Is Gene-Culture Coevolution at the Reins of Recent, Rapid Human Evolution?

Recent, Rapid Human Evolution: Is Gene-Culture Coevolution Responsible?

Introduction

The notion that human cultural innovation, and the consequential capacity to change the world around us, has allowed us to sufficiently divorce ourselves from the natural world as to escape natural selection, is pervasive. So much so that entire bodies of human sociobiological work have been built upon it, prime among these being the field of evolutionary psychology with its assumptions that our Neolithic minds have been unable to keep up with our rapidly changing, culturally constructed world (Laland & Brown, 2011). Recent work in molecular evolutionary biology has begun to seriously degrade the plausibility of such viewpoints. Utilising a survey of the human genome, Hawks et al. (2007) have argued, based on single nucleotide polymorphisms and linkage disequilibrium, that in response to human cultural innovations that have occurred within the last 10,000 years, human biological evolution has, far from conforming with the common view above, experienced a period of unprecedented acceleration. It would appear that rather than reducing selection pressures, our cultural innovations (namely agriculture and urbanisation), mobilised as a kind of niche construction (Laland, 2008), have generated potent selective pressures of their own.

The field of ‘gene-culture coevolution’ stands in an ideal location to offer explanations on how these man-made environmental alterations have in turn altered our genes at an unprecedented rate. While much of the early work in this field was theoretical/mathematical in nature (Feldman & Cavalli-Sforza, 1976; Laland & Brown, 2011), the mapping of the human genome and our increasing understanding of which genes are related to particular phenotypes has allowed workers in this field to assess with ever increasing accuracy which genes are likely to have been under recent, culturally mediated, selective pressure (Richerson, Boyd, & Henrich, 2010).

Wang et al. (2006), utilising molecular techniques, identified several functional groupings of genes that seem to have undergone strong recent selection. Among these groupings, three are of particular interest when viewed from the perspective of gene-culture coevolution: genes relating to food processing, genes involved in disease resistance and genes expressed in the brain. This essay shall evaluate a selection of alleles that fall within these three categories in an effort to assess the likelihood that cultural innovations in the last 10,000 years have influenced their selection. In following with the views of Diamond (1991), the position that agriculture, as a niche construction activity, is the key to the development of complex societies shall be taken. Genes that seem to have been placed under greater selective pressure by the adoption of this cultural innovation and associated dietary changes shall be explored first. Secondly, based upon the idea that an agricultural base allows populations of greater density to be built (Diamond, 1991), evidence of genetic change related to resistance of diseases endemic to highly populated areas shall be examined. Finally, evidence for recent selection of genes associated with brain function, the ultimate human tool for social interaction, shall be considered in the light of social changes generated by agriculture and increases in population density.

Agriculture, Diet and Genes

In considering the last 10,000 years, one human cultural innovation dwarfs all others for its flow on effects in terms of the human environment, agriculture (Diamond, 1991).  Agriculture is thought to have arisen independently in (and then culturally radiated out from) various regions, including the Fertile Crescent, Central and Northern Africa, East Asia and the Americas between 7,000 and 10,000 years ago (Diamond, 1991). It is conceivable that this ‘Neolithic Revolution’ marked the beginning of the evolutionary acceleration identified by Hawks et al. (2007). In generating a stable niche in terms of food availability, perhaps in response to a stabilising climate (Richerson, Boyd, & Bettinger, 2001), Neolithic humans likely found themselves consuming a much more homogenous diet and/or utilising nutrient sources previously less favoured (Richerson, et al., 2010). As shall be demonstrated, the resultant change in diet was adequate to increase selection for certain genes that allowed these early agriculturalists to make the most of the nutrient sources present.

