BEHAVIORAL AND BRAIN SCIENCES (2000) 23, 131–175 Printed in the United States of America Niche construction, biological evolution, and cultural change Kevin N. Laland Sub-Department of Animal Behaviour, University of Cambridge, Madingley, Cambridge CB3 8AA, United Kingdom [email protected] www.zoo.cam.ac.uk/zoostaff/laland/index.html John Odling-Smee Institute of Biological Anthropology, University of Oxford, Oxford OX2 6QS, United Kingdom [email protected] www.admin.ox.ac.uk/oxro/ad.htm Marcus W. Feldman Department of Biological Sciences, Stanford University, Stanford, CA 94305-5020 [email protected] www.stanford.edu/dept/biology Abstract: We propose a conceptual model that maps the causal pathways relating biological evolution to cultural change. It builds on conventional evolutionary theory by placing emphasis on the capacity of organisms to modify sources of natural selection in their envi- ronment (niche construction) and by broadening the evolutionary dynamic to incorporate ontogenetic and cultural processes. In this model, phenotypes have a much more active role in evolution than generally conceived. This sheds light on hominid evolution, on the evolution of culture, and on altruism and cooperation. Culture amplifies the capacity of human beings to modify sources of natural selection in their environments to the point where that capacity raises some new questions about the processes of human adaptation. Keywords: adaptation; altruism; cooperation; evolutionary psychology; gene-culture coevolution; human evolution; human genetics; niche construction; sociobiology 1. An evolutionary framework have provoked strong opposition, and the relevance of bio- for the human sciences logical evolution to the human sciences remains widely dis- puted. The relationship between genetic evolution and culture Less familiar, but equally deserving of attention, are em- raises two causal issues. The first concerns the extent to pirical data and theoretical arguments suggesting that hu- which contemporary human cultures are constrained or di- man cultural activities have influenced human genetic evo- rected by our biological evolutionary heritage; the second lution by modifying sources of natural selection and altering concerns whether hominid genetic evolution has itself been genotype frequencies in some human populations (Bodmer influenced by cultural activities. We contend that these is- & Cavalli-Sforza 1976; Durham 1991; Feldman & Laland sues are inextricably tied: The significance of evolutionary 1996; Wilson 1985). Cultural traits, such as the use of tools, theory to the human sciences cannot be fully appreciated weapons, fire, cooking, symbols, language, and trade, may without a more complete understanding of how phenotypes have also played important roles in driving hominid evolu- in general, and human beings in particular, modify signifi- tion in general and the evolution of the human brain in par- cant sources of selection in their environments, thereby ticular (Aiello & Wheeler 1995; Byrne & Whiten 1988; codirecting subsequent biological evolution. Our principal Dunbar 1993; Holloway 1981). It is likely that some cultural goal is to delineate and explore the interactions between practices in contemporary human societies are still affect- biological evolution and cultural change. ing human genetic evolution. Evolutionary biology has been widely invoked to account Historically, evolutionary theory has suggested only two for human behaviour and social institutions. These expla- possible routes via which feedback from human cultural ac- nations have generated sociobiology (Trivers 1985; Wilson tivities could influence human genetic evolution. Human 1975), human behavioural ecology (Borgerhoff Mulder cultural activities may either directly change the genes that 1991), and evolutionary psychology (Barkow et al. 1992), as humans pass on to their descendants by generating muta- well as evolutionism and social Darwinism (Kuper 1988). tions, or they may change the probability of humans sur- However, evolutionary approaches to human behaviour viving and reproducing. The first alternative was ruled out © 2000 Cambridge University Press 0140-525X/00 $12.50 131 Laland et al.: Niche construction by the failure of Lamarkism. The so-called Weismann bar- of how human genetic evolution influences culture but also rier effectively stops genes from being affected by any of of how human culture can drive or codirect at least some the acquired characteristics of phenotypes, including the genetic changes in human populations (Boyd & Richerson culturally acquired characteristics of human beings (Mayr 1985; Cavalli-Sforza & Feldman 1981; Durham 1991; Feld- 1982). Modern molecular biologists do interfere with genes man & Laland 1996). These models include culturally bi- directly on the basis of their acquired scientific experiences, ased nonrandom mating systems (see, e.g., Aoki & Feldman but this innovation is too recent to have had any impact on 1997; Durham 1991; Laland 1994), the treatment of human human genetic evolution. The failure of this route therefore sociocultural or linguistic environments as sources of nat- left only the second alternative, which encouraged sociobi- ural selection (Aoki & Feldman 1987; Cavalli-Sforza & ology’s claim that phenotypes of all species, including our Feldman 1983), and the impact of different cultural activi- own, reduce to “survival machines” or “vehicles” for their ties on the transmission of certain diseases such as malaria genes (Dawkins 1989) and that the only role phenotypes and sickle-cell anaemia (Durham 1991). The common ele- play in evolution is to survive and reproduce differentially ment among these cases is that cultural processes change in response to natural selection and chance. This subordi- the human selective environment and thereby affect which nate status for phenotypes does not cut off human culture genotypes survive and reproduce. from human genetic evolution entirely, insofar as it still al- Culture works on the basis of various kinds of transmis- lows culture to contribute to human adaptations (Alexander sion systems (Boyd & Richerson 1985; Cavalli-Sforza & 1979) and hence to genotypic fitnesses. However, accord- Feldman 1981), which collectively provide humans with a ing to this perspective, culture has no power to codirect second, nongenetic “knowledge-carrying” inheritance sys- human genetic evolution through active modification or tem. If the cultural inheritance of an environment-modify- creation of selection pressures. ing human activity persists for enough generations to gen- Other evolutionary biologists maintain that culture fre- erate a stable selection pressure, it will be able to codirect quently does affect the evolutionary process, and some have human genetic evolution. The culturally inherited tradi- begun to develop mathematical and conceptual models of tions of pastoralism provide a case in point. Apparently, the gene-culture coevolution that involve descriptions not only persistent domestication of cattle, and the associated dairy- ing activities, did alter the selective environments of some human populations for sufficient generations to select for Kevin Laland is a Royal Society University Research genes that today confer greater adult lactose tolerance Fellow at the Sub-Department of Animal Behaviour, (Durham, 1991; Feldman & Cavalli-Sforza 1989). University of Cambridge. Born in 1962, he was edu- This approach is explicitly species specific. Although cated in Psychology at the University of Southampton other species of animals have their “protocultures” (Galef (BSC) and University College London (PhD), before 1988), it has generally been assumed that Homo sapiens is being awarded a fellowship from the Human Frontier the only extant species with cultural transmission stable Science Program to join the Biology Department at the enough to codirect genetic evolution (Boyd & Richerson University of California, Berkeley, USA, followed by a 1985). If this is the case, “culture” can be used to explain lit- BBSRC fellowship in the Zoology Department at Cam- tle in primate evolution that happened prior to the appear- bridge. He is the author of a substantial number of em- ance of powerful, accumulatory cultural inheritance. pirical and theoretical articles on animal social learning, niche construction, and cultural evolution. We think this particular human-centred perspective is misleading. Humans may be unique in their extraordinary John Odling-Smee is Scientific Associate in Biologi- capacity for culture, but they are not unique in their capac- cal Anthropology at Oxford University. After a misspent ity to modify natural selection pressures in their environ- youth and a late start, he studied psychology at Univer- ments. Many other species do the same, either on the basis sity College London, publishing empirical and theoret- of simple protocultural traditions or, most often, without ical papers, several in collaboration with Henry Plotkin, any help from culture at all (Jones et al. 1997; Lewontin on animal learning, culture and evolution, including an 1983; Odling-Smee et al. 1996). We suggest that a deeper earlier contribution to the Behavioral and Brain Sci- understanding of the relationship between genes and cul- ences (1981, 4: 225–268), and an initial article on niche ture can be derived from evolutionary theory by demon- construction in The Role of Behaviour in Evolution (1988, MIT Press). A Leverhulme Fellowship led to the