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Gene-Culture Coevolutionary Theory

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Gene-Culture Coevolutionary Theory REVIEWS Gene-culture coevolutionarytheory Marc W. Feldman and Kevin N. Laland tone tools appear in the Gene-culture coevoiutionary theory is a geneticssJ0Jr. And more recently, archaeological record ap branch of theoretical population genetics these general methods have been proximately two and a half that models the transmission of genes applied to address specific cases S million years ago. The signifi- and cultural traits from one generation to in which there is an interaction cance of this observation is not the next, exploring how they interact. between a cultural trait and some simply that Homo habifis and later These models have been employed to genetic variation that influences hominid species had the guile to examine the adaptive advantages of its prevalence12-17. manufacture a lithic technology, learning and culture, to investigate the In a gene-culture model, indi- but also that these skills were forces of cultural change, to partition viduals must be described in terms transmitted from one generation the variance in complex human behavioral of both their genotype and their to the next. These simple artifacts and personality traits, and to address cultural trait, a combination known thus represent the earliest evi- specific cases in human evolution in as a ‘phenogenotype’. Thus, in dence for culture. In fact, compara- which there is an interaction between addition to the rules of mendelian tive evidence for social learning genes and culture. inheritance, transmission rules for in a variety of vertebrate species cultural traits must be described”. suggests that cultural trans- Typically, it is assumed that the mission almost certainly preceded Marc Feldman is at the Dept of Biological Sciences, probability of an individual adopt- Stanford University, Stanford, CA 94305, USA: Homo habilis by a considerable ing a trait depends on whether its Kevin Laland is at the Sub-Dept of Animal Behaviour, length of time. However, social parents have that trait (vertical University of Cambridge, Madingley, learning in animals is rarely stable Cambridge, UK CB3 8AA. transmission), but equivalent mod- enough to support traditions in els have been developed in which which information accumulates learning is from unrelated individ- from one generation to the next. uals (horizontal and oblique trans- The archaeological record documents the fact that for at mission), key individuals in the social group (indirect least the past two million years hominid species have reli- transmission), or the majority in the group (frequency- ably inherited two kinds of information, one encoded by dependent transmission)sJl. In all cases, in the place of a genes, the other by culture. How does dual inheritance system of recurrence equations that describe how allele or affect the evolutionary process? Gene-culture coevolution- genotype frequencies change over time, gene-culture mod- ary theory is designed to answer this question. els use an equivalent system for phenogenotype frequencies. Gene-culture coevolutionary theory is a branch of theo- The methods of gene-culture coevolutionary theory dif- retical population genetics, which, in addition to modeling fer from those of sociobiology, human behavioral ecology, the differential transmission of genes from one generation and evolutionary psychology in two important respects. to the next, incorporates cultural traits into the analysis. First, a population’s culture is not regarded as largely de- The two transmission systems cannot be treated indepen- pendent on either its genetic constitution or the prevailing dently, both because what an individual learns may depend pattern of ecological resources. Instead, consistent with the on its genotype, and also because the selection acting on predominant view in the human sciences, culture is treated the genetic system may be generated or modified by the as shared ideational phenomena (ideas, beliefs, values, spread of a cultural trait. To give a simple example, the fre- knowledge) that are learned and socially transmitted be- quency of the sickle cell mutant among populations in West tween individuals. Below, we illustrate through examples Africa depends on their means of subsistencelJ. Populations how this view of culture makes a considerable difference to that chop down trees to cultivate yams create the conditions the evolutionary dynamics of a gene-culture system. Sec- where heavy rainfall will leave pools of standing water in ond, although the framework of gene-culture coevolution- which mosquitoes thrive, leading to more intense selection. ary theory does not preclude an adaptationist perspective, For yam cultivators, there is a correlation between amount and several such models have incorporated the assumption of standing water and sickle cell frequency, but not for other- that an individual’s genotype influences the probability that wise identical populations. In this example, the intensity of a particular cultural trait will be adopted, practitioners are selection on a gene hangs critically on the frequency of a also free to assume that traits may be adopted independent cultural trait (yam farming) in the population. of their fitness consequences. The gene-culture approach is minimalist in that assumptions about the adaptive impor- Gene-culture models tance of traits are not an obligatory step in the modeling The quantitative study of gene-culture coevolution be- exercise. Note that although Lumsden and Wilson’s labeled gan in 1973, when Cavalli-Sforza and Feldman introduced their theoretical work ‘gene-culture coevolution’, their ap- a simple dynamic model of cultural transmission into the proach is in the sociobiological tradition, and should not be nature-nurture debates. The emerging body of theory has confused with contemporary gene-culture coevolutionary been used in a variety of ways. One class of models is em- theory. ployed to partition the variance in behavioral and personality Mathematical analyses suggest that evolution in popu- traits into a variety of components including a transmitted lations with a dynamic, socially transmitted culture is dif- cultural components-s. Dynamic models address very gen- ferent from evolution in acultural populations for a number eral questions about the adaptive advantages of complex of reasons. First, cultural transmission can modify selection forms of phenotypic plasticity, such as learning and pressures, thereby affecting the course of a population’s culture&g. Other general models explore the forces of cul- evolution. For example, below we describe how the cultural tural change, and the nature of their interaction with tradition of dairy farming may have created the selective TREE uol. II, no. II November I996 0 1996, Elsevier Science Ltd Pll: SOl69-5347(96)10052-5 453 REVIEWS climate in which genes for lactose absorption have been related variability in its incidence. There is a broad range of favored. Second, culture can generate new evolutionary conditions under which the absorption allele does not mechanisms; for instance, Boyd and Richerson8J4JsJ9 have spread despite a significant fitness advantage. Cultural pro- developed a series of models of human cooperation, which cesses complicate the selection process to the extent that demonstrate the feasibility of a culturally preserved process the outcome may differ from that expected under purely gen- of group selection. Third, the interplay between genetic and etic transmission. Here, because of interactions between cultural transmission may produce time lags in the action of genes and culturally influenced behaviors, the response to any selection that may be operating on a traitlo; the equiva- selection is typically slowed down, lent phenomenon has been seen in recent treatments of ma- ternal transmission of quantitative biological traitGO.Fourth, Excess female mortality in the same way that there can be non-linear interactions That the nature of a genetic response to selection may de between genes (linkage disequilibrium), nonrandom asso- pend on the characteristics of cultural transmission is illus- ciations between genes and cultural traits can occur*Q* that trated even more clearly in a gene-culture coevolutionary can significantly affect the genetic response to selection. analysis of the evolutionary and demographic consequences Fifth, because of its strong, homogenizing influence on of excess female mortality. In many regions of the world behavior, and capacity for rapid diffusion, culture may some (China, India, Pakistan), parents exhibit a preference for sons times generate atypically strong selection pressures, leading over daughters and act on this bias to change the natural to very strong selection. Examples of these last two phenom- sex ratio among their offspring27.28.Such behavior includes ena are given in the sex-ratio case discussed below. direct female infanticide, the neglect and abandonment of daughters, differential allocation of resources toward sons, lactose absorption and female-biased abortion following sex determination by The evolution of lactose absorption represents a good amniocentesis or ultrasound. The aggregate effect of these example of gene-culture coevolution. Systematic variation activities over vast continents may generate significant dis- exists in the milk digestive physiology of adult humans. In tortion of the adult sex ratio. For instance, in India, the adult fact, most adult humans are lactose malabsorbers: that is, sex ratio has shown a consistent trend toward increasing their level of enzyme (lactase)
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