The Units of Selection and the Bases of Selection

The Units of Selection and the Bases of SelectionAuthor(s): David WaltonSource: Philosophy of Science, Vol. 58, No. 3 (Sep., 1991), pp. 417-435Published by: The University of Chicago Press on behalf of the Philosophy of Science AssociationStable URL: http://www.jstor.org/stable/187941 .

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THE UNITS OF SELECTION AND THE BASES OF SELECTION*

DAVID WALTONtt

Committee on the Conceptual Foundations of Science University of Chicago

A correct analysis of hierarchical selection processes must specify 1) the objects that succeed differentially as units, and 2) the properties that provide the causal bases for differential success. Here I illustrate how failing to recognize the units/bases distinction creates a contradiction in Elliott Sober's recent account of selection. A revised criterion for units of selection is developed and applied to examples at several biological levels. Criteria for bases of selection are discussed in terms of the degree of context-dependence and directness of a property's effect on the success of units. The significance of previous work by Sober, Wimsatt and Brandon is thereby clarified.

1. Introduction. In this paper, I argue that much of the confusion present in the literature on hierarchical selection processes stems from a failure to clearly distinguish the question, "What are the objects that selection acts upon as units?" from the question, "Which properties are causally relevant, in a specified way, to selection among the given units?" The former corresponds to the traditional units of selection problem. The latter has to do with what I call the bases of selection. My claim is that past attempts to define units of selection have often employed criteria appro- priate only to bases.

I begin, in section 2, by bringing out an apparent contradiction in Elliott Sober's (1984) account of genic and group selection. This is followed by my own analysis, which shows how Sober's view becomes coherent once the units/bases distinction is recognized. In section 3, a revised criterion for units of selection is developed in terms of the uniform influence of a property on the success of the selected unit. The revised criterion is then used to reinterpret the examples given by Sober of selection at different levels. While our group selection analyses largely agree, I interpret most of his putative cases of genic selection as selection on a larger unit. The

*Received September 1988; revised June 1989. tI am grateful to David Hull, Ron McClamrock, Robert Richards, Elliot Sober, David

Sloan Wilson and an anonymous referee for their insightful comments on this paper. I owe a special debt to William Wimsatt for his unflagging support of my work. Mardi Solomon provided much needed encouragement, for which I thank her.

tSend reprint requests to the author, Committee on the Conceptual Foundations of Sci- ence, University of Chicago, 1126 East 59th Street, Room 207, Chicago, IL 60637.

Philosophy of Science, 58 (1991) pp. 417-435. Copyright C) 1991 by the Philosophy of Science Association.

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418 DAVID WALTON

goal in section 4 is to flesh out the notion of a selective basis. This involves two sorts of considerations. The first is that of context-dependence in the adaptive consequences of genes and other properties, as discussed by William Wimsatt and again by Sober. Their arguments suggest an interesting sense in which the effects of higher-level properties may be "emergent". Second, Robert Brandon argues for the importance of direct- acting over indirect-acting properties (phenotype over genotype) in selection. The novel aspect of the present effort is to treat claims about the emergence and directness of causal properties as distinct from, and po- tentially independent of, claims about which entities are being selected as units. Section 5 is a summary of the main points.

2. Sober's Account. The starting point for recent approaches to the units- of-selection problem is the maxim, first elaborated by Darwin and gen- eralized by Lewontin (1970), that natural selection requires variation in properties that influence success in survival and reproduction, that is, variation in fitness.' In a given selection process, however, variation in fitness may exist simultaneously at more than one level of organization. For example, variation in the fitnesses of different genes usually implies fitness differences among the organisms that house those genes. Variation in organismic fitness may, in turn, translate into the differential productivity of groups of organisms. Consequently, the variation-in-fitness criterion fails to specify "at what level(s) the causal machinery of selection really acts" (Brandon 1982, 321).

Sober's solution to this problem hinges on the distinction he draws between selection of objects and selection for properties:

"Selection of" pertains to the effects of a selection process, whereas "selection for" describes its causes. To say that there is selection for a given property means that having that property causes success in survival and reproduction. But to say that a given sort of object was selected is merely to say that the result of the selection process was to increase the representation of that kind of object. (1984, 100)

It is easy to guess from Sober's use of "merely" in describing the selection of objects that he intends to make selection for properties the linchpin of his positive account:

'I omit the additional desideratum that the variation in fitness be heritable-that off- spring resemble their parents with respect to characters contributing to survival and reproduction-because I am concerned in this paper only with the conditions necessary for selection per se, and not the evolutionary response to selection (see Lande and Arnold 1983, 1210). The problem addressed here is therefore both narrower and more tractable than the one motivating authors who include heritability as an integral feature of their analyses, for example, Wimsatt and Hull (see f.n. 10 and f.n. 14 below).



UNITS AND BASES OF SELECTION 419

Group selection means that group properties cause differential survival and reproductive success. Genic selection means that genic properties are causally efficacious in this way. But . . . it remains to be said what the objects are that these causally efficacious properties attach to. (Ibid., 279)

In general, then, Sober requires that a unit of selection possess a property which causes differential success in survival and reproduction. How- ever, the differential success appealed to in this criterion is not generally that of the unit itself, but rather that of a reference object which Sober calls a "benchmark". For example, organisms are the benchmarks in his initial definitions of both genic and group selection (ibid., 280).

