Human populations have increased immensely in numbers during the past 50,000 years or more. In the last 40,000 years, positive selection has accelerated greatly among humans and the past 10,000 years have seen rapid skeletal and dental evolution and the appearance of many new genetic responses to diets and disease in human populations (Hawks 2007). As with any other species, human populations are subject to the usual forces of natural selection and are continuously evolving. However, accounts of human evolution frequently assume that the selective events that shaped human populations were changes in the external environment that were beyond human control. While the usual forces, famine, disease, and climate, have profoundly influenced human evolution, a new force has stirred the minds of many evolutionists: human culture. Human culture, defined as information that is capable of affecting individuals' behavior, which they acquire from other individuals through teaching, imitation, and other forms of social learning (Laland 2010), has been a powerful force of natural selection as people adapt genetically to sustained cultural changes such as new diets and modified environmental conditions. 'Information,' used in the definition of culture, includes knowledge, beliefs, values, and skills. The rapid and dramatic cultural change in recent times due to economic development, globalization of culture, and technological advancement has had a profound effect in shaping human evolution. Diseases and domesticates from all around the world have been introduced to climatically compatible regions. Large populations of mixed-race people have emerged. Many populations have reduced exposure to infectious diseases. Some populations have become so wealthy that consumption of food leads to diseases of nutritional excess rather than diseases of nutritional deficiency. Kin have become less important in social networks in urban societies, leading to a host of fitness-related changes (Richerson 2010). These cultural changes all have generated a measurable selective pressure on genes. Analyses of data from the human genome reveal numerous genes that have experienced positive selection, many of which exhibit functions that imply that they are responses to human cultural practices (Voight 2006). The implication of this gene-culture co-evolution theory is profound, it implies that for the last 40,000 years or so, humans have inadvertently been shaping their own evolution. Gene-culture dynamics are faster, stronger, and operate over a broader range of conditions than conventional evolutionary dynamics, which leads to the argument that gene-culture co-evolution could be the dominant mode of human evolution.
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Genes and culture resemble a symbiosis - two inheritance systems occupying the same physical body (Richerson 2010). Genes and culture are two interacting forms of inheritance, with offspring acquiring both a genetic and a cultural legacy from their ancestors. Genetic tendencies influence what cultural organisms learn and culturally transmitted information spreads through populations, modifying selection pressures that act back on populations (Laland 2010). As a result of this cycle, gene-culture co-evolutionists view culture as an active process that can shape the material world. Through gene-culture analyses, which explore how learned behavior co-evolves with alleles that affect the expression of the behavior, models have shown that cultural processes can dramatically affect the rate of change of allele frequencies in response to selection (Feldman 1996). These models include the lactose-tolerance allele that has spread from low to high frequencies, the EDAR gene that is associated with thicker hair that has experienced a gene-culture co-evolutionary version of sexual selection, and the HbS sickle cell allele in West Africa that has increased due to protection against malaria (Laland 2010). Culture has long seemed to play the opposite role, according to many biologists, than seen in the light of gene-culture co-evolutionists. Biologists have seen culture as a potential shield from selective pressures. Culture was thought to have a buffering action that would blunt the rate of human evolution or even bring it to a halt. For example, clothes and shelter protect humans from the dangers of cold and farming helps grow crops to avoid famine. This buffering action is instead caused by counteractive nice construction, part of the niche-construction theory, which will be explained in detail later. While it does shield humans from other forces, culture itself is a powerful force of natural selection. In fact, culturally derived selection pressures are stronger than non-cultural ones. Cultural processes occur by way of acquired knowledge carried in human brains that is transmitted between individuals. There's evidence that culturally modified selective environments are capable of producing strong natural selection that is highly consistence in directionality over time. Also, many genes are favored as a result of co-evolutionary events that are activated by phenotypic changes in other species (Bersaglieri 2004). If a cultural practice modifies selection on human genes, the larger the number of individuals exhibiting the cultural trait, the greater is the intensity of selection on the gene. A quick spread of the cultural practice leads to maximal intensity of selection on the advantageous genetic variant (Laland 2010). Culturally derived selection, therefore, can produce selective pressures stronger and faster than non-cultural pressures. The gene-culture co-evolutionary models exemplify this idea by reporting more rapid responses to selection than conventional population genetic models. In addition to the gene-culture co-evolutionary theory, the niche-construction theory, which investigates the evolutionary impact of the modification of environments by organisms also demonstrates how humans have co-directed human evolution. Over the past 50,000 years, humans have spread to the far corners of the world, begun to exploit agriculture, domesticated hundreds of species of plants and animals, and experienced closer proximities to animal pathogens. These events, all self imposed, represent a major transformation in human selection pressures (Smith 2007). The niche-construction theory leads to the expectation that gene-culture co-evolution has been a general feature of human evolution. Part of the niche-construction theory is counteractive niche construction which occurs when an organism responds to change in an environmental factor. Counteractive niche construction may oppose or nullify the effects of environmental change leading to the buffering of selection. Variation in the capacity for counteractive niche construction potentially explains genetic differences between humans and other animals and geographical variation in human allele frequencies (Laland 2001).
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Gene-culture co-evolutionary theory provides possible explanations for why genes expressed in the externally visible phenotype might be likely targets for selection. Genes that are associated with externally visible phenotypes in humans show the strongest signatures of local adaptation (Laland 2010). For example, the lighter skin pigmentation in non-African populations is the result of selection on a number of skin pigmentation genes, genes that are expressed in hair follicles, eye, and hair color are also well presented in selective events (Voight 2006). While some of this variation is in part due to natural selection, many of the selective events could potentially be explained through a form of sexual selection in which culturally learned mating preferences favor biological traits in the opposite sex. A mathematical model that combines sexual selection and gene-culture co-evolutionary theory was developed to show that even if human mating preferences are learned, socially transmitted and culture-specific, sexual selection will still result. In fact, culturally generated sexual selection was found to be faster and more potent than its gene-based counterpart (Laland 1994). This leads to the hypothesis that social transmission may exert a powerful influence on the selection of secondary sexual characteristics and other physical and personality traits that affect human mate choice. A prime example of a gene associated with externally visible phenotypes is the EDAR gene. The EDAR gene is involved in controlling the growth of hair as well as changed in the skin, teeth, and sweat glands (Sabeti 2007). A variant form of the EDAR gene is very common in East Asians and Native Americans. While one explanation the EDAR gene has experienced strong positive selection is due to the advantage thicker hair provides in Siberian climates, the prominent theory is that the trait became common through a form of gene-culture co-evolution sexual selection. Culture is a source of adaptive behavior in which individuals acquire solutions to problems, such as the question "with whom to mate?" The EDAR gene illustrates how learned behavior co-evolves with alleles that affects the expression and/or acquisition of the behavior or whose fitness is affected by the cultural environment (Sabeti 2007).
Anthropological and archaeological studies of contemporary, or recent, human populations demonstrate gene-culture co-evolution in action. While researchers usually develop hypotheses based on theory or derived from observations of human interactions with environments, recent years have witnessed the emergence of mathematical phylogenetic methods applied to cultural variation. One of the best known cases of gene-culture co-evolution in anthropology is the "sickle-cell" gene in the presence of malaria. While clearing forests to grow crops, often yams, the Kwa-speaking agriculturists from West Africa inadvertently increased the amount of standing water when it rained due to the removal of trees. The standing water provided better breeding grounds for malaria-carrying mosquitoes. This intensified natural selection on the hemoglobin S sickle-cell allele because it presents protection against malaria in the heterozygous form. Adjacent populations whose agricultural practices are difference did not show the same increase in allele frequency which leads to the idea that cultural practices can drive genetic evolution (Livingstone 1958). Malaria became a health problem only after the invention of farming, but several genes seem to have been favored by selection because they provide resistance to the disease. Another case of gene-culture co-evolution in anthropology is the dispersal into new environments, which is an example of inceptive niche construction (i.e. When an organism invades a new environment) initiating selection on human genes. The dispersal of human ancestors and the cultural capabilities that made such dispersals possible had the potential to shape the genetic landscape worldwide. For example, ancestors of present-day Polynesians experienced long ocean voyages, which subjected them to cold stress and starvation. There may have been strong selection for energetic efficiency during the Polynesian migrations (Houghton 1990). A type 2 diabetes-associated allele that may have lead to a thrifty metabolism shows a signature of strong positive selection in Polynesians. Present-day Polynesians may have inherited increased type 2 diabetes susceptibility due to the dispersal of their ancestors (Houghton 1990).
Although anthropological theories provide powerful evidence for gene-culture co-evolution, a major roadblock for the gene-culture co-evolution theory has been its lack of evidence in genetic data. However, not until recently, biologists have been able to scan the whole genome for the signatures of genes undergoing selection. Such a signature is formed when one version of a gene becomes more common than other versions because its owners are leaving more surviving offspring. Genome scans have provided the first steps in evaluating without bias the relative contribution of gene-culture co-evolution to human adaptation. The statistical signatures in the human genome include high-frequency alleles in linkage disequilibrium, unusually long haplotypes of low diversity, and an excess of rare variants (Laland 2010). There are several categories of human genes that seem to be overrepresented in lists of positively selected genes. The shift from a hunter-gatherer nomadic lifestyle to an agrarian lifestyle favored many genes involved in diet and metabolism. Starch consumption is a feature of agricultural societies and hunter-gatherers in arid environments. This behavioral variation raises the possibility that different selective pressures have acted on amylase, the enzyme responsible for starch hydrolysis. Amylase is an enzyme in the saliva that breaks down starch. Perry et al. found that the number of salivary amylase gene is positively correlated with salivary amylase protein level and that individuals from populations with high-starch diets have more amylase gene copies than those with low-starch diets. Higher amylase copy numbers and protein levels are believed to improve digestion of starchy foods (Perry 2007). The transition to novel food sources with the advancement of agriculture and the colonization of new habitats has been a major source of selection on human genes (Voight 2006).
