bobrov, et al. Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens. Science 309, 1720–1722 (2005).
Dediu, D. & Ladd, D. R. Linguistic tone is related to the population frequency of the adaptive haplogroups of two brain size genes, ASPM and Microcephalin. Proc. Natl Acad. Sci. USA 104, 10944–10949 (2007).
Aoki, K. A stochastic model of gene–culture co-evolution suggested by the 'culture historical hypothesis' for the evolution of adult lactose absorption in humans. Proc. Natl Acad. Sci. USA 83, 2929–2933 (1986).
Itan, Y., Powell, A., Beaumont, M. A., Burger, J. & Thomas, M. G. The origins of lactase persistence in Europe. PLoS Comput. Biol. 5, e1000491 (2009).
Nasidze, I., Quinque, D., Rahmani, M., Alemohamad, S. A. & Stoneking, M. Concomitant replacement of language and mtDNA in South Caspian populations of Iran. Curr. Biol. 16, 668–673 (2006).
Kayser, M. et al. Melanesian and Asian origins of Polynesians: mtDNA and Y chromosome gradients across the Pacific. Mol. Biol. Evol. 23, 2234–2244 (2006).
Oota, H., Settheetham-Ishida, W., Tiwawech, D., Ishida, T. & Stoneking, M. Human mtDNA and Y-chromosome variation is correlated with matrilocal versus patrilocal residence. Nature Genet. 29, 20–21 (2001). This article shows how cultural boundaries can shape gene flow.
Cordaux, R. et al. Independent origins of Indian caste and tribal paternal lineages. Curr. Biol. 14, 231–235 (2004).
Fisher, S. E., Vargha-Khadem, F., Watkins, K. E., Monaco, A. P. & Pembrey, M. E. Localisation of a gene implicated in a severe speech and language disorder. Nature Genet. 18, 168–170 (1998).
Enard, W. et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418, 869–872 (2002).
Enard, W. et al. A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 137, 961–971 (2009).
Stedman, H. H. et al. Myosin gene mutation correlates with anatomical changes in the human lineage. Nature 428, 415–418 (2004).
Liao, B. Y. & Zhang, J. Null mutations in human and mouse orthologs frequently result in different phenotypes. Proc. Natl Acad. Sci. USA 105, 6987–6992 (2008).
Caspari, R. & Lee, S. H. Older age becomes common late in human evolution. Proc. Natl Acad. Sci. USA 101, 10895–10900 (2004).
Scrimshaw, N. & Murray, E. The acceptability of milk and milk products in populations with a high prevalence of lactose intolerance. Am. J. Clin. Nutr. 48, 1079–1159 (1988).
Hollox, E. J. et al. Lactase haplotype diversity in the old world. Am. J. Hum. Genet. 68, 160–172 (2001).
Swallow, D. M. Genetics of lactase persistence and lactose intolerance. Annu. Rev. Genet. 37, 197–219 (2003).
Enattah, N. S. et al. Identification of a variant associated with adult-type hypolactasia. Nature Genet. 30, 233–237 (2002).
Lewinsky, R. H. et al. T-13910 DNA variant associated with lactase persistence interacts with Oct-1 and stimulates lactase promoter activity in vitro. Hum. Mol. Genet. 14, 3945–3953 (2005).
Enattah, N. S. et al. Independent introduction of two lactase-persistence alleles into human populations reflects different history of adaptation to milk culture. Am. J. Hum. Genet. 82, 57–72 (2008).
Ulijaszek, S. J. & Strickland, S. S. Nutritional Anthropology: Prospects and Perspectives (Smith-Gordon, London, 1993).
Myles, S. et al. Genetic evidence in support of a shared Eurasian–North African dairying origin. Hum. Genet. 117, 34–42 (2005).
Simoons, F. Primary adult lactose intolerance and the milking habit: a problem in biological and cultural interrelations. II. A culture historical hypothesis. Dig. Dis. Sci. 15, 695–710 (1970).
Beja-Pereira, A. et al. Gene–culture co-evolution between cattle milk protein genes and human lactase genes. Nature Genet. 35, 311–313 (2003).
Laland, K. N. & Galef B. G. Jr (eds) The Question of Animal Culture (Harvard Univ. Press, 2009).
Lachlan, R. F. & Slater, P. J. B. The maintenance of vocal learning by gene–culture interaction: the cultural trap hypothesis. Proc. R. Soc. Lond. B 266, 701–706 (1999).
Beltman, J.B., Haccou, P. & ten Cate, C. The impact of learning foster species' song on the evolution of specialist avian brood parasitism. Behav. Ecol. 14, 917–923 (2003).
Beltman, J. B., Haccou, P. & ten Cate, C. Learning and colonization of new niches: a first step towards speciation. Evolution 58, 35–46 (2004).
Bryk, J. et al. Positive selection in East Asians for an EDAR allele that enhances NF-κB activation. PLoS ONE 3, e2209 (2008).
Chang, S. H. et al. Enhanced Edar signalling has pleiotropic effects on craniofacial and cutaneous glands. PLoS ONE 4, e7591 (2009).