There is group selection for groups that have some property P if and only if:

(1) Groups vary with respect to whether they have P, and (2) There is some common causal influence on those groups that makes

it the case that (3) Being in a group that has P is a positive causal factor in the

survival and reproduction of organisms.

There is selection for possessing the gene P if and only if:

(1) Organisms vary with respect to whether they have P, and (2) There is some common causal influence on those organisms that

makes it the case that (3) Possessing the gene P is a positive causal factor in the survival

and reproduction of organisms.

Clause (1) of each definition requires there to be variation in the property being selected for. Clause (2) requires that the varying members of the population be exposed to a common selective environment; this guar- antees that they are all participating in the same selection process (ibid.). According to clause (3), the property in question must be a "positive causal factor in the survival and reproduction of organisms". Such a property "raises the probability of the effect in at least one background context and [does] not lower it in any" (ibid., 294). Thus, group selection requires that the group property increase the fitness of some group members, and not lower the fitness of any. Selection for a gene requires that some of its bearers be more fit, and none less fit, than they would be otherwise. The important thing in both cases is that the property play "a univocal causal role" (ibid., 303) with respect to organismic success.

In taking organisms as the benchmarks, Sober attempts to explain genic selection in terms of the "upward" effects of a gene on higher-level success while his group selection explanations work "downward" from group



420 DAVID WALTON

properties to lower-level success. Later in the book (chap. 9), Sober allows for cases of genic selection in which the benchmarks are either chromosomes (meiotic drive) or the genes themselves ("selfish DNA"), and a case of group selection in which the whole group is the benchmark (species selection). Even then, however, the genic selection benchmarks are never less inclusive than the individual gene, while the group selection benchmarks are never more inclusive than the group. This seems natural, given that Sober is expanding in both directions from an initially organism- centered view of selection. Nonetheless, I argue that if one follows Sober in interpreting his "bottom-up" and "top-down" criteria as different-level variants of a single method for picking out units of selection, then the answers obtained from their application fail to cohere.

Comparison of the two criteria is complicated by the fact that in none of Sober's examples are groups taken as benchmarks for genic selection, and vice versa. In effect, the organismic level acts as a buffer zone between the higher and lower levels. This is probably why the contradictory nature of the criteria is not immediately apparent. The contradiction is revealed through a simple perceptual shift in which the genes in an organism are viewed as analogous to organisms in a group.

Consider, for example, a quantitative character of organisms such as height, its value determined by the small but cumulative effects of a large number of genes at different loci. Suppose that a "plus" gene-one that increases height-has a bottom-up effect on organismic reproductive success which is positive for all of the organisms inhabiting a particular selective environment.2 In Sober's lexicon, each plus gene is a positive causal factor in the success of organisms. Assume further that the organisms vary in the number of such genes they possess. Given a situation like this, Sober concludes that there is genic selection for plus genes; the gene, he asserts, is the unit of selection (ibid., 305-306).

Now comes the perceptual shift. When a plus gene is added to an organism's genome, all of the genes in that organism benefit equally from the resulting increase in organismic fitness. From this top-down view- point, the organismic property of having that plus gene is a positive causal factor in the success of genes. Consequently, an analogue of Sober's group selection criterion is satisfied at the organismic level where each organism is now characterized as a group of genes. But this implies that the unit of selection is the organism, not the gene as concluded in the previous paragraph. Brought face to face without the benefit of a third intervening level, the bottom-up and top-down accounts of selection give mutually exclusive solutions to the same problem.

The difficulty in Sober's scheme is illustrated equally well at the level

2This will be true if all individuals are below the optimal height for that environment.




of conventional groups. Sober argues that groups count as units of selection when each organism's fitness is increased by being in a "tall group" (ibid., 316). To give this example some flesh, imagine groups of visual predators hunting in tall grass. Groups with more members tall enough to see over the grass are better at locating prey than groups with fewer tall members. If the spoils of the kill are shared among group members, the group property of containing many tall members is then a positive causal factor in the success of organisms. Continuing our analogy, let us now liken the organisms in each group to genes in an organism. Just as each plus gene causes an incremental increase in the height of an organism, so the height of each organism contributes in a linear fashion to the average height of its group. If containing a tall organism improves the fitness of each group, the organism is a positive causal factor with respect to group success. Sober's bottom-up analysis would thus point to the organism as the unit of selection, which is in flat contradiction to his original top-down invocation of group selection.

A comparable switch in perspective may be carried out to like effect at virtually any level. Where Sober sees genic selection against a dominant lethal (ibid., 306), a top-down view reveals organismic selection against organisms carrying the lethal gene. To Sober's bottom-up view of meiotic drive in which chromosomes act as benchmarks for genic selection (ibid., 308), one may oppose a top-down argument that makes genes the benchmarks in chromosomal selection. Arguing the other way, might not selection even among selfish DNA molecules (ibid., 309-310) be explicable in terms of the bottom-up effects of particular nucleotide substitutions? I conclude that Sober's analysis fails to supply consistent answers to the question, "What are the units of selection"?

