Philosophy and Phenomenological Research Vol. LXV, No. 3, November 2002

Group Selection, Pluralism, and the Evolution of Altruism

MAlTHEW BARRETT AND PETER GODFREY-SMITH

Stanford University

Sober and Wilson have done evolutionary biologists and philosophers of biology a great service in writing this book. They vigorously defend a “multi-level” view of natural selection, in which group selection can play a significant role, and argue that group selection was involved in the evolution of altruistic behavior in humans. The book is entirely persuasive in its argu- ment that attempts to marginalize group-selectionist ideas in the latter part of the 20th century were mistaken. Sober and Wilson also apply their multi- level evolutionary framework to the question of whether the psychological mechanisms underlying human behavior are wholly egoistic or in part genu- inely altruistic. In this review we focus on Sober and Wilson’s treatment of the “units of selection” question, and the relation between this issue and the evolution of altruism. So we leave untouched their applications of group selection to human evolution and psychology.

Varieties of Pluralism Sober and Wilson make much of their “pluralism” about the units acted on by natural selection. This is a term with a complex history in the units of selection debates. In what sense is Sober and Wilson’s position pluralist?

One version of pluralism was defended in a well-known paper by Sterelny and Kitcher (1988). In this sense, pluralism is the view that any given selec- tive process can be described at a variety of different levels in the biological hierarchy (genes, organisms, groups, etc.). On Sterelny and Kitcher’s view, one can explain giraffe necks in terms of competition among longer-necked and shorter-necked giraffes (along with a heritability assumption), and one can also explain them in terms of competition among the genes that lead to these differences in neck size. Although these descriptions might have diffehent heuristic virtues, neither description has a special explanatory status that the other lacks.

Sober (1990) rejected this view, arguing instead for a position that Sterelny and Kitcher call “hierarchical monism.” Hierarchical monism makes

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two claims. The first is the claim that there are several different, hierarchi- cally organized, levels of selection in natural systems. The second is the claim that any particular process is best described in terms of some determi- nate combination of forces operating at different levels. It is this second claim that distinguishes hierarchical monism from pluralism in the sense of Sterelny and Kitcher. Hierarchical monism says there is one best description of a given selective episode, which accurately represents its causal structure. The alternative descriptions of that episode endorsed by a pluralist fail to represent that causal structure, and are therefore at best only predictively

The early chapters of Unto Others suggest a change of heart on Sober’s part. Sober and Wilson call their view pluralist, and say repeatedly that there are “insights” available from models of the evolution of altruism that repre- sent selection only at the genic, or organismal, level.

There is, however, potential for confusion here. These expressions of support for “pluralism” in Unto Others come with qualifications, and often sit alongside claims that express hierarchical monism instead. Although a genic or organismal model may offer “insights,” Sober and Wilson are adamant that only a group selectionist description can do justice to the causal structure of many selective processes (pp. 33, 54, 99). Altruism, in particular, is the result of an evolutionary conflict between group-level selec- tion for altruism and individual-level selection against it. The trajectory of the population is determined by the “sum” of these two opposing forces.

Hence, the evolution of altruism can only be properly understood via “multi-level selection theory,” which models the simultaneous operation of selective forces at different levels of the hierarchy. Exclusively individualist models can predict the frequencies of altruist and non-altruist individuals that selection will produce, but fail to accurately represent the causes of these outcomes.

Some clarification of Sober and Wilson’s position on pluralism is offered at the very end of the book. There Sober and Wilson say that they endorse two forms of “pluralism”: pluralism of perspectives, and pluralism about the actual causes of evolution. Pluralism about causes, in their sense, is the idea that “there exists a plurality of causes of evolutionary change, which can and do occur in different combinations” (p. 331). We take this to express hierar- chical monism: the causal basis of a particular selective episode is some determinate combination from among a range of causes of evolutionary change.

What is pluralism of perspectives? This is the claim that ‘There is noth- ing wrong with representing the same process in different ways, provided that diflerences in mode of presentation are not confused with diferences in substantive claims about nature” (p. 331, emphasis added). The second,

adequate.

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emphasized clause here amounts to a denial of pluralism in Sterelny and Kitcher’s (1988) sense. One description of an evolutionary process gets its causal structure right. Alternative descriptions are acceptable, but only on the understanding that they do not contest causal issues.

But as we noted earlier, Sober and Wilson say there are “insights” avail- able via other descriptions. What sorts of insights can these be? We interpret Sober and Wilson to claim that other perspectives can sometimes have heuristic value even when they are inadequate as descriptions of causal struc- ture. An alternative description can suggest a novel angle on a problem or a system, highlighting factors that might be hard to discern from other points of view.

Ultimately then, the position defended in Unto Others is a special version of hierarchical monism. Pluralism of perspectives is endorsed with respect to predictive and heuristic tasks, but not with respect to causal description, or to explanatory tasks more generally. Pluralism of the kind found in Sterelny and Kitcher (1988), Dugatkin and Reeve (1994), and Sterelny (1996) involves a stronger kind of “pluralism of perspectives,” in which a plurality of causal descriptions are recognized as legitimate as well.