The domestication of rice, barley, wheat and other cereal crops, along with root vegetables like potatoes and yams, significantly increased the intake of starch for Neolithic farmers (Meisenberg, 2008).  This would have generated a positive selective pressure for genes allowing more efficient processing of this particular plant carbohydrate. Evidence of this is seen today, as the copy number of the gene AMY1, responsible for the production of salivary amylase (an enzyme that breaks starch into simpler sugars), seems to vary by population group in relation to their history of starch consumption (Ley, Lozupone, Hamady, Knight, & Gordon, 2008; Richerson, et al., 2010). Essentially, populations with a long history of agriculture and thus a starchy diet, have more copies of this particular gene. It is highly likely that this trend had its origins in the Neolithic agricultural revolution.

Molecular evidence derived from the DNA of Southern Chinese populations seems to indicate that fermentation of domesticated plants (the production of alcohol) followed soon after the advent of rice based agriculture in this region (Peng et al., 2010). This trend seems to be temporally true of other early agricultural centers also with various ancient populations (Egypt, Mesopotamia, Greece) seeming to have a long history of alcohol production, based on archaeological evidence (Dietler, 2006). The negative health affects of excessive alcohol consumption are well known today and it would seem that these produced selective pressure for genes that enhance the breakdown of this chemical (Peng, et al., 2010). In the case of the Chinese population mentioned, the enrichment of a certain class of alcohol dehydrogenase sequence polymorphism, dated to approximately 7,000-10,000 years ago, supports this notion (Peng, et al., 2010). Should alcohol consumption indeed generate selective pressures like those posed here, it is expected that other populations with a long history of alcohol consumption should show similar recent adaptations as a function of convergent evolution.

Agriculture, of course, encompasses more than the domestication of plants. The domestication of animals is also thought to have generated pressure for genetic change in early farmers (Laland, Odling-Smee, & Myles, 2010). Perhaps the most well studied example of this relates to the consumption of milk and the persistence of lactase production in adults in populations with a history of this practice (Laland, et al., 2010; Richerson, et al., 2010). The presence of the gene responsible for the persistence of lactase production in European adults (the word persistence is used as all humans produce lactase as infants and generally cease production sometime after weaning in non-milk consuming populations) is estimated to have reached significant frequencies some 5,000-10,000 years ago, based on molecular evidence, and is absent in DNA extracted from ancient remains from earlier time periods (Laland, et al., 2010).  This matches relatively closely with our archaeological understanding of when animal domestication became widespread (Diamond, 1991). The genetic mechanisms behind lactase persistence in non-European populations present compelling evidence for the selective strength of this cultural innovation as different, independently selected, genes are responsible in some populations (Enattah et al., 2008).

In addition to the diet related adaptations mentioned above, agriculture enabled significant changes in human demography. With a stable, agriculture based, source of resources, populations became more sedentary and greater numbers of individuals were able to be supported by a given tract of land (Diamond, 1991). Hawks et al. (2007) have argued that this population boom was in fact responsible for the genetic diversity necessary to fuel the rapid digestive adaptations mentioned and as shall be demonstrated, was likely a crucial factor in the genetic adaptations relating to disease resistance and brain function to be expounded below.

Population Growth, Disease Burden and Genes of Resistance

            The Neolithic agricultural revolution allowed humans to live at densities that had been impossible prior (Diamond, 1991), in turn, this generated an environment in which infectious diseases were readily transmissible (Barnes, Duda, Pybus, & Thomas, 2011). It is conceivable that following outbreaks of diseases endemic to populated areas, individuals with a biological edge, alleles of resistance, would be more likely to pass these useful genes onto future generations. Several recent research projects seem to support this line of reasoning.

One of the most often discussed examples of recent human evolution relating to disease resistance is the advent, and subsequent increase in frequency, of the sickle cell (HbS) gene in response to high rates of infection with malaria in West Africa (Richerson, et al., 2010). In this case, it is thought that the cultivation of yams by West Africans generated large areas of standing water that had previously been non-existent in the area, allowing malaria harbouring mosquitos to proliferate (Laland, 2008). This combined with what was likely a growing agricultural population, created sufficient selective pressure that the HbS gene, only beneficial in a heterozygous state (Laland, 2008), was able to reach incredibly high frequencies for an otherwise fitness reducing, even lethal, gene (Mansilla-Soto, Rivière, & Sadelain, 2011). This speaks volumes for the selective pressures that must have been present, as nothing but an incredibly strong selective environment would encourage the presence of a gene that is only beneficial to 50% of offspring (see Appendix 1).