One might attempt to defend Sober at this point by questioning the validity of the perceptual shifts used to generate the above contradictions. For example, by analogizing organisms first to groups and then to genes, I may appear to have unfairly applied Sober's group and genic selection criteria in ways that he never endorsed. But in doing so, I did no violence to the form of his analysis; I merely shifted levels. Any criterion for units of selection that works only at certain preferred levels is fatally pro- vincial. A successful criterion must be applicable throughout the hierarchy of potential units. The paradoxes to which Sober's approach leads should at least motivate us to search for an alternative that avoids these difficulties.

So far, I have illustrated how Sober's top-down and bottom-up criteria come into conflict when both are used to identify units of selection. Rather than take this conflict as grounds for rejecting one or both criteria, I suggest that they are really getting at different aspects of the selection process. This brings us back to the distinction, mentioned at the beginning,



422 DAVID WALTON

between units and bases. In my view a strengthened version of Sober's criterion for group selection correctly picks out entities that are being selected as units. On the other hand, his genic selection criterion identifies one kind of property (though not the only kind) that provides a causal basis for the differential success of units. These issues will be addressed in turn.

3. Selection of Objects as Units: The Units of Selection. Selection involves the differential success of entities that vary in fitness. However, a given episode of selection may alter the frequencies of entity-types at multiple levels. The challenge is to identify those entities that are not only being selected, but those that are being selected as units. This requirement may be unpacked as follows. Since selection distinguishes entities according to differences in their fitness values, an entity can be selected as a unit only if some aspect of fitness has been causally determined for that entity as a unit. I will first spell out what it means for entities to qualify as units in the latter sense, and then work backwards to the original stipulation that the entities actually vary in fitness.

In an important early paper, Sober (1981) writes:

When group selection occurs, all the organisms in the same group are bound together by a common fate. As far as this selective force is concerned, they are equally fit. What determines these identical fitness values (on the component of fitness at issue) is their mem- bership in the same group. (P. 107)

In other words, for the fitness of a group to be determined for the group as a unit, some group property must first identically determine the fitnesses of all individuals within the group. As Sober notes parenthetically, this is not to say that all group members must have the same total fitness. Instead, the required identity need obtain only for some shared component of fitness, corresponding to the causal effect of the group property on organismic survival and reproduction in relation to a particular environ- mental force (e.g., predation). However, whereas Sober allows the magnitude of the effect to vary as long as its direction remains constant (recall his positive causal factor criterion), my argument demands complete uni- formity of effect on success within the group. Anything less than this introduces a degree of disunity into the group with respect to fitness.

The last point needs clarification. On my analysis, the fact that a property impacts unequally upon the success of different group members does not preclude that group from being a unit with respect to fitness. Instead, the group has its fitness determined as a unit to the extent that the effect on all members is the same. For example, a bacterium might secrete a toxin whose concentration, and hence harmful effect on other bacteria,




falls off as a function of distance. In this case, the degree to which any given individual is part of the unit defined by that effect diminishes with distance as well. This gives rise to a series of overlapping units, each centered around a particular bacterium, and each with a "fuzzy" boundary that gradually fades out at the edges. Regarding the value of this fitness component, however, it remains true by definition that the members of a given unit are identical. Here, I restrict discussion to the simpler cases in which the units have spatially distinct beginnings and ends.

Construed as above, Sober's top-down criterion still captures only half of what it means for a group to be a unit with respect to fitness. The flipside of the requirement that the group property uniformly affect the success of all individuals in the group is that the property not have the same effect on any individual outside of the group. That is, the group in question must be the most inclusive collection of organisms whose members are so influenced. If the homogenizing effect of the property on organismic success extends to nonmembers as well, then the original group does not itself have its fitness determined as a unit. Instead, it becomes part of a yet larger group whose fitness is determined as a unit. The limits of that larger group are defined by the range over which the property in question exerts a uniform effect on the success of organisms.3

In characterizing groups as units, the required relationship between group property and group success has so far been stated in terms of the shared fate of organisms comprising the group. Sometimes, however, variation in fitness among the units at one level may have no counterpart at lower levels. For example, selection could favor groups that are more stable than other groups even when the "death" of a group corresponds, not to the death of its members, but to their reassortment into associations of a stabler kind.4 It does not matter that the property conferring stability upon the group as a whole has no effect on stability at lower levels, so long as the property does not cause stability differences among smaller entities within the group. I therefore agree with Sober that reference to lower- level fitnesses is not generally necessry to describing units of selection (see Sober 1984, 366-368). The important thing is that there be an ex- haustive way to divide up each unit such that the relevant property ho- mogenizes fitnesses within the unit but allows for differential fitness among units. Whether this division is fine-grained (referring to lower-level fitnesses) or coarse-grained (referring to the fitness of the unit as a whole) will depend upon the causal structure of the situation at hand.

3This range is equivalent to the "sphere of influence" of a trait that D. S. Wilson (1980) refers to when defining the trait-groups that figure in his models of group selection.

4Indeed, the entire history of life may be viewed as just such a reassortment process, iterated on a geological time scale, among the handful of relatively immutable chemical elements that make up living systems.



424 DAVID WALTON

All of the ingredients that go into my criterion of units have now been presented. Before applying this criterion to the putative examples of selection at different levels discussed by Sober, I would like to cast it into a general form:

Property P determines fitness component W for entity E as a unit if, and only if, E is the most inclusive entity such that, for some ex- haustive division of the entity into parts, P identically determines W among all parts, and does not differentially determine W within any part.