Izagirre, N., Garcia, I., Junquera, C., de la Rua, C. & Alonso, S. A scan for signatures of positive selection in candidate loci for skin pigmentation in humans. Mol. Biol. Evol. 23, 1697–1706 (2006).
Lao, O., de Gruijter, J. M., van Duijn, K., Navarro, A. & Kayser, M. Signatures of positive selection in genes associated with human skin pigmentation as revealed from analyses of single nucleotide polymorphisms. Ann. Hum. Genet. 71, 354–369 (2007).
Myles, S., Somel, M., Tang, K., Kelso, J. & Stoneking, M. Identifying genes underlying skin pigmentation differences among human populations. Hum. Genet. 120, 613–621 (2007).
Myles, S. et al. Identification and analysis of high Fst regions from genome-wide SNP data from three human populations. Ann. Hum. Genet. 72, 99–110 (2008).
Ihara, Y., Aoki, K. & Feldman, M. W. Runaway sexual selection with paternal transmission of the male trait and gene–culture determination of the female preference. Theor. Popul. Biol. 63, 53–62 (2003).
Livingstone, F. B. Anthropological implications of sickle-cell distribution in West Africa. Am. Anthropol. 60, 533–562 (1958).
Hawley, W. A., Reiter, P., Copeland, R. S., Pumpuni, C. B. & Craig, G. B. Aedes albopictus in North America: probable introduction in used tires from Northern Asia. Science 236, 1114–1116 (1987).
Bindon, J. R. & Baker, P. T. Bergmann's rule and the thrifty genotype. Am. J. Phys. Anthropol. 104, 201–210 (1997).
Houghton, P. The adaptive significance of Polynesian body form. Ann. Hum. Biol. 17, 19–32 (1990).
Myles, S. et al. Identification of a candidate genetic variant for the high prevalence of type II diabetes in Polynesians. Eur. J. Hum. Genet. 15, 584–589 (2007).
Neel, J. V. Diabetes mellitus: a 'thrifty' genotype rendered detrimental by 'progress'? Bull. World Health Organ. 77, 694–703 (1962).
Gleibermann, L. Blood pressure and dietary salt in human populations. Ecol. Food Nutr. 2, 143–156 (1973).
Young, J. H. et al. Differential susceptibility to hypertension is due to selection during the out-of-Africa expansion. PLoS Genet. 1, e82 (2005).
Perry, G. H. et al. Diet and the evolution of human amylase gene copy number variation Nature Genet. 39, 1256–1260 (2007). A good example of gene–culture co-evolution in which changes in human diet favour copies of a gene.
Richards, M. P., Schulting, R. J. & Hedges, R. E. M. Archaeology: sharp shift in diet at onset of Neolithic. Nature 425, 366 (2003).
Kelley, J. L. & Swanson, W. J. Dietary change and adaptive evolution of enamelin in humans and among primates. Genetics 178, 1595–1603 (2008).
Soranzo, N. et al. Positive selection on a high-sensitivity allele of the human bitter-taste receptor TAS2R16. Curr. Biol. 15, 1257–1265 (2005).
Haygood, R., Fedrigo, O., Hanson, B., Yokoyama, K. D. & Wray, G. A. Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nature Genet. 39, 1140–1144 (2007).
Chen, C. et al. Interaction between the functional polymorphisms of the alcohol-metabolism genes in protection against alcoholism. Am. J. Hum. Genet. 65, 795–807 (1999).
Han, Y. et al. Evidence of positive selection on a class I ADH locus. Am. J. Hum. Genet. 80, 441–456 (2007).
Boyd, R. & Richerson, P. Why does culture increase human adaptability? Ethol. Sociobiol. 16, 125–143 (1995).
Feldman, M. W. & Zhivotovsky, L. A. Gene–culture co-evolution: towards a general theory of vertical transmission. Proc. Natl Acad. Sci. USA 89, 11935–11938 (1992).
Feldman, M., Aoki, K. & Kumm, J. Individual versus social learning: evolutionary analysis in a fluctuating environment. Anthropol. Sci. 104, 209–231 (1996).
Henrich, J. & Boyd, R. The evolution of conformist transmission and the emergence of between-group differences. Evol. Hum. Behav. 19, 215–241 (1998).
Henrich, J. & McElreath, R. The evolution of cultural evolution. Evol. Anthropol. 12, 123–135 (2003).
Efferson, C., Lalive, R., Richerson, P., McElreath, R. & Lubell, M. Conformists and mavericks: the empirics of frequency-dependent cultural transmission. Evol. Hum. Behav. 29, 56–64 (2008).
Aoki, K. & Feldman, M. W. Toward a theory for the evolution of cultural communication: co-evolution of signal transmission and reception. Proc. Natl Acad. Sci. USA 84, 7164–7168 (1987).
Aoki, K. & Feldman, M. W. Pleiotrophy and preadaptation in the evolution of human language capacity. Theor. Popul. Biol. 35, 181–194 (1989).