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The most prominent and extensively investigated example of gene-culture co-evolution to date is the co-evolution of dairy farming and adult lactose tolerance. The lactose tolerance in adults illustrates the range of methods that can be used to investigate gene-culture co-evolution, which includes anthropological and demographic studies of the covariation between cultural practices and human phenotypes, detection of a variety of statistical signatures of recent selection by geneticists, analysis of ancient DNA, statistical estimation from genetic data of the magnitude of selection pressures, biochemical analyses, and mathematical models of gene-culture co-evolutionary processes using population genetic and phylogenetic methods (Laland 2010). Throughout most of human history, the ability to digest lactose, the main sugar of milk, has been switched off after weaning since the lactase enzyme that breaks the sugar apart is no longer needed. However, in some populations, lactase activity continues into adulthood, which is known as lactose tolerance. Lactose tolerance is most common in northern Europeans and in pastoralist populations from Africa and the Middle East, but is absent elsewhere, these differences relate to genetic variation near the lactase gene (Aoki 1985). A strong correlation exists across cultures between the frequency of lactose tolerance and a history of dairy farming and milk drinking. This led to the theory that dairying created the selection pressures that drove alleles for lactose tolerance to high frequency. The signature of selection around the lactase gene is one of the strongest in the human genome and the onset of the selection has been dated to 5,000 to 10,000 years ago (Bersaglieri 2004). The lactose-tolerance allele has spread from low to high frequencies in less than 9,000 years since the inception of farming, with an estimated selection coefficient of 0.09 to 0.19 for a Scandinavian population (Bersaglieri 2004). The lactose-tolerance allele was absent in ancient DNA extracted from early Neolithic Europeans which suggests that the allele was absent or at low frequency 7,000 to 8,000 years ago. Neolithic humans exposed themselves to a strong selection pressure for lactose tolerance by drinking fresh milk. When cattle was first domesticated 9,000 years ago and people started consuming fresh milk, selective pressures favored individuals with a mutations that kept the lactase gene switched on. The principle mutation, found among Nilo-Saharan-speaking ethnic groups of Kenya and Tanzania, arose 2,700 to 6,800 years ago, which fits well with archaeological evidence that shows that pastoral peoples from the north reached northern Kenya about 4,500 years ago and southern Kenya and Tanzania 3,300 years ago (Laland 2010). The mutations conferred an enormous selective advantage since those with the mutations not only gained extra energy from lactose but also, in drought conditions, would have benefited from the water in milk. The lactose-tolerance example shows how rapidly a positively selected gene caused by culture can invade a population.
Human culture has shaped the way of life and has had an impact on nearly every aspect of life for the past 50,000 years and onward. Culture has shaped society, human life, nearly all species in this world, and the world itself. Most prominently, human culture has inadvertently shaped human evolution and has been arguably the most dominant mode of human evolution. Given the shallow time depth for selection on many human genes, the case for gene-culture co-evolution is reinforced by the sheer ubiquity of culture in modern human lives - it becomes hard to think of selection acting on humans that would not be modified by culture. The development of an agrarian society, the close proximity of new plants and animals, the development of modern technology, the dispersal of the human population to the ends of the Earth have all contributed to the evolution of the human species. Human culture is cumulative, with tools and technologies building on earlier forms, which implies that humans must possess more culture and more potent culture now than earlier in history which will accelerate gene-culture co-evolution even faster. Through the examples of sexual selection with a culturally transmitted mating preference, anthropological studies of gene-culture co-evolution, genetic responses to human diet, and dairy farming and lactose intolerance, it is undeniable that gene-culture co-evolution has been the dominant mode of human evolution. The case for gene-culture co-evolution does not rest exclusively on genetic date, but is reinforced by theoretical analyses. Theoretical analyses are needed to demonstrate the mechanisms by which gene-culture interactions can affect evolutionary rates and dynamics and explain geographical variation in gene frequencies. However, genetic evidence must be strengthened further in order to validate and prove the gene-culture co-evolution theory. Genome scans that test for selection have severe limitations since they cannot see the signatures of ancient selection, which get washed out by new mutations. Therefore, there is no baseline to judge whether recent natural selection has been greater than in earlier times. There are also likely to be many false positives among genes that seem favored. In time, however, as more genetic and anthropological evidence is gathered, it will be shown that human culture has been the dominant mode of human evolution.