Once this condition is satisfied, selection requires only variation among units in the relevant component of fitness:

Entities E1, E2, . . ., En are units of selection (i.e., each entity is selected as a unit) if and only if they vary with respect to a property that determines the same fitness component for each entity as a unit.

This definition leads to roughly the same conclusions that Sober draws in examples of group selection. First, recall our groups of cooperative hunters in which the survival of group members is enhanced by increasing the number of tall predators in the group. Suppose that such an increase benefits all individuals within the group equally, but leaves the fitnesses of any animals outside the group unchanged. It follows then that the property of having many tall members determines the fitness of each group as a unit, as per the above definition. If groups vary along this dimension, the requirements for group selection are satisfied.

A second example shows how my definition accomodates cases in which selection is acting simultaneously at more than one level. In the Myxoma- rabbit system discussed by Lewontin (1970, 14-15; also see Sober 1984, 331-334), low virulence in a given virus particle determines two different components of fitness. The effect on immediate replication rate is negative and restricted to the individual virus. To this extent, a less virulent virus particle has its fitness decreased as a unit, and there is selection against low virulence at this level. At the same time, by helping to fore- stall the death of its host, the less virulent individual reduces the extinc- tion risk of the virus group as a while. This results in group selection for less virulent groups. All cases of such "altruistic" behaviors are correctly analyzed in terms of selection acting in opposite directions at different levels (see, for example, Wilson 1980).

Now let us shift the focus to Sober's putative examples of genic se-

'In a work currently in progress (1989), I refer to fitness components that are determined in this way as the exclusive fitness of an entity because selection at a given level acts exclusively on variation in such components.




lection, for there the results of our respective analyses diverge. Sober discusses two cases that he sees as genic selection with an organismic benchmark. In the first, the effect of a gene on organismic success is positive in all genetic contexts, as exemplified by the genes for tallness discussed earlier. The second involves a dominant lethal that kills the organism carrying it, also without regard to context. On my analysis, the units of selection in both of these examples are not genes, but organisms.

The argument is straightforward. The relevant property will be a gene's tendency to cause the production of a phenotypic character which, in turn, determines fitness. But the question is, the fitness of what? It is true that the property affects the success of the gene itself. We may further pre- sume that the gene is internally homogeneous with respect to this fitness component, for example, that there is no differential propagation of certain nucleotide bases over others. Again, however, this constitutes only half of the necessary conditions for the gene to be the unit of selection. The other half, that the property not uniformly affect the success of any entity external to the gene, is manifestly violated. As noted earlier, the influence of each gene on the organismic phenotype affects the success of all the other genes in that body to an equal degree. Assuming that this uniform fitness effect does not extend beyond the boundaries of the organism-as it might if the gene caused behavior affecting neighboring organisms as well-then the whole organism, and not the isolated gene, will be the entity whose fitness is determined as a unit. Given variation in this component of fitness among organisms, a process of organismic selection will ensue.

The above argument holds even if the effect of a gene on organismic success is independent of which other genes are present. Sober's dominant lethal, for example, which is unconditionally fatal to its bearer, is not a unit of selection precisely because its poisoning effect uniformly impacts an entity larger than itself. Moreover, even in the complete absence of dominance, heterozygote advantage and epistatic interactions among loci, it is still true that the genes in a given organism are selected, not individually, but as a unit. This conclusion goes against the claim that the gene would be the unit of selection if only "beanbag genetics" were true (Wimsatt 1980, 237; Sober 1984, 312), supporting instead the traditional neo-Darwinian emphasis on organisms for a large class of adaptive traits.6

Of course, this is not to say that the organism is always the unit of selection where genic effects are concerned. For example, in cases of

6While irrelevant to the units of selection debate, the degree to which genic effects on organismic success are context-independent is central to the issue of selective bases to be taken up in the next section.



426 DAVID WALTON

meiotic drive, the driving allele increases the fitness of the whole chromosome as a unit. All genes on a chromosome containing this allele consequently have the same increased chance of making it into a successful gamete, while the genes on a chromosome lacking the allele have their fitnesses uniformly reduced. Like the organismic-level explanations offered above, this one in terms of chromosomal selection conflicts with Sober's version of gene selectionism.

As far as genic selection is concerned, my analysis agrees with Sober's only in the case of selfish DNA. An individual piece of DNA is better than other pieces at making copies of itself within the genome. The property that allows this "jumping gene" to replicate faster does not identically determine the replication ability of any other gene, not even others on the same chromosome. To the extent that the fitnesses of genes vary independently in this manner, and to this extent only, does each gene ex- perience selection as a unit.7

A final word is in order about benchmarks (i.e., reference objects) vis- a-vis my account of selection. I have argued that an entity is a unit of selection in virtue of a special kind of causal relation between a property of the entity and the entity's ability to survive and reproduce. The form of this relation was expressed by saying that the property must determine a fitness component of the entity as a unit. Since the property's effect must ultimately be referred to no other entity than the unit of selection itself, the unit is, strictly speaking, the only relevant benchmark for the selection process in which it participates. In this sense, Sober's idea of a benchmark as something distinct from the units on which selection acts, has no role in the conceptual scheme proposed here. At the same time, it has often proven useful to equate the fitness of a unit of selection with that component of fitness held in common by the smaller entities of which it is composed (a "fine-grained" analysis). This is simply a way of describing the uniform effect of the relevant property on the success of the unit, and as such is entirely unproblematic. What is explicitly forbidden on my view is that the "sphere of uniform influence" of the property should ever include an entity larger than the putative unit of selection, for this would entail selection at the level of the larger entity instead. In sum, only a top-down analysis-one moving from the properties of a unit of selection to the success of the unit itself or its lower-level parts-is consistent with my characterization of these units.