So far this is not to criticize Unto Others, only to locate it in the land- scape of options. However, a criticism can be mounted at this point. Sober and Wilson’s hierarchical monism sits badly with their very liberal concep- tion of what counts as a group, and what counts as group selection.

Locating Group Selection

Sober and Wilson’s view is that there is group structure wherever indi- viduals affect each other’s fitness. Groups are sets of individuals that affect each other with respect to the fitness of some trait (p. 92).

This is a very liberal conception of biological groups. It is also a different conception from that suggested by Sober and Wilson’s most persuasive examples. Those examples involve cases where lower-level entities are combined into complex, higher-level systems. In those cases the recognition of higher-level entities is often irresistible. Indeed, individual organisms are themselves “just” collections of mostly-cooperating lower-level biological units. If we countenance selection at the level of the “super-cell “ (individual), we should also countenance selection at the level of the super-organism (group), with the social insects as star examples.

Groups of cooperating cells making up a body, and groups of cooperating social insects, have definite features that support the identification of a higher level of organization. Most individual members of these groups lack inde- pendent, long-term reproductive futures. In these cases there are also coopera- tion-enforcing mechanisms, and the groups have tight functional integration and fairly clear boundaries in space and time.

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In contrast, the view of Unto Others is that a group is simply any set of organisms that affect each other with respect to fitness. So two people in a Prisoner’s Dilemma scenario count as a group. Any kin selection model is ips0 fact0 a group selection model.

In his review of Unto Others, John Maynard Smith (1998) found this last consequence objectionable. We agree. Sober and Wilson’s hierarchical monism, and their ultra-liberal conception of groups, are a bad match. Ultra- liberalism means that group-selectionist explanations are almost always available-wherever inter-organismal interactions affect fitness. Hierarchical monism means that where they are available, they are mandatory in causal explanation. As a consequence, too much counts as group selection. Causal description of evolution in individualist terms ends as soon as interaction between individuals begins.

We stress that the problem here arises from the combination of ultra-liber- alism about groups and hierarchical monism. The problem does not arise-or arises far more benignly-for those who combine a liberal conception of groups with a stronger form of pluralism, as they do not preclude an alterna- tive description in individualist terms. But further, we hold that a properly formulated pluralism about group selection has advantages over hierarchical monism of any kind. The particular version of pluralism we endorse is that developed in Kerr and Godfrey-Smith (forthcoming), which is a modification of earlier views (especially Sterelny (1996) and Dugatkin and Reeve (1994)). Kerr and Godfrey-Smith argue for the utility of a “gestalt-switching’’ plurality of perspectives on many cases that Sober and Wilson would insist be under- stood as group selection. When we study evolution in structured populations, we can treat groups as higher-level whole units which can be assigned fitness values, or we can assign fitnesses only to individuals but do so in a way that is sensitive to the social environments in which individuals find themselves. (This kind of individualist model does not give special status to the “aver- aged” individual fitnesses that Sober and Wilson discuss critically in Unto Others.) The two modeling approaches are mathematically interchangeable, and neither involves any distortion of causal structure. So which is better? The “gestalt-switching” form of pluralism defended by Kerr and m y - Smith holds that we do best to retain the ability to switch between both these perspectives on evolution in structured populations. Each perspective makes some facts vivid while obscuring others. (We should also note that Sterelny (1996) withdraws his pluralist attitude when dealing with groups that have very high degree of integration, while Ken and Godfrey-Smith do not.)

Unifying the Explanation of Altruism Why do Sober and Wilson develop such an inclusive, ultra-liberal concept of group selection, given the authors’ sensitivity to problems arising from

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earlier attempts to “define away” phenomena? It appears that Sober and Wilson see group selection as the way forward to a properly uni$ed account of the evolution of altruism. The group-selection process is what underlies all the various forms of kin selection, reciprocity, and selection on spatially separated demes, that can generate altruism (p. 99). We suggest that a better way to unify our understanding of the evolution of altruism is available, and this alternative is found in some earlier work by Sober himself.

Sober (1992) argued for a view that differs from his later work with Wilson. There he argued that the key to the evolution of altruism is correla- tion. If altruist behaviors are more likely to encounter altruist behaviors than are non-altruist behaviors, altruism has a chance of being selected for. A divi- sion of the population into groups which differ in composition is one mechanism that can generate correlations of the right kind. But there are others. Some of these other mechanisms do not require a clustering of the organisms themselves. For what is required is correlated behavior, and this can be produced even in cases where the distribution of organisms is unstruc- tured. The tit-for-tat strategy is a mechanism that generates correlation between behaviors even where the meetings between individuals are random. Sober (1992) drew the moral that “the evolution of altruism depends on the costs and benefits of the behaviors considered and on the degree of correlation that obtains among interacting individuals. This is the fundamental criterion that kin selection, reciprocal altruism, and group selection must satisfy” (p. 185).

So Sober’s older view took correlation at the level of behavior to be the key to the general problem of the evolution of altruism. The structuring of a population into groups is seen as one mechanism.for the generation and maintenance of correlation. We suggest that this earlier position is superior to the view developed in Unto Others, with respect to giving a unified thee retical account of the evolution of altruism (though Sober’s 1992 paper is not even cited in the book). In Unto Others, all the various mechanisms that can produce the right kind of correlation to generate altruism are lumped together as cases of group selection. It seems that Sober and Wilson think that this is the only, or the best, way to give a unified account of how the evolution of altruism works. But Sober’s 1992 paper shows us another way, a way that does not require the shoe-homing of too many disparate cases into the c a b gory of group selection.

Consider again the relation between kin selection and group selection. Some, but not all, kin selection models are usefully understood as instances of group selection. Models in which altruistic acts are performed in a group consisting entirely of siblings are profitably viewed as being group-selection- ist, and Sober and Wilson note that there is a history of modeling kin selec- tion in this way. Sober and Wilson keep models like these in the reader’s

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mind while arguing that all cases of kin-selection are cases of group selec- tion. But other kin-selection models have a different structure. “Chen-beard” models, for instance, assume that kin are scattered in a population that includes many non-kin, but behave differently when they meet kin. So Maynard Smith was right to complain that kin selection is not always a case of group selection. Nor is selection for reciprocal altruism of the sort seen in the success of the tit-for-tat strategy in the Iterated Prisoner’s Dilemma. The success of tit-for-tat does not (above a threshold tit-for-tat hquency) require non-random encounters between individuals. Is there something that unifies our understanding of the success of below-threshold tit-for-tat, above-thresh- old tit-for-tat, kin selection of various kinds, and the paradigm cases of group selection? Sober’s 1992 suggestion was basically right: costs, benefits, and correlation between behaviors. (Some definitions of “altruism” do not even require a positive correlation between behaviors for altruism to evolve; these cases are discussed in Kerr and Godfrey-Smith (forthcoming).)

If group structure is seen as one way to generate correlations of the rele- vant kind, this raises again the question: what is a group? Which cases are the real cases of group selection? In reply to this question we note first that the view that correlation is central here is compatible with the kind of pluralism endorsed earlier in this review. There is no need to lay down a hard-and-fast borderline between cases where we must recognize a real group bearing its own fitness value, and cases where an individual’s social relations comprise part of the individual’s environment. Both modes of description will often be useful. Having said that, it remains true that some groups (cells in an organ- ism, ant colonies) have special properties of integration, cohesion, and suppression of intra-group competition. These are the cases that serve Sober and Wilson’s argument in Unto Others so well, and also induce Sterelny to withdraw his pluralism. Though the cases do not warrant that response, they are indeed special. But we suggest that it is unclear whether we should be looking for a single criterion to demarcate these cases from the others. Perhaps there is a cluster of important properties and distinctions to consider here.

Concluding Remarks

We first distinguished the “pluralism” of Unto Others from stronger versions of pluralism endorsed by other authors. The position of Unto Others is really a special kind of hierarchical monism, as it insists on the use of group-selec- tionist ideas when our aim is to answer causal and explanatory questions, especially concerning the evolution of altruism. We then argued that hierar- chical monism fits badly with Sober and Wilson’s ultra-liberal conception of what counts as a group, and what counts as group selection. We endorsed a

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modified version of the form of pluralism familiar from earlier stages in the units of selection debate.

We then argued that if our aim is to give a unified account of how altru- ism can evolve, Sober’s 1992 suggestion is superior to the view proposed in Unto Others. The key to the natural selection of altruism is cost, benefit, and correlation at the level of behaviors. Group structure is one way among several to generate the relevant hnd of correlations. At the very end we C O M C Z ~ ~ ~ this idea back to our preferred form of pluralism. Despite these many disagreements with the specific proposals in Unto Others, we close by expressing once again our high regard for this lucid and adventurous book.

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Acknowledgment: We thank Ben Kerr, Ken Reisman, and Michael Weisberg for helpful discussions of these issues.

References Dugatkin, L. A. and H. K. Reeve (1994). “Behavioral Ecology and Levels of

Selection: Dissolving the Group Selection Controversy.” Advances in the Study of Behavior 23: 101-33.

Kerr, B. and P. Godfrey-Smith (forthcoming). “On the Relations Between Individualist and Multi-Level Models of Selection in Structured Popula- tions.’’ To appear in Biology and Philosophy.

Maynard Smith, J. (1998). “The Origin of Altruism.” Nature 393: 639-640. Sober, E. (1990). “The Poverty of Pluralism: A Reply to Sterelny d

Kitcher.” Journal of Philosophy 87: 15 1-8. Sober, E. (1992). ‘The Evolution of Altruism: Correlation, Cost and Bene-

fit.” Biology and Philosophy 7 : 177-88. Sober, E. and D. S. Wilson (1998). Unto Others: The Evolution and Psy-

chology of Unselfish Behavior. Cambridge MA: Harvard University Press.

Sterelny, K. (1996). “The Return of the Group.” Philosophy of Science 63:

Sterelny, K. and P. S. Kitcher (1988) ‘The Return of the Gene.” Jounzal of 5 62- 84.

Philosophy 85: 339-60.

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