BEHAVIORAL AND BRAIN SCIENCES (1994) 17, 585-654Printed in the United States of America

Reintroducing group selection to the human behavioral sciencesDavid Sloan WilsonDepartment of Biological Sciences, State University of New York at Binghamton, Binghamton, NY 13902-6000 Electronic mail: dwilson@bingvaxa.bitnet

Elliott SoberDepartment of Philosophy, University of Wisconsin, Madison, Wl 53706 Electronic mall: esober@vms.macc.wisc.edu

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 selfinterest - 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 individual interactions. This group-level perspective can be found in biology and all branches of the human behavioral sciences (e.g., anthropology, economics, psychology, sociology). It is opposed by another perspective that treats individuals as primary and social groups as mere consequences of individual interactions. Although the conflict 1994 Cambridge University Press 0140-525X194 $5.00+.00

between the two perspectives is often dismissed as semantic, 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 Lamarkianism. 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 articles 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 585

Wilson & Sober: Group selectionTable 1. A guide to the biological literature on group selection since 1970. T = theoretical models (both mathematical and verbal), E = possible empirical examples (including examples not verified by experiments), F = field experiments, L = laboratory experiments, R = literature reviews, P = philosophical treatments, C = criticisms of group selection interpretations, and H = papers that are especially relevant from the standpoint of human evolutionary biology. (Theoretical; Empirical; Field; Laboratories; Reviews; Philosophical; Critiques; Human). Table 1. (Continued)

CITATION Crozier and Consul 1976 Damuth 1985 Damuth and Heisler 1988 Dugatkin 1990 Dugatkin and Reeve 1994 Dugatkin et al 1992 Eberhard 1990 Eibl-Eibesfeldt 1982 Eshel 1972 Eshel 1977

T E F L R pX X X X X X X X X ! X X X

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CITATION Alexander and Borgia 1978 Aoki 1982 Aoki 1983 Aviles 1986 Aviles 1993 Bell 1978 Boehm 1981 Boorman and Levitt 1973 Boorman and Levitt 1980 Boyd and Richerson 1980 Boyd and Richerson 1982 Boyd and Richerson 1985 Boyd and Richerson 1988 Boyd and Richerson 1989 Boyd and Richerson 1990a Boyd and Richerson 1990b Brandon 1990 Breden and Wade 1989 Buss 1987 Camazine and Sneyd 1991 Campbell 1979 Campbell 1983 Campbell 1991 Campbell 1993 Cassidy 1978 Cavalli-Sforza and Feldman 1978 Chao and Levin 1981 Charlesworth 1979 Charlesworth and Toro 1982 Chepko-Sade, Dow, and Cheverud 1988 Cohen and Eshel 1976 Colwell 1981 Craig 1982 Crespi and Taylor 1990 Crow and Aoki 1982 Crow and Aoki 1984 Crozier 1987

T E F L R pX X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X

cHX

X X X X X X X X X1i

Eshel and Montro 1988 Ewald 1993 Fagan 1980X

X

X X X X X X X X X X X X X X X X X X X X X X X X X X X X

Findlay 1992 Fix 1985 Frank, S. A. 1986a Frank, S. A. 1986b

X X X X X X

Frank, S. A. 1987 Gadgil 1975 Garcia and Toro 1990 Gilinsky and Mayo 1987 Gilpin 1975 Gilpin and Taylor 1988 Goodnight 1985 Goodnight 1990a Goodnight 1990b Goodnight 1991

X X X X

Goodnight, Schwartz, and Stevens 1992 Goodnight, K. 1992 Gould 1980 Govindaraju 1988 Grafen 1984 Griesmer and Wade 1988 Griffing 1977 Harpending and Rogers 1987

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