4. Selection For or Against Properties: The Bases of Selection. Given that a correct units of selection analysis is always top-down, is it yet

7This argument helps to undermine the early genic reductionism of Williams (1966) and Dawkins (1976) which privileges the gene as the sole unit of selection. Arguments against the reductionist position arise in the next section as well.




possible to make sense of Sober's bottom-up claims about genic selection? This can be done by recognizing an inherent ambiguity in the claim itself. In particular, the term "genic selection" may be taken as referring either to a process in which genes are themselves being selected as units, or to one in which possession of a gene is the property that causes selection of a higher-level unit such as an organism.8 To mark this crucial distinction, let us say in the first case that genes are the units of selection, and in the second case that a genic property is the basis of selection among organisms as units.

What makes a property causally efficacious with respect to selection among a given set of units? The analysis in the previous section suggests that the property must increase or decrease the fitnesses of units exhibiting it relative to units not exhibiting it. A positive effect on the success of a unit entails selectionfor the property, a negative effect selection against it. However, two issues may be raised at this point.9 First, consider a property whose effect is context-dependent, that is, one whose instances or "tokens" vary in their quantitative effects on different units within a population. Under what conditions should we still say that there is selection for or against the property in the population as a whole? This is the problem that Sober attempts to solve in his analysis of genic selection. An alternative solution was offered prior to Sober's by Wimsatt (1980, 1981). Both authors invoke facts about context-dependence to refute the dogmatic "gene's eye" perspective on selection (Williams 1966, Dawkins 1976), and it is instructive to compare their approaches. Second, even if the property (e.g., possessing a certain gene) increases fitness in all existing contexts, suppose it does so only indirectly through the mediating effects of a second causal property (a phenotype). Should this affect the relative significance that we attach to selection favoring each of the two properties? Brandon's (1982, 1985) affirmative response to this query is scrutinized toward the end of the section. Though some attempt is made to evaluate each of these positions, my primary goal is to argue that questions about causal properties in selection-the bases of selection-should be treated separately from questions about the selected units.

4.1. Context-Independence of Effect. For Sober, the thesis of genic selection involves a claim about "the population-level causal role of a gene of a given kind" (1984, 296). As an example, say that in a given population the effect on organismic success of gene A at one locus is positive in the presence of gene B, but negative in the presence of the alternative allele b at a second locus. Sober's point is that one cannot say uncon-

'An anonymous reviewer suggested this way of expressing the point. 9Mayr (1963, 184, 295) prefigured later discussion of both issues.



428 DAVID WALTON

ditionally that there is selection for or against A. At most, one can say that A is selected for in the B context and selected against in the b context. Here, claims about the causal role of individual tokens of gene A go through, but an unconditional claim about the overall causal role of that gene-type does not. The latter claim holds only for a gene whose effect does not flip from positive to negative in different contexts. Sober's criterion for genic selection reflects this requirement: the gene must increase the probability of success in at least one context and not lower it in any (For further discussion see Sober 1984, 281-314, and Sober and Lewontin 1982).

Let us contrast Sober's conclusion with Wimsatt's general definition of units of selection, viewed now as an attempt to define the properties that are being selected for or against:

A unit of selection is any entity for which there is heritable context- independent variance in fitness among entities at that level which does not appear as heritable context-independent variance in fitness (and thus, for which the variance in fitness is context-dependent) at any lower level of organization. (Wimsatt 1980, 236)

At the genic level, Wimsatt equates "context-independent variance in fitness" with additive genetic variance in fitness among organisms. The existence of such variation does not require that a gene's effect be additive in the strong sense of being completely independent of context, but only that the average effect of the gene over all existing contexts be non- zero. In the example above, gene A would have to have a net positive (or negative) effect on organismic success when averaged over the B and b contexts. Since this may obtain even when the direction of the effect differs for different tokens of A, Wimsatt's minimum criterion for genic selection is weaker than Sober's. On the other hand, a gene that always increases fitness may nevertheless be more beneficial in some genetic contexts than in others, making its effect partly "nonadditive". Sober is obliged to describe this situation wholly as one of genic selection. Wimsatt, however, recognizes genic selection only to the extent that the associated variance in fitness is additive, excluding any selection that arises from the gene's nonadditive effects.

On both of these readings of the genic selection issue, context-dependence of genic effects in excess of the maximal amount allowed has the following important consequence: it implies selection for a higher-level gene complex whose effect on organismic success is not reducible to the isolated contributions of the component genes. Thus, possessing genes A and B together may be unconditionally advantageous even if A itself is deleterious in the absence of B. Here, there would be selection for AB in Sober's sense, but this would not be the mere summed effect of se-




lection for A and B independently (Sober 1984, 314). The same result follows from Wimsatt's criterion because at least some of the variance in fitness not explained by the additive effects of single genes would be explained by the additive effect of the gene pair. For Wimsatt but not Sober, the existence of any residual variance not so explained would entail additional selection for a still larger gene combination, again acting in a partly irreducible manner. 1

I will not attempt to defend either Sober's or Wimsatt's position as the correct one. It does seem important to know whether a given gene is adaptive for all organisms in a population or only on average, so Sober's concerns seem well-motivated. Recall, however, that while a gene satis- fying Sober's criterion must be adaptive in at least one context, it might be adaptively neutral in others, as long as it is nowhere maladaptive. But when assessing the population-level causal role of a gene, it seems as much a mistake to confound selection for the gene with no selection at all, as it is to confound selection for with selection against. If Sober wants to pick out genes that are truly univocal in their adaptive consequences- as opposed to ones that are vocal in some places but mute in others- then he should demand positive fitness effects in all existing contexts.

