BEHAVIORAL AND BRAIN SCIENCES (1994) 17, 585-654 Printed in the United States of America Reintroducing group selection to the human behavioral sciences David Sloan Wilson Department of Biological Sciences, State University of New York at Binghamton, Binghamton, NY 13902-6000 Electronic mail: [email protected] Elliott Sober Department of Philosophy, University of Wisconsin, Madison, Wl 53706 Electronic mall: [email protected] Abstract: In both biology and the human sciences, social groups are sometimes treated as adaptive units whose organization cannot be reduced to individual interactions. This group-level view is opposed by a more individualistic one that treats social organization as a byproduct of self-interest. According to biologists, group-level adaptations can evolve only by a process of natural selection at the group level. Most biologists rejected group selection as an important evolutionary force during the 1960s and 1970s but a positive literature began to grow during the 1970s and is rapidly expanding today. We review this recent literature and its implications for human evolutionary biology. We show that the rejection of group selection was based on a misplaced emphasis on genes as "replicators" which is in fact irrelevant to the question of whether groups can be like individuals in their functional organization. The fundamental question is whether social groups and other higher-level entities can be "vehicles" of selection. When this elementary fact is recognized, group selection emerges as an important force in nature and what seem to be competing theories, such as kin selection and reciprocity, reappear as special cases of group selection. The result is a unified theory of natural selection that operates on a nested hierarchy of units. The vehicle-based theory makes it clear that group selection is an important force to consider in human evolution. Humans can facultatively span the full range from self-interested individuals to "organs" of group-level "organisms." Human behavior not only reflects the balance between levels of selection but it can also alter the balance through the construction of social structures that have the effect of reducing fitness differences within groups, concentrating natural selection (and functional organization) at the group level. These social structures and the cognitive abilities that produce them allow group selection to be important even among large groups of unrelated individuals. Keywords: altruism; group selection; human evolution; levels of selection; sociobiology The existence of egoistic forces in animal life has long been recognized. It is not so well known that the idea of group-centered forces in animal life also has a respectable history. (Allee 1943, p. 519) It is a crude oversimplification to conceive of social motives as being capable of direct derivation from a hedonic algebra of self- interest - real or fictitious - based on a few universal human drives, whatever the choice of the drives may be. (Tajfel 1981, p. 36) These quotations illustrate a perspective in which social groups have a primacy that cannot be reduced to individ- ual interactions. This group-level perspective can be found in biology and all branches of the human behavioral sciences (e.g., anthropology, economics, psychology, so- ciology). It is opposed by another perspective that treats individuals as primary and social groups as mere conse- quences of individual interactions. Although the conflict between the two perspectives is often dismissed as se- mantic, it refuses to go away, suggesting that substantive issues are involved. In biology, the conflict between the two perspectives has had a remarkable history. Prior to 1960, it was quite acceptable to think of social groups and even whole ecosystems as highly adapted units, similar to individuals in the harmony and coordination of their parts. 1 Williams (1966) and others argued that group-level adaptations require a process of natural selection at the group level and that this process, though theoretically possible, is unlikely to be important in nature. Their verdict quickly became the majority view and was celebrated as a major scientific advance, similar to the rejection of Lamarkian- ism. A- generation of graduate students learned about group selection as an example of how not to think and it became almost mandatory for the authors of journal arti- cles to assure their readers that group selection was not being invoked. Nevertheless, a positive literature began to grow in the '70s and is rapidly expanding today (Table I). 2 It is no longer heretical for biologists to think of © 1994 Cambridge University Press 0140-525X194 $5.00+.00 585