Tuberculosis is another disease with a long history in human populations, with remains containing molecular traces of this infection being identified from as long ago as 3,000 BCE in Egypt (Zink et al., 2003). It is highly likely that the disease is much older than this, though the debate surrounding its history as a human pathogen is still underway (Smith, Hewinson, Kremer, Brosch, & Gordon, 2009). Recent work on SLC11A1 1729 + 55del4, an allele associated with tuberculosis resistance, has uncovered a positive correlation between the frequency of this gene and the length of urban history for a given population (Barnes, et al., 2011) (Figure 1). This is strong evidence for the above assertion that increased population density should increase disease load and thus select for individuals with resistance to problem infectious diseases.

Figure 1. Time since first urban settlement is displayed on the x-axis while frequency of the allele for tuberculosis resistance is displayed on the y-axis. Mathematical lines of best fit are as published in Barnes et al. (2011). Adapted from Barnes et al. (2011).

It is highly likely that selective pressure from other known population diseases has played a similar role in recent human evolution. Wang et al. (2006) identified at least a half-dozen genes relating to host-pathogen interaction in addition to those given above, some of which with functions that are not yet adequately understood. It is reasonable to predict that should future research into genes associated with resistance to other infectious diseases historically endemic to areas of high population, be carried out (see Conclusion for suggestions), further evidence of how cultural lifestyle changes can influence human biological evolution will be found.

Cultural Change and the Human Brain: How Sociality Shapes Our Genes

            Ultimately, living in social groups, especially those of the size and complexity characteristic of large agricultural settlements (and eventually cities), relied upon the ability of ancient humans to successfully interact with one another. If cultural innovations, such as agriculture and following this settlements and cities, have produced selective pressures sufficient to change our genes with regard to food digestion and disease resistance, it is sensible to infer that changes to genes relating to our neurophysiology, and thus interactive capacities, should also be present. The findings of Wang et al. (2006) and Laland (2008), among others,  seem to suggest just this.

While the brain expressed genes identified by Wang et al. (2006) are thought to have undergone rapid, recent selection, their functions are unfortunately as of yet unknown. Laland (2008), however, lists 29 recently selected genes thought to be related to nervous system and brain ontogeny, brain function and, importantly, language skills and learning. The role of learning and communication in cultural innovation is extremely important (Laland & Hoppitt, 2003), it is thus unsurprising that genes relating to such functions have undergone recent selection in light of the societal changes discussed prior.

Perhaps more interestingly, work within the last two years has identified potentially recent polymorphisms of a gene that may represent a genetic consequence of selective pressures generated by a cultural interaction style. Chiao & Blizinsky (2009) reported that the 5-HTTLPR gene, associated with serotonin reuptake and thus mood, is present in long and short alleles that are geographically distributed in a manner fairly consistent with our notions of collectivist and individualist cultures (Figure 2). The short allele, argued to be related to collectivist cultures (Chiao & Blizinsky, 2009), essentially allows less reuptake of serotonin at the synapses, much the same affect exerted by many of today’s common antidepressant and antianxiety drugs (Bullock, Manias, & Galbraith, 2006). This has the mean result of elevating mood and, as Chiao & Blizinksy (2009) argue, reducing rates of behaviour that are harmful to social harmony (and thus fitness reducing, for both the errant individual and the group).