On the other hand, constancy of effect isn't everything. Even when a gene has opposite fitness effects in different contexts, it still matters whether, on average, the gene has been selected for, against, or not at all. A gene that increases in frequency because its own causal influence on organismic success was on balance positive (though sometimes negative) has been "selected for" in a sense importantly different from the mere "selection of" a neutral gene that happens to be linked to the causally potent gene. Wimsatt succeeds in capturing this distinction, but Sober does not. Wimsatt's criterion has the additional virtue of being sensitive to causal context-dependencies that show up as variation in the magnitude, though not in the direction, of a gene's effect. Both sorts of context-dependence contribute to the "emergent" character of multi-gene complexes.11

Whether one is working with Sober's, Wimsatt's, or some other criterion of context-independence for genic selection, it is essential to recognize that all such criteria are properly aimed at characterizing the causal bases of a selection process, not the units of selection. In comparing the

'?These higher-level effects, while additive from the standpoint of selection within a generation, will lead to heritable change across generations only if the genes in question tend to be inherited together (e.g., linked genes on the same chromosome). Random as- sortment of genes would break up the interacting gene complexes, rendering their effects nonheritable. Wimsatt uses "additive" in the strong, heritable sense; I have adopted the weak reading in accordance with the ground rule laid down in footnote 1.

"The definition of emergent higher-level properties in terms of context-dependent effects at lower levels is developed more fully by Wimsatt (1986). See Lloyd (1988) for a sus- tained defense of Wimsatt's additivity criterion.



430 DAVID WALTON

fitness effects of gene A alone with those of A and B together, for instance, we assumed in both cases that the entity experiencing those effects as a unit is the whole organism, not single genes or gene pairs. Following Sober, if the effect of A is positive regardless of whether B is present, we might say that organisms are selected as units on the "univocal basis" of carrying A. If instead A is adaptive in company with B, but maladaptive otherwise, then organisms are still the units of selection, but they are now selected on the emergent univocal basis of carrying the AB combination. At the same time, A would still qualify as a "net basis" of selection (a' la Wimsatt) as long as its average effect on organismic success were non- zero. Equivalently, we could say that there is "emergent univocal selection" for AB, but only "net selection" for A.

Considerations of context-dependence are equally relevant when the entities being selected as units are smaller than organisms. With reference to meiotic drive, for example, Sober (1984, 308-309) mentions the existence of genes that can suppress the segregation-biasing powers of the driving allele. If suppression occurs on some chromosomes but not on others, the allele will still be selectively favored for its net positive effect on chromosomal success. Opposing this, however, will be selection against suppressed tokens of the driving allele relative to unsuppressed tokens, a process which is clearly not reducible to the allele's average effect across contexts. In either case, the whole chromosome is the unit which differentially propagates on the basis of carrying that allele.

Even when single genes are the units of selection, the basis of selection may turn out to be in some sense emergent. Thus, imagine a point mu- tation T occurring at position 2 in the nucleotide sequence of a jumping gene. If the effect of T on the gene's autonomous replication rate is positive when position 5 of the gene is C, but negative when position 5 is G, then T itself is not a univocal basis of selection among such genes. However, T in combination with C does have a univocal effect; hence TC is emergent relative to T and C separately.

Finally, toward the opposite end of the biological spectrum, selection among groups as units may occur on the basis of differences in the kinds of organisms in different groups. This is true for both the imaginary groups of tall predators and the real groups of Myxoma rabbit viruses described earlier. In these examples, there is selection for tall predators and against virulent viruses not as units themselves, but as properties of larger units. If organisms "interact" in their effects rather than influencing group success independently, the group will exhibit emergent properties above the organismic level just as interacting genes give rise to emergent properties within an organism.12 However, the existence of emergent group prop-

"2Wimsatt (1980, 237) discusses the role of "epistatic interactions between individuals" in group selection.




erties is not a prerequisite for groups to be units of selection any more than the selection of organisms, chromosomes, or genes as units requires emergent properties at those levels. The lower-level properties of organisms acting "additively" will suffice as long as their adaptive effects ram- ify back onto the group in a sufficiently unifying fashion.13

4.2. Directness of Effect. Let us turn now to the second issue raised at the beginning of this section with regard to causal properties. Here the focus is no longer on how context-dependent a property's effects are, but rather on how direct they are. For example, even if all copies of a gene have exactly the same impact on the success of the organisms bearing them, that effect must always be mediated by the production of an adaptively significant phenotype which is "visible" to selection. The phenotype is therefore the proximal, or direct, cause of success, and the gene a more remote cause.

