Unto Others: The Evolution and Psychology of Unselfish Behavior;

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Unto Others: The Evolution and Psychology of Unselfish Behavior; Elliott Sober and David Sloan Wilson, Harvard University Press, 1998, 394 pp. ISBN: 0674930460 Multi-Level Selection and Human Cooperation In Unto Others, Elliott Sober and David Sloan Wilson (henceforth, “SW”) make an impassioned plea for the importation of multi-level selection thinking into evolutionary analyses of social behavior, especially cooperation among humans. By “multi-level” selection models, they mean the “intra-demic,” “trait-group,” or “within population” group selection models that systematically partition an individual’s (really a specific trait’s) fitness into within-group and between-group components. (Evolutionary explanations of cooperation based on “good-of-the-species” arguments involve “between-population” or “inter-demic” selection and usually are rejected because natural selection, in all but a few special circumstances, operates much more speedily within breeding populations than between them—the latter models, which unfortunately share the label “group selection” with intra-demic models, are not the kind of group selection framework being advanced by SW). Importantly, in the first part of their book, SW make the case that the multi-level approach does not imply an evolutionary process that is different from those implied by inclusive fitness or gene-centered approaches. They state that “Inclusive fitness theory, evolutionary game theory, and selfish gene theory . . . are not regarded as competing theories that invoke different processes, such that one can be right and the others wrong. They are simply different ways of looking at the same world.” Likewise, “The theories that were launched as alternatives to group selection are merely different ways of looking at evolution in group structured populations” (p. 98). In the second part of their book, SW consider the possibility that group-selected altruism has left an imprint on the human brain, manifested as “psychological altruism,” i.e., naturally selected desire to help others in certain contexts. As has been pointed out repeatedly by several evolutionary biologists over the last two decades (and now by SW), the “new” group selection models, in which subgroups of the population, rather than individuals, can be seen as vehicles of selection, are not mathematically different from the broad-sense individual selection (e.g., inclusive fitness) models at all. Rather, the group selection models are generated from a fitness-accounting scheme that merely produces an alternative picture of the same selective processes described by the in-

Corresponding author: Hudson Kern Reeve, Section of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA. E-mail address: hkr1@cornell 1090-5138/00/$ – see front matter © 2000 Elsevier Science Inc. All rights reserved. PII: S1 0 9 0 - 5 1 3 8 ( 9 9 ) 0 0 0 2 0 -3

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clusive fitness models. The new group selection models can be translated readily into inclusive models, and vice versa. This “equivalence principle” is so important, and yet so simple, that the essential argument should be driven home yet again, especially because SW do not consistently follow its implications. Suppose we have a two-person group. Let s(x) be the offspring production of the focal member (“self”) as a function of its behavior x and p(x) be the offspring production of its partner, also as a function of the focal individual’s behavior x. According to Hamilton’s inclusive fitness theory (also popularly known as “kin selection theory”), selection will act on x so as to maximize the inclusive fitness quantity: rs s ( x ) + r p p ( x )

(1)

where rs is the focal individual’s relatedness to its own offspring, and rp is its relatedness to the partner’s offspring (this simple, additive version of Hamilton’s rule is easily generalized to cases where costs and benefits do not combine additively). When the partner and the focal individual are maximizing their inclusive fitnesses simultaneously, game-theoretic methods are invoked to solve for the evolutionarily stable values of x. The first term in Equation 1 is called the personal component of inclusive fitness, and the second term is called the kin component of inclusive fitness. A multi-level selection approach in effect further partitions the inclusive fitness as follows. The offspring production of the local member s(x) is decomposed into the fraction f(x) of the dyad’s total offspring that is produced by the focal member times the total group output k(x). Likewise, the partner’s offspring output is partitioned into its fraction of the group’s total offspring 1⫺ f(x) times the group output k(x). The new version of inclusive fitness becomes (Eq. 2): r s f ( x )k ( x ) + r p [ 1 – f ( x ) ]k ( x )

(2)

which can be rearranged as: k ( x ) [ r p + ( rs – r p ) f ( x ) ]

