Gene-culture coevolution in the age of genomics

Abstract

The use of socially learned information (culture) is central to human adaptations. We investigate the hypothesis that the process of cultural evolution has played an active, leading role in the evolution of genes. Culture normally evolves more rapidly than genes, creating novel environments that expose genes to new selective pressures. Many human genes that have been shown to be under recent or current selection are changing as a result of new environments created by cultural innovations. Some changed in response to the development of agricultural subsistence systems in the Early and Middle Holocene. Alleles coding for adaptations to diets rich in plant starch (e.g., amylase copy number) and to epidemic diseases evolved as human populations expanded (e.g., sickle cell and G6PD deficiency alleles that provide protection against malaria). Large-scale scans using patterns of linkage disequilibrium to detect recent selection suggest that many more genes evolved in response to agriculture. Genetic change in response to the novel social environment of contemporary modern societies is also likely to be occurring. The functional effects of most of the alleles under selection during the last 10,000 years are currently unknown. Also unknown is the role of paleoenvironmental change in regulating the tempo of hominin evolution. Although the full extent of culture-driven gene-culture coevolution is thus far unknown for the deeper history of the human lineage, theory and some evidence suggest that such effects were profound. Genomic methods promise to have a major impact on our understanding of gene-culture coevolution over the span of hominin evolutionary history.T he human cultural system supports the cumulative evolution of complex adaptations to local, often ephemeral environments. Using elaborate technology and depending on large bodies of cultural knowledge about plants and animals, stone-age foragers spread to a much wider range of habitats than any other mammal, from the frigid tundra in the Arctic to the arid deserts of Australia. The Polynesian outrigger canoe and the Arctic kayak are examples of the astoundingly sophisticated cultural adaptations that people have used to occupy distant corners of the globe. The forms of social organizations observed in humans are more diverse than the rest of the primate order combined. Humans constitute one of the world's most impressive adaptive radiations. We have occupied virtually every habitat on earth by using technology and social organization to generate thousands of socioeconomic systems (1, 2). Cultural Evolution and Gene-Culture CoevolutionCulture has many definitions, but for our purposes a useful one is all of the information that individuals acquire from others by a variety of social learning processes including teaching and imitation (3). Transmission fidelity is often sufficiently high for culture to act as an inheritance system (4). We commonly observe that the ideas, practices, skills, attitudes, norms, art styles, technology, ways of speaking, and other elements...

Evolutionary accounts of human behavioural diversity

“…Gene -culture coevolution research implies that the history of selection on our species is characterized by a dynamic interaction between genetic and cultural inheritance. From the gene -culture coevolutionist's perspective, human beings have continued to experience substantive evolution right to the present day, with the majority of selective sweeps probably triggered by human cultural activities, and this biological change is likely to have affected cognition [51,116]. At this point, it is unclear how many human genes have been subject to recent selection, what their phenotype and selection pressures were, and how they impact on human behaviour.…”

Cultural diversification promotes rapid phenotypic evolution in Xavánte Indians

“…cultural evolution | morphology | mtDNA | multiple factor analysis | Amerindians C lassic hypotheses about modern human evolution frequently assume that the evolutionary forces acting on the populations are triggered mainly by changes in the external (climatic, geographic, topological) environment. However, recent anthropological studies suggest that shifts in cultural practices can potentially modify environmental and behavioral conditions, thus promoting faster evolutionary rates shaped by gene-culture interactions (1)(2)(3)(4)(5). Because humans have lived in small aggregates in most of their evolutionary history, studying the influence of cultural practices on the demographic and genetic parameters of small groups can shed more light on modeling the effect of culture on biological evolution.…”

“…These fissions generally occur along kinship lines, leading to a highly nonrandom migration. Therefore, social structure and cultural practices promote demographic isolation and periodic reshuffling of genetic variation, creating unusual combinations of allele frequencies that may play a role in promoting fast evolution (1)(2)(3)(4)(5). However, welldocumented examples regarding cultural shifts and evolutionary rates involving Native Americans and suggesting some degree of impact of the former on the genetic, phenotypic, or life-history trait variability, are inexistent or very scarce (7).…”

Variants at serotonin transporter and 2A receptor genes predict cooperative behavior differentially according to presence of punishment

“…Moreover, it suggests an additional route by which cross-cultural variation in cooperation could be produced. Whereas the ability of cultural environments to shape selective pressures has received attention (33,34), and has even been implicated in the global distribution of the short allele at 5-HTTLPR (35), the possible role of epigenetic regulation in this scenario has not. Genetic variation that enables behavioral plasticity could facilitate the rapid evolution of behavior in response to changing environments (36), including sanctioning institutions and other aspects of the sociocultural environment.…”