The directness argument has been nicely formalized by Brandon in terms of W. C. Salmon's screening-off relation. As Brandon puts it, A screens off B from outcome E if and only if "A renders B statistically irrelevant with respect to outcome E, but not vice versa" (1982, 317). He argues that "in episodes of organismic selection phenotypes screen off both genes and genotypes from the reproductive success of organisms" (ibid.). This is shown by the fact that "having a certain genotype is causally irrelevant to having a certain level of reproductive success . . . given the organism's phenotype" (1985, 90). Echoing Mayr, Brandon concludes that "organismic selection acts on phenotypes, not directly on genes or genotypes" (1982, 317).

Brandon uses the directness argument to advocate the causal primacy of phenotypic characters in selection. Sober (1984, 228-230), defending Dawkins for a change, denies that the phenotype's greater directness grants it a privileged role. Sober even suggests that genes are important precisely because they are the "deeper" causes of differential success (1984, 229). I agree with Sober that when a particular gene is present, its phenotypic effects must be taken seriously. Where those effects are adaptive, the gene is selected for, albeit indirectly. On the other hand, the same phenotype may have different genetic causes in different individuals, in which case its appearance is directly selected for even in the absence of any particular gene. The robustness of the phenotypic selection process over a varied range of genetic circumstances gives Brandon's argument its force.

13This implies that the causal potency of organisms vis-a-vis group success can no more be taken as evidence against groups as units of selection than genes influencing organismic success disproves the hypothesis of selection among organisms as units. The first argument, but obviously not the second, has often been marshalled by biologists defending a strictly organismic view of selection.



432 DAVID WALTON

Since the directness of a property's effect is logically distinct from its degree of context-dependence, these two variables may be combined to create a four-fold classification of selective bases. A gene that is selected for the average of its adaptive and maladaptive phenotypic effects in different genetic contexts counts as an "indirect net basis" of selection. Lumping in the relevant background genes yields an emergent basis whose effect is univocal but still indirect. Similarly, the adaptive value of a phenotypic trait may vary according to the states of functionally related traits. Suppose, for example, that a certain change in molar size either increases or decreases chewing efficiency-and hence survival-de- pending upon the associated mandible shape and jaw muscle geometry. There will be no net selection for this change whatsoever if its opposing effects cancel out over the existing array of phenotypic contexts. There may nevertheless be net selection for trait dyads (molar X + mandible Y), and univocal selection for the entire integrated trait complex (molar X + mandible Y + muscle Z). Unlike the genes that produced them, however, each of these emergent phenotypic bases would be selected for directly.

Nor must genic properties always play as indirect a role in selection as suggested so far. The physical structure of a selfish DNA strand directly facilitates its binding to the replicase enzyme. As Hull (1988, 409) ob- serves, here the gene's structure is the relevant phenotype. And though the phenotype of an organism necessarily represents a more direct basis of selection than its underlying genotype, a particular trait may influence organismic reproductive success in a manner tortuously indirect relative to some still more proximal trait. A case in point is the control of mating behavior by hormones.

Including information about directness of effect thus lends an added dimension to the description of those properties that cause differential success, that is, the bases of selection. Notice that this information is, in principle, as extraneous to the units of selection issue as facts about context- independence of effect were earlier shown to be. Brandon (1982) insight- fully splits off context-independence at the start, though he treats it more as a distraction than as a possible source of further insights. The re- maining two issues are confounded in Brandon's ensuing discussion of the "levels of selection". After arguing that organismic selection always acts at the phenotypic level instead of the genotypic level, he goes on to ask under what conditions there is organismic selection verses group selection. As we have seen, the first comparison is between properties dif- fering in degree of causal directness, but which both function as bases of selection for the same unit. The second comparison bears on the identity of the unit itself. 14

14Both of the meanings contained within Brandon's levels discussion were originally




It is worth dwelling briefly on what can be recognized in hindsight as the units half of Brandon's analysis. For differential reproduction among entities at a given level to constitute selection at that level, Brandon requires that " [t]he adaptedness values [adaptive properties] of these entities screen off the adaptedness values of entities at every other level from reproductive values at the given level" (ibid., 319). In group selection, for instance, the group property must screen off the properties of both lower-level organisms and higher-level "metagroups" from the success of the given group. If this is interpreted to mean that the property must uniformly determine a component of fitness within the group, but not do so between groups, then Brandon's criterion picks out the same entities as does my definition of units of selection.15 However, Brandon's arguments wander back and forth between the units issue and the bases issue, and he does not always address the one relevant to a given situation.

For example, Brandon (1985) uses the fact that phenotypes screen off genotypes from organismic success to defend against Richard Dawkins's claim that adaptations are "for the good of" the gene instead of the organism. However, what this fact really proves is that phenotypic characters are more direct than genes in their adaptive consequences, that is, that such characters are the very adaptations we care about. This constitutes a claim about which property-carrying a gene, or manifesting a phenotypic trait-represents the direct basis of selection. In contrast, the correct way of completing the sentence, "Adaptations are for the good of . . .", depends at the very least on which entity benefits from the presence of a particular trait. If this is all that is being asked, and if one agrees that both organisms and their genes benefit, then the question is moot. However, it seems more meaningful to ask which entity benefits as a unit in the sense developed in this paper. In that case, the fact to emphasize is not that phenotypic traits screen off genes from reproductive success, but that some trait or another screens off other causal factors from the success of the whole organism as a unit, and not simply from

incorporated into David Hull's useful concept of an "interactor", which Hull defines as "an entity that directly interacts as a cohesive whole with its environment in such a way that replication is differential" (1980, 318). The stipulation that interaction be direct maps onto the directness criterion for causal properties, while the demand that the entity interact as a cohesive whole answers to the requirement that the property determine fitness for that entity as a unit. Hull contrasts interactors with "replicators", a term drawn from Dawkins (1976). Replicators correspond to what might be called the "units of heredity"; as such, they are explicitly what this paper is not about (see f.n. 1).