(3)

which is still mathematically equivalent to Equation 1. Now, multi-level selectionists note that Equation 3 is the product of k(x), which now is called the group fitness (the size of the total “pie” represented by the overall group output) and the quantity [rp ⫹ (rs⫺ rp)f(x)], which becomes known as the individual fitness of the focal individual (the fraction of the total pie containing the focal individual’s genes). Thus, inclusive fitness theorists divide overall fitness into “personal” versus “kin” components (Equation 1), whereas multi-level selectionists alternatively divide the same fitness into “group” versus “individual” components (Equation 3). Probably one reason that the inclusive fitness approach has been the more intuitively appealing among evolutionary biologists is that its two fitness components each refers to a cohesive object (the focal individual and its partner, respectively) whereas the two fitness components of multi-level selection theory do not! These two alternative fitness-partitioning schemes carry with them alternative definitions of altruism and adaptation. SW define altruism as resulting when the behavior x causes increases in the group output k(x) while decreasing the selfish fraction [rp ⫹ (rs⫺rp)f(x)]. To the extent that the behavior x maximizes the group output k(x) instead of the selfish fraction

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[rp ⫹ (rs ⫺ rp)f(x)], we have a group-level adaptation. One can get both altruism and a group-level adaptation without a positive relatedness rp between the focal individual and the partner. Suppose rp is zero (the focal individual is a non-relative of the partner). Then the multi-level selection version of Equation 3 becomes just: k ( x )r s f ( x ).

(4)

A behavior will still appear to maximize the group output k(x), even among non-relatives, if, for example, social reward and punishment mechanisms prevents the focal individual from using its behavior to increase its selfish share of the reproduction f(x) at the expense of group output [mathematically, f(x) in such a reward/punishment system no longer is an increasing function of x, instead becoming a constant or even a decreasing function of x]. Now, for inclusive fitness theorists, who use Expression 1, altruism is said to occur when a behavior decreases the personal fitness component in Expression 1 but increases the kin component in Equation 1. Note that this is very different from “altruism” as defined by multi-level selection theorists. In particular, for the latter, altruism between non-relatives can be favorably selected. For inclusive fitness theorists, however, altruism can be favorable selected only among relatives, as required by Equation 1, because an increased kin component can compensate for a decreased personal component only if r ⬎ 0. The inclusive fitness theorist and the multi-level selection theorist are not really disagreeing when they make these alternative claims, of course (they cannot disagree, because they must use the same over-all fitness construct)—the apparent disagreement arises only because they have defined altruism in different ways. That is essentially all there is to the mathematical relationship between inclusive fitness and multi-level selection models—they are essentially equivalent, their only differences being definitional. This may be surprising to some, considering the amount of ink that has been spilled on the group selection controversy. (To immunize against inevitable later confusion, I have required that my students master the rules of translation between the inclusive fitness and multi-level selection approaches.) Every multi-level selection model has a twin representation in an inclusive fitness model, and vice versa, regardless of what kind of phenotype, including behavior, is being modeled. SW give the clearest argument in favor of the equivalence principle that I have yet seen from the group selection literature (it has not been clearly stated by most on either side of the group selection controversy). However, following their announced adherence to this principle early in the book, they unfortunately lose sight of it again in subsequent discussions and make some crucial errors. Here is a sampling of instances. On page 116, in discussing why altruistic foraging specialists have evolved in foundress associations of a desert ant, SW conclude that kin selection has not operated because the foundresses are unrelated. The equivalence principle tells us that this must be wrong. The error made by SW is that they failed to remember that the foraging specialist’s relatedness to its own offspring is crucial to the evolution of the behavior, as revealed by the rs term in the multi-level selection version of overall fitness for the case of non-relatives (Equation 4). The evolution of cooperative interactions among non-relatives (e.g., “altruism” as defined by multi-level selection, but not inclusive fitness, theorists) is just a special case of inclusive fitness theory (rp ⫽ 0) and hinges just as critically on a relatedness value (rs) as does the evolu-