Furthermore, Chiao & Blizinksy (2009), relating back to the previous section on infectious disease, propose that collectivism seems to correlate with populations with a history of high disease burden and argue that selection for collectivist behaviour is somehow protective in this regard. This remains to be explored more comprehensively and may well represent a case of correlation as opposed to causation. While the question of how societies come to be collectivist or individualist to begin with remains largely unanswered, this study does provide a relatively robust example of a relationship that exists between a gene and an observable cultural selective pressure.  It is conceivable that such pressures have exerted impacts on other genes relating to behaviour or cognition. Genes relating to other neurotransmitters, perhaps dopamine or gamma-amino butyric acid, seem likely targets given their role in the regulation of human emotional states.

Figure 2. Distribution of the S (short) allele of the 5-HTTLPR gene in relation to individualism-collectivism and prevalence of anxiety across countries. Adapted from Chiao & Blizinsky (2009).

Conclusion

            Utilising modern molecular techniques, it is evident that a considerable number of human genes have undergone recent and rapid change (Hawks, et al., 2007). Many of these changes are estimated to have occurred within the last 10,000 years (Hawks, et al., 2007), a period of great cultural change that saw the adoption of agriculture and as a consequence sedentary settlements that, in some cases, grew to become the first urban centres (Diamond, 1991). Generally, niche construction activities are undertaken by animals in order to reduce the impact of environmental change, and this was likely the case for the first Neolithic farmers (Laland, 2008; Richerson, et al., 2001). The flow on effects of agriculture and subsequent human cultural innovation, however, produced a novel and rapidly changing environment with selective pressures of its own. It could be argued that these culturally mediated selective pressures outstripped their ecological predecessors for selective sway, generating a range of genetic adaptations related to diet, resistance to disease and neurophysiology (Barnes, et al., 2011; Chiao & Blizinsky, 2009; Laland, 2008; Richerson, et al., 2010), at a rate possibly unmatched in prior Homo evolution.

As further studies of the human genome for signatures of recent evolutionary change are performed, it is anticipated that further evidence for this period of rapid evolution will be found in gene-culture coevolutionary studies. Of particular interest to future researchers might be genes associated with resistance to dietary diseases (diabetes, obesity and vitamin D deficiency), other diseases endemic to highly populated areas (smallpox, the black death, influenza and more recently, HIV/AIDS) and the search for further evidence of cognitive changes related to an increasingly social lifestyle, especially where tolerance of non-kin is concerned.

In closing, it should be mentioned here that the above model, for the sake of brevity, has not considered how a lack of agricultural culture would manifest in the genetics of hunter-gatherer societies. It is predicted that, far from refuting the above, populations with limited exposure to agriculture, and as a consequence sedentary settlements of high population density, should display recent reactive selection only in accordance with the magnitude of their exposure. Should this hypothesis hold, it would be both complementary to, and supportive of, the main argument here given.

References

Barnes, I., Duda, A., Pybus, O. G., & Thomas, M. G. (2011). ANCIENT URBANIZATION PREDICTS GENETIC RESISTANCE TO TUBERCULOSIS. Evolution, 65(3), 842-848.

Bullock, S., Manias, E., & Galbraith, A. (2006). Fundamentals of Pharmacology. Frenchs Forest: Pearson Australia.

Chiao, J. Y., & Blizinsky, K. D. (2009). Culture-gene coevolution of individualism-collectivism and the serotonin transporter gene. Proceedings of The Royal Society: Biological Sciences, 277, 529-537.

Diamond, J. (1991). Guns, Germs and Steel. London: Jonathan Cape.

Dietler, M. (2006). Alcohol: Anthropological/Archaeological Perspectives. Annual Review of Anthropology, 35, 229-249.

Enattah, N. S., Jensen, T. G. K., Nielsen, M., Lewinski, R., Kuokkanen, M., Rasinpera, H., et al. (2008). Independent Introduction of Two Lactase-Persistence Alleles into Human Populations Reflects Different History of Adaptation to Milk Culture. The American Journal of Human Genetics, 82, 57-72.

Feldman, M. W., & Cavalli-Sforza, L. L. (1976). Cultural and biological evolutionary processes, selection for a trait under complex transmission. Theoretical Population Biology, 9, 238-259.

Hawks, J., Wang, E. T., Cochran, G. M., Harpending, H. C., & Moyzis, R. K. (2007). Recent acceleration of human adaptive evolution. Proceedings of the National Academy of Sciences, 104(52), 20753-20758.

Laland, K. N. (2008). Exploring gene-cultural interactions: insights from handedness, sexual selection and niche-construction case studies. Philosophical Transactions of The Royal Society: Biological Sciences, 363, 3577-3589.

Laland, K. N., & Brown, G. R. (2011). Sense & Nonsense (2nd ed.). Oxford: Oxford.

Laland, K. N., & Hoppitt, W. (2003). Do animals have culture? Evolutionary Anthropology: Issues, News, and Reviews, 12(3), 150-159.

Laland, K. N., Odling-Smee, J., & Myles, S. (2010). How culture shaped the human genome: bring genetics and the human sciences together. Nature Reviews: Genetics, 11, 137-148.

Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R., & Gordon, J. I. (2008). Worlds within worlds: evolution of the vertebrate gut microbiota. [10.1038/nrmicro1978]. Nat Rev Micro, 6(10), 776-788.

Mansilla-Soto, J., Rivière, I., & Sadelain, M. (2011). Genetic strategies for the treatment of sickle cell anaemia. British Journal of Haematology, 154(6), 715-727.

Meisenberg, G. (2008). On the Time Scale of Human Evolution: Evidence for Recent Adaptive Evolution. Mankind Quarterly, 48(4), 407-444.

Peng, Y., Shi, H., Qi, X., Xiao, C., Zhong, H., Ma, R. Z., et al. (2010). The ADH1B Arg47His polymorphism in East Asian populations and expansion of rice domestication in history. BMC Evolutionary Biology, 10(15), 1-8.

Richerson, P. J., Boyd, R., & Bettinger, R. L. (2001). Was Agriculture Impossible During the Pleistocene but Mandatory During the Holocene? A Climate Change Hypothesis. American Antiquity, 66(3), 387-411.

Richerson, P. J., Boyd, R., & Henrich, J. (2010). Gene-culture coevolution in the age of genomics. Proceedings of the National Academy of Sciences, 107(Supplement 2), 8985-8992.

Smith, N., Hewinson, R., Kremer, K., Brosch, R., & Gordon, S. (2009). Myths and misconceptions: the origin and evolution of Mycobacterium tuberculosis. Microbiology, 7, 537-544.

Wang, E. T., Kodama, G., Baldi, P., & Moyzis, R. K. (2006). Global landscape of recent inferred Darwinian selection for Homo sapiens. Proceedings of the National Academy of Sciences of the United States of America, 103(1), 135-140.

Zink, A. R., Sola, C., Reichl, U., Grabner, W., Rastogi, N., Wolf, H., et al. (2003). Characterizatio of Mycobacterium tuberculosis Complex DNAs from Egyptian Mummies by Spoligotyping. Journal of Clinical Microbiology, 41(1), 359-367.

Appendix 1.

A cross between two parents heterozygous for the HbS gene will result, statistically in: 25% homozygous HbS (potentially lethal), 50% heterozygous HbS (protection against malaria) and 25% homozygous non-HbS (no malaria protection, under high disease burden potentially deadly). Similarly, a cross between a non-HbS homozygote and a heterozygote will produce 50% heterozygote offspring but with the other 50% being non-HbS homozygotes. A cross involving a HbS homozygote is less likely due to the deleterious nature of this genotype.

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~ by confusedious on November 2, 2011.

One Response to “Is Gene-Culture Coevolution at the Reins of Recent, Rapid Human Evolution?”

  1. […] Confusedious has highlight the varied genetic changes in recent populations of Homo sapiens.  His excellent post on gene culture coevolution is a detailed and elegant essay detailing rapid and modern genetic changes in H. sapiens regarding […]

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