"5This interpretation imports more causal detail into the statement of the criterion than Brandon provides. The very fact that Brandon uses the screening-off relation to get at both the direct bases of selection and the units of selection shows that his criterion for each needs refining.



434 DAVID WALTON

the success of the individual gene.'6 The key nature of this fact is ob- scured in Brandon's argument, but comes into perspective in light of the units/bases dichotomy.

5. Conclusion. In closing, I will relate my analysis back to Sober's original distinction between "selection of objects" and "selection for properties". Sober rightly rejects the crude variation in fitness criterion as insufficient for defining units of selection. That there has been "selection of" a particular entity is not enough to make it a unit of selection. In this paper, I try to give meaning to the claim that an entity is not only being selected, but is being selected as a unit. I also argue that this claim is distinct from the claim that a property is being "selected for" its adaptive effects. The term "genic selection", for instance, is ambiguous because it could be taken as referring either to genes qua units, or to genic properties qua causal factors. In contrast, a prime virtue of the units/bases terminology advocated here is that it makes possible such unambiguous statements as, "Chromosomes are differentially favored as units on the basis of carrying a driving allele" and "The basis of selection among groups as units is the proportion of tall organisms within a group". Fur- thermore, it allows one to characterize properties according to the nature of their effects (net/univocal, indirect/direct), and the level of organization at which they emergently appear (genic, chromosomal, organismic, group), but without confounding this taxonomy with the hierarchy of units (genes, chromosomes, organisms, groups) that actually succeed or fail on the basis of having these properties. As diverse as these rela- tions are, the basis of selection and the unit of selection lie always at opposite ends of a single causal arrow. This arrow points from property to object, from that which confers triumph or defeat in the "struggle for existence" to that which partakes in the struggle as a unit. A complete account of any selection process can afford to neglect neither.

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Brandon, R. (1982), "The Levels of Selection", in P. Asquith and T. Nickles (eds.), PSA 1982, vol. 1. East Lansing: The Philosophy of Science Association, pp. 315-323.

. (1985), "Adaptation Explanations: Are Adaptations for the Good of Replicators or Interactors?", in B. Weber and D. Depew (eds.), Evolution at a Crossroads: The New Biology and the New Philosophy of Science. Cambridge, MA: Bradford/MIT Press, pp. 81-96.

16For the purpose of identifying units, the effect of the screened-off property need not even be indirect relative to that of the property doing the screening off. Thus, in the example of group selection in house mice cited by Brandon (1982, 319-320), all members of a group in which the males are sterile will fail to reproduce, sterile males and fertile females alike. Yet, belonging to such a group is not a more direct cause of reproductive failure than being a sterile male oneself.




Dawkins, R. (1976), The Selfish Gene. Oxford: Oxford University Press. Hull, D. L. (1980), "Individuality and Selection", Annual Review of Ecology and System-

atics 11: 311-332. . (1988), Science as a Process: An Evolutionary Account of the Social and Con-

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1: 1-18. Lloyd, L. (1988), The Structure and Justification of Evolutionary Theory. Westpont, CT:

Greenwood Press. Mayr, E. (1963), Animal Species and Evolution. Cambridge, MA: Belknap Press of Harvard

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R. Giere (eds.), PSA 1980, vol. 2. East Lansing: The Philosophy of Science Asso- ciation, pp. 93-121.

- . (1984), The Nature of Selection: Evolutionary Theory in Philosophical Focus. Cambridge, MA: Bradford/MIT Press.

Sober, E. and Lewontin, R. C. (1982), "Artifact, Cause, and Genic Selection", Philosophy of Science 49: 157-180.

Walton, D. (1989), "Hierarchical Selection and Exclusive Fitness", unpublished manu- script.

Williams, G. C. (1966), Adaptation and Natural Selection. Princeton: Princeton University Press.

Wilson, D. S. (1980), The Natural Selection of Populations and Communities. Menlo Park, CA: Benjamin/Cummings.

Wimsatt, W. (1980), "Reductionistic Research Strategies and Their Biases in the Units of Selection Controversy", in T. Nickles (ed.), Scientific Discovery: Case Studies, vol. 60. Dordrecht: Reidel, pp. 213-259.

. (1981), "The Units of Selection and the Structure of the Multi-Level Genome", in P. Asquith and R. Giere (eds.), PSA 1980, vol. 2. East Lansing: The Philosophy of Science Association, pp. 122-183.

. (1986), "Forms of Aggregativity", in A. Donagon; A. N. Perovich, Jr.; and M. V. Wedin (eds.), Human Nature and Natural Knowledge: Essays Presented to Marjorie Grene on the Occasion of Her Seventy-Fifth Birthday. Dordrecht: Reidel, pp. 259-291.



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The Units of Selection and the Bases of Selection