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tion of co-operative interactions among relatives. (Dawkins identified the failure to understand this as one of the “twelve misunderstandings of kin selection.”) Thus, the evolution of cooperation among ant foundresses can be understood just as well through inclusive fitness theory as through multi-level selection theory. This must be so, by SW’s own earlier arguments. Now it is true that the multi-level selection approach can shed new light on the structure of the selective forces that favor foraging specialization (i.e., the behavior decreases the forager’s selfish share of the group output pie but increases the total size of the pie by enhancing the worker force and thus its colony’s resistance to marauding foreign workers), but this explanation is not inherently superior to that provided by inclusive fitness theory (an individual that becomes a forager in a group of non-foragers increases its own future offspring production by increasing the worker force and thus its colony’s resistance to foreign workers). This and related errors are revisited throughout the book. On page 134, SW incorrectly assert that “genealogical relatedness is not required for group selection to be a strong evolutionary force.” Of course, they mean that a positive relatedness between group members is not required for group selection, but, as seen earlier, this is not the only genetic relatedness that counts in social evolution (rs must be ⬎ 0 for group selection to work). Moreover, inclusive fitness models, too, do not require a positive relatedness among group members to explain the evolution of the cooperation. Thus, the occurrence of the evolution of cooperation among non-relatives does not (and cannot) imply the correctness of one approach over the other. SW then go much further (p. 134) by arguing that kin selection theorists treat “genealogical relatedness as the only important variable in the evolution of group-level functional organization.” This is decidedly false, as can be seen from an inspection of Expression 1, which includes two relatedness terms and two individual output terms, the latter being sensitive to ecological factors. Indeed, the application of inclusive fitness theory to the evolution of animals groups and cooperation has a long tradition of examining the contributions of the ecologically determined individual output terms (when appropriately combined with the relatednesses) to the evolution of cooperation (see any edition of Krebs and Davies’ Behavioral Ecology: An Evolutionary Approach). One would hardly know from the treatment by SW that this huge literature exists. SW’s erroneous refusal to acknowledge that multi-level selection models themselves hinge critically on genetic relatedness (or an equivalent parameter), and their unfair caricature of inclusive fitness theory as “riveting” attention exclusively on genetic relatedness (see also p. 332), represent a total abandonment of the equivalence principle. This abandonment paves the way for their suggestion that multi-level selection theory actually ought to replace kin selection theory (p. 332), which they (by this time) see as constituting at best a special case of group selection theory. As I (and many others, cited in SW) have shown, this characterization of the logical relationship between the two theories is simply wrong: The most general inclusive fitness and multi-level selection models are exactly mathematically equivalent. To the extent that SW argue that the latter supersedes the former, inclusive fitness theorists will continue to recoil from the potentially useful multi-level selection approach. Thus, I fear that the carelessness in some of SW’s arguments ultimately will undermine one of the stated goals of their book. SW use other examples to undergird their claim that some phenomena demand multi-level selection analyses [e.g., cooperation facilitated by assortative interactions (p. 137) and com-

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munity selection for inter-species cooperation (p. 120)], but in each case the multi-level selection models have perfectly workable counterparts in inclusive fitness (⫽ broad-sense individual selection) theory, taking the form of partner-choice models of reciprocity or gametheoretic models of mutualism. On page 31, SW present a general argument that classical individual selection approaches cannot handle such cases (cases of multi-level “altruism” in particular) because such approaches commit the “averaging fallacy,” i.e., they average fitnesses of traits across groups, in the process losing the crucial information about the structure of the selective force that shapes behavior such as altruism. In other words, one cannot even meaningfully speak of altruism unless some kind of group structure is assumed by one’s model. In fact, the “averaging fallacy” is rarely committed by kin selection theorists. Inspection of the inclusive fitness expression (Expression 1) shows that kin selection theory, like multilevel selection theory, resolves fitness into two components, the personal component and the kin component, although these are not the same as the between-group and within-group fitness components of multi-level selection theory. Thus, inclusive fitness formulations do provide information about the structure of selection. For example, they show that a trait that lowers the personal component might still evolve if it sufficiently raises the kin component. Thus, inclusive fitness analyses are perfectly fine for understanding at least the sort of “altruism” recognized by inclusive fitness theorists, i.e., the possibility for altruism has not been discarded by some sort of averaging procedure. (The “averaging fallacy” would only apply to kin selection theory as represented by classical population-genetic or “neighbor-modulated” fitness, but hardly anyone uses these fitness constructs in theoretical discussions.) Thus, I view the discussion of the “averaging fallacy” as another aborted and misguided attempt to demonstrate the inherent theoretical superiority of multi-level selection models over inclusive fitness or broad-sense individual selection models. These considerations lead me to conclude that the first part of the book, in which SW first embrace the equivalence principle but then desert it, is completely logically orthogonal to the second part of the book in which multi-level selection theory is applied to the evolution of human cooperation. In my view, the evolution of cooperation in humans is as amenable to inclusive fitness analysis as to multi-level selection analysis, as it must be according to the equivalence principle. By inappropriately discarding inclusive fitness theory in the second half of the book, SW cut themselves off from the currently best-articulated mathematical theories of societal evolution, which brings me to my second major criticism of their book. In the second half of the book, SW attempt to sketch how human societies have come to exhibit such intricate forms of cooperation (⫽ group-level adaptations). They present no detailed theory of cooperation in human societies, but offer only the insight that altruism (which they call an example of a “primary” behavior) can evolve among unrelated humans with little difficulty once there are social mechanisms in place that reward some behaviors (such as group-cooperative behaviors) and/or punish others (such as individually selfish behaviors). The reward/punishment systems constitute “secondary” behaviors. SW are silent about what kinds of secondary behaviors will evolve in which kinds of ecological contexts, except to repeat Boyd’s intriguing suggestion that between-group selection might select among alternative culturally enforced normative systems (secondary behaviors) to favor groups whose normative systems happen to maximize group output. If the latter is true, one should be able to predict what kinds of normative systems will prevail in different kinds of

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ecological circumstances, regardless of whether these systems evolved by natural selection, cultural selection, or a mix of both. Instead of taking the latter approach, SW ignore the ecological context and predict that what appears (at first glance) to be a bewildering array of cultural systems may represent a fundamental indeterminacy in the evolution of cultural systems. Their argument is that secondary behaviors can favor almost any conceivable set of primary behaviors, and because secondary behaviors can be quite low cost, well, almost anything goes in the evolution of human social behavior. This leads SW to conclude that their multi-level approach ultimately has had the beneficial effect of bringing “nonfunctionalism” into the happy family of causal pluralism, which includes individual-level functionalism and group-level functionalism (p. 331). To many (including me), the conclusion that cultural evolution is largely indeterminate will seem astonishingly premature. Many also will question whether it is any laudable achievement at all that multi-level selection theory has already opened the door for the research-deadening effects of nonfunctionalism. Let us take the SW claims about the evolution of human social behavior one at a time. First of all (echoing the earlier points), it simply is not true that primary and secondary behaviors can be seen only as group selected, i.e., analyzed only with the multi-level selection perspective. It follows from the equivalence principle that they are also amenable to an inclusive fitness analysis. Indeed, the one specific example of secondary behavior from the nonhuman behavioral literature (“worker policing” in honey bees; p. 148) usually is explained as follows. In social Hymenoptera, when the mother queen mates more than two times, workers are more closely related to their brothers than to their nephews; hence, the workers are selected to police against male production by their sister workers. In other words, worker policing is readily (perhaps most easily) explained in an inclusive fitness framework. Indeed, other forms of secondary behaviors, such as reproductive bribing, have been explained in inclusive fitness frameworks. Even more importantly, for the second part of the book, SW have completely overlooked a rapidly growing theoretical and empirical literature on a mathematically well-articulated class of models of societal evolution, models in which cooperation is fostered by reproductive transactions among group members. These inclusive fitness-based models of “optimal reproductive skew” attempt to explain the degree of reproductive sharing within animal societies by predicting the conditions under which dominant breeders will reproductively “pay” subordinates to stay and cooperate peacefully instead of leaving to reproduce solitarily or fighting to the death for complete control of the group’s resources. It turns out that these models not only quantitatively predict the reproductive partitioning within societies but also the conditions under which a group should form at all. Moreover, the skew models generate detailed, testable predictions about how genetic relatedness, ecological constraints on solitary reproduction or movement to other groups, ecological benefits of being in a group, and competitive efficiencies of group members will interact to affect both the reproductive partitioning and the scope for conflict within groups. By firmly coupling the reproductive skew to the ecological context and to the reproductive options of group members, these models eliminate the fuzzy indeterminacy of SW’s version of human social evolution and make specific predictions about the properties of societies, and, yes, about the extent that these societies will exhibit group-level adaptedness (via the equivalence principle!).

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For example, skew theory predicts that extensive reproductive sharing and low levels of intra-group conflict should occur in small groups of non-relatives for which there are only moderate benefits to grouping or relatively weak ecological barriers to dispersal or solitary reproduction. This potentially explains SW’s observation that extensive resource sharing typically is exhibited in locally autonomous, small-scale human societies (p. 184). It should be noted that these skew theories do not assume genetic differences among societies and will be strongly predictive even if humans are programmed with extremely flexible inclusive fitness-maximizing algorithms. Interestingly, SW missed an opportunity to show that skew theory can comfortably fit into a multi-level selection framework (the equivalence principle at work again!). For a simple two-person group, let sol ⫽ a subordinate’s expected success if it breeds solitarily, lone ⫽ a dominant’s success if the subordinate leaves, and group ⫽ the dyad’s total reproductive output if the subordinate joins the dominant. Many interested in optimal skew theory may find it shocking that the condition for stable group formation reduces to just sol ⫹ lone ⬍ group (this condition is usually presented in the less transparent mathematical form x ⬍ k ⫺ 1, where x ⫽ sol/lone and k ⫽ group/lone). In other words, according to optimal skew theory, which is derived from standard Hamiltonian inclusive fitness, a group should form whenever the group output exceeds the summed output of the two solitary individuals. This sounds like unabashed group selectionism, but the above relatedness (rp)-independent condition for favored grouping is derived straight from Hamilton’s kin selection theory! The explanation is that a reproductive transaction between a dominant and a subordinate causes their genetic interests to align in exactly the way that maximizes overall group success. The reproductive transaction is stable, however, only if there are checks on cheating during the transaction (secondary behaviors in the sense of SW). The most valuable contribution made by SW in their section on human societal evolution is their illustration of how an anthropological data base known as the Human Relations Area Files (HRAF) might serve as a fertile testing ground for theories of human societal evolution (pp. 160–194). Although the theory advanced by SW has too many degrees of freedom and thus is consistent with almost any pattern of normative systems, data from HRAF ideally will provide useful qualitative tests of theories, like skew theories, that make specific predictions about connections between ecology and societal attributes. Finally, the extensive discussion of “psychological altruism” in the last part of the book represents an exciting initial penetration of evolutionary thinking into the psychology of motivation. Of course, the insights to be gained can be represented either in the multi-level selection or in inclusive fitness theory. For example, it would not be at all surprising if there are distinct “pleasure centers” in the human brain corresponding to the “between-group” versus “within-group” component of overall fitness or to the “personal component” versus “kin component” of inclusive fitness. So what is a modern evolutionary biologist to make of Unto Others? One can enthusiastically embrace the advocated procedural pluralism, as implied by the equivalence principle, although many will be scared away by SW’s own inconsistent adherence to this principle. The causal pluralism, particularly the admission of nonfunctionalism into the analysis of human cooperation, is far less welcome, particularly because there are much better-elaborated evolutionary theories of societal attributes (skew theories) that are standing in line to be

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tested first. Unto Others is at its best when it colonizes new conceptual lands for evolutionary biology, as in the novel use of anthropological data to form and test evolutionary hypotheses, as well as in the new investigation into the evolutionary underpinnings of psychological motivation. Hudson Kern Reeve, Associate Professor Section of Neurobiology and Behavior Cornell University Ithaca, New York