Aoki, K. & Feldman, M. W. Recessive hereditary deafness, assortative mating, and persistence of a sign language. Theor. Popul. Biol. 39, 358–372 (1991).
Lachlan, R. F. & Feldman, M. W. Evolution of cultural communication systems: the co-evolution of cultural signals and genes encoding learning preferences J. Evol. Biol. 16, 1084–1095 (2003).
Feldman, M. W. & Otto, S. P. Twin studies, heritability, and intelligence. Science 278, 1383–1384 (1997).
Cochran, G., Hardy, J. & Harpending, H. Natural history of Ashkenazi intelligence. J. Biosoc. Sci. 38, 659–693 (2005).
Boyd, R. & Richerson, P. J. Cultural transmission and the evolution of cooperative behavior. Hum. Ecol. 10, 325–351 (1982).
Boyd, R. & Richerson, P. J. The evolution of reciprocity in sizeable groups. J. Theor. Biol. 132, 337–356 (1988).
Boyd, R., Gintis, H., Bowles, S. & Richerson, P. J. The evolution of altruistic punishment. Proc. Natl Acad. Sci. USA 100, 3531–3535 (2003).
Henrich, J. et al. Costly punishment across human societies. Science 312, 1767–1770 (2006).
Gintis, H. The hitchhiker's guide to altruism: gene–culture co-evolution, and the internalization of norms. J. Theor. Biol. 220, 407–418 (2003).
Gintis, H. The genetic side of gene–culture co-evolution: internalization of norms and prosocial emotions. J. Econ. Behav. Organ. 53, 57–67 (2004).
Fehr, E. & Fischbacher, U. The nature of human altruism. Nature 425, 785–791 (2003).
McElreath, R., Boyd, R. & Richerson, P. J. Shared norms and the evolution of ethnic markers. Curr. Anthropol. 44, 122–129 (2003).
Lumsden, C. J. & Wilson, E. O. Genes, Mind and Culture (Harvard Univ. Press, 1981).
Aoki, K. & Feldman, M. W. A gene–culture co-evolutionary model for brother–sister mating. Proc. Natl Acad. Sci. USA 94, 13046–13050 (1997).
Mesoudi, A. & Laland, K. N. Culturally transmitted paternity beliefs and the evolution of human mating behaviour. Proc. R. Soc. Lond. B 274, 1273–1278 (2007).
Kumm, J., Laland, K. N. & Feldman, M. W. Gene–culture co-evolution and sex ratios: the effects of infanticide, sex-selective abortion, and sex-biased parental investment on the evolution of sex ratios. Theor. Popul. Biol. 46, 249–278 (1994).
Kumm, J. & Feldman, M. W. Gene–culture co-evolution and sex ratios: II. Sex-chromosomal distorters and cultural preferences for offspring sex. Theor. Popul. Biol. 52, 1–15 (1997).
Osier, M. V. et al. A global perspective on genetic variation at the ADH genes reveals unusual patterns of linkage disequilibrium and diversity. Am. J. Hum. Genet. 71, 84–99 (2002).
Elbers, C. C. et al. Variants in neuropeptide Y receptor 1 and 5 are associated with nutrient-specific food intake and are under recent selection in Europeans. PLoS ONE 4, e7070 (2009).
Thompson, E. E. et al. CYP3A variation and the evolution of salt-sensitivity variants. Am. J. Hum. Genet. 75, 1059–1069 (2004).
Wooding, S. P. et al. DNA sequence variation in a 3.7-kb noncoding sequence 5′ of the CYP1A2 gene: implications for human population history and natural selection. Am. J. Hum. Genet. 71, 528–542 (2002).
Saunders, M. A., Hammer, M. F. & Nachman, M. W. Nucleotide variability at G6pd and the signature of malarial selection in humans. Genetics 162, 1849–1861 (2002).
Nielsen, R., Hellmann, I., Hubisz, M., Bustamante, C. & Clark, A. G. Recent and ongoing selection in the human genome. Nature Rev. Genet. 8, 857–868 (2007).
Hancock, A. M. et al. Adaptations to climate in candidate genes for common metabolic disorders. PLoS Genet. 4, e32 (2008).
Sulem, P. et al. Genetic determinants of hair, eye and skin pigmentation in Europeans. Nature Genet. 39, 1443–1452 (2007).
The authors' research was supported in part by grants from the Biotechnology and Biological Sciences Research Council (BB/C005430/1) and the European Union (NESTPathfinder, CULTAPTATION) to K.N.L. S.M. is supported by the US Department of Agriculture. We are grateful to M. Feldman, L. Fortunato, P. Sabeti and M. Stoneking for helpful comments on earlier drafts of this manuscript.
The authors declare no competing financial interests.
About this article
Cite this article
Laland, K., Odling-Smee, J. & Myles, S. How culture shaped the human genome: bringing genetics and the human sciences together. Nat Rev Genet 11, 137–148 (2010). https://doi.org/10.1038/nrg2734
Human Genomics (2022)
Scientific Reports (2022)
Journal for General Philosophy of Science (2022)
Philosophy & Technology (2022)