The primary impetus to explicit debate appeared with the publication, in 1962, of V. C. Wynne-Edwards's Animal Dispersion in Relation to Social Behavior. Since most evolutionists now regard Wynne-Edwards's primary argument as wrong (and I do not dispute this consensus), we greatly undervalue his work and misconstrue its importance. Most evolutionists today, many of who have never read Wynne-Edwards, know his book only by reputation as a dumb argument for group selection that George Williams and others thoroughly demolished. I regard this assessment as entirely unfair. Wynne-Edwards's claim for group selection may be wrong, but I can cite few other theories, presented within evolutionary biology during my career, that could be deemed so challenging in implication, so comprehensive in claims, so fascinating in extension, and so thought-provoking.
First of all, and essential for grasping the book's sweep, “Animal Dispersion” presents a theory about organic self-regulation of population numbers, not primarily an argument for group selection in general (although group selection serves as a fundamental feature of the proposed mechanism). Wynne-Edwards begins, as so many others have done (including Darwin), with an analogy to human institutions. When predators show no restraint in the midst of plenty, ecosystems may crumble as both predators and prey succumb. He speaks with feeling about the collapse of Arctic whaling (1962, p. 5): “The stocks of the two right whales have never recovered, and the population of Greenland-whaling men and of those who ministered to them has become effectively extinct.”
Wynne-Edwards then generalizes from carnivory to food-based limitation in any kind of eating, and to the transcendent need for regulating population sizes of consumers in any ecosystem. I am fascinated that Wynne-Edwards, in this statement, invokes the same, largely metaphysical, argument that Darwin proposed in specifying a summum bonum for the construction of nature (a situation established by very different mechanisms in Wynne-Edwards's and Darwin's systems): the old principle of plenitude, or maximization of the kinds and numbers of organisms in any given segment of earthly real estate (see p. 229 for Darwin's version): [Page 548]
The need for restraint in the midst of plenty, as it turns out, must apply to all animals whose numbers are ultimately limited by food whether they are predators in the ordinary sense of the word or not... Where we can still find nature undisturbed by human interference, whether under some stable climax of vegetation or proceeding through a natural succession, there is generally no indication whatever that the habitat is run down or destructively overtaxed. On the contrary the whole trend of ecological evolution seems to be in the very opposite direction, leading towards the highest state of productivity that can possibly be built up within the limitations set by the inorganic environment. Judging by appearances, chronic over-exploitation and mass poverty intrude themselves on a mutually-balanced and thriving natural world only as a kind of adventitious disease, almost certain to be swiftly suppressed by natural selection. It is easy to appreciate that if each species maintains an optimum population-density on its own account, not only will it be providing the most favorable conditions for its own survival, but it will automatically offer the best possible living to species higher up the chain that depend on it in turn for food. Such prima facie argument leads to the conclusion that it must be highly advantageous to survival, and thus strongly favored by selection, for animal species (1) to control their own population-densities, and (2) to keep them as near as possible to the optimum level for each habitat they occupy (1962, pp. 8-9).
In Darwinism, this regulation proceeds by a fundamentally Malthusian method — imposed from outside by a hecatomb on populations that outstrip resources. Wynne-Edwards holds that such an indirect and inefficient mode of external imposition wreaks havoc upon ecosystems, and that existing stabilities therefore imply the operation of an entirely different system for regulating populations — internally, by complex sets of behaviors that limit reproduction and match population sizes to appropriate resources. Since the Darwinian imperