Culture-Gene Interactions in Human Origins

Friday, April 13, 2012


What constitutes the essential behavior of our species is contentious. Evolutionary scenarios leading to both the capacity for and practice of these essential behaviors are even more debated. Genetics, cognitive and evolutionary psychology, morphology, reconstructions of climate variation, and the archaeology of human behavior all provide pathways to explore these questions. Furthermore, the newly published genomic studies of our extinct sister species, Neandertals and Denisovans, together with the archaeology, morphology and paleogeography of the former, provide a comparative framework for understanding the antiquity of some of these unique aspects of our species behavior, as well as the conditions under which these behaviors were favored. While we can document increasing cultural complexity in Africa after 100,000 years ago, leading ultimately to an out-of-Africa migration that largely overwhelmed the existing archaic species of Eurasia, was this due to a sudden genetic mutation or was it the ratcheting up of an earlier trajectory towards greater behavioral and emergent cultural complexity? When and where can we document in archaeology the existence of an ability to build innovation on the framework of earlier inventions, which must underlie the cultural trajectory documented in the last 100,000 years? Two of the biggest mysteries are the evolution of large brain size in the Middle Pleistocene and the behavioral innovation of spoken language. Is one of these related to the other? This presentation will review the evidence for the accumulation of distinctive human behaviors in a comparative framework.

As our australopithecine ancestors moved out of receding rain forests and into drier habitats, they abandoned a primarily fruit-based diet and began consuming more meat and tubers.  This increase in consumption protein, fat, and starch coincided in time with important evolutionary changes in cognition and brain size.  Genetic and genomic methods are providing insights into the relationship between these two parallel sets of adaptations.  Several genes have now been identified that may have mediated a link between changes in diet and changes in behavior during human origins. 

In the classic nature-nurture dichotomy, nature has a stronger or weaker influence on nurture, but certainly nurture was supposed to have no impact on nature. Human culture is often taken to be a form of nurture. However, culture itself has evolutionary properties. In particular, culture generates novel environments that in turn select for novel genes. A few dramatic cases of this effect are well known and many more are suspected. The nature-nurture dichotomy is an impediment to clear thinking and should be abandoned!

In most individuals, the ability to digest lactose, the sugar present in milk, declines rapidly after weaning because of decreasing levels of the enzyme lactase in the small intestine. However, there are individuals who maintain the ability to digest milk into adulthood due to a genetic adaptation in populations that have a history of pastoralism. Here I will discuss our studies of the genetic basis of lactose tolerance in African pastoralist populations.  We have identified several mutations that arose independently in East African pastoralist populations.  We demonstrate a striking footprint of natural selection in the genomes of individuals with these mutations.  We show that the age of the mutations associated with lactose tolerance in Europeans and Africans is correlated with the archeological evidence for origins of cattle domestication.  Thus, the genetic adaption for lactose tolerance is an excellent example of gene-culture co-evolution.  

Indo-European languages are native to populations from Ireland to Afghanistan and India and, in historical times, to the Tarim Basin in China. This spread occurred within a few thousand years carried by people who were mostly horse pastoralists and who carried a mutant regulator of the lactase gene so that they could as adults digest milk sugar.  Individuals with such lactase persistence are able to extract 40% more calories from milk, while others usually ferment away the milk sugar lactose by making cheese or yogurt.  While superior technology of invaders can be adapted by indigenous people, such a biological advantage cannot be copied.

The history of human evolution and dispersal was associated with remarkable environmental challenges to those processes that maintain stable physiological conditions.  Indeed, environmental change over time and over space has been a major feature of human evolution. Though many adaptations undoubtedly occurred at the cultural and behavioral levels, the striking variation of human phenotypes suggests that adaptations also involved genetic changes.  Cultural changes, e.g. different modes of subsistence or diets, in turn created new selective pressures. We have developed approaches for test for the impact that selective pressures associated with specific environmental factors have had on the human genome. Using these approaches, we identify adaptations to selective pressures related to climate as well as diet and subsistence. Some of these beneficial alleles were selected in multiple continents while others represent continent-specific adaptations.  Interestingly, many alleles strongly correlated with climate variables also influence risk to diseases of the immune response. 

For many species, including humans, matings occur among a restricted pool of partners. In humans, restrictions on the choice of partners are culturally determined and frequently are the result of homophily, namely, contacts among individuals that are similar on some dimension. The dimension may itself be culturally transmitted, and its transmission may affect the transmission of other characters, which may be genetically determined, but have nothing to do with the dimension on which the mating choice is based. Socioeconomic choice of consanguineous marriage is an example; it has important consequences for genetic variation in many populations around the world.

A grandmother hypothesis links the evolution of human longevity to ecological changes that left ancestral youngsters unable to get enough food on their own. Help from grandmothers allowed mothers to bear their next baby sooner while setting novel social problems for both mothers and offspring. These connections link grandmothering not only to the evolution of our long lifespans, but also to other features of human life history, physiology, and behavior. Even if only some are correct, they make human postmenopausal longevity much less of a puzzle after all.

But how do we do it? Estrogen is crucial to the maintenance of many physiological systems aside from fertility. Yet ovarian estrogen secretion depends on menstrual cycling which ends at similar ages in all great apes including humans. Like most mammals, other primates display geriatric symptoms while still cycling and rarely survive their fertile years while women remain strong and healthy beyond menopause. The contrast points to non-ovarian sources of estrogen in somatic maintenance. A likely nominee is an adrenal androgen that circulates at a higher level in humans than any other hormone and is estimated to be the precursor for most of the estrogen in women’s peripheral tissues even before menopause. Chimpanzee levels of this steroid are much lower, consistent with the hypothesis that shifts in adrenal function are an important mechanism for slowed aging in our lineage. Comparisons with other apes also reveal intriguing puzzles about somatic maintenance in our closest living relatives.

Language is a hallmark of modern humans: only humans have language. Yet, while no human society lacks a language, individual languages exhibit wide variety.  In this, language differs greatly from bipedalism, the other hallmark of humans. We explore the question of whether there is a relation between the variety among languages and genetic variation, concentrating on the emergence of sign languages in societies with a high incidence of deafness due to genetic traits.  We show that the emergence of sign languages in such societies is also tied to a number of preexisting cultural factors.  This type of interaction, where genetics and culture, both separately and together, provide the foundation for a particular type of language, has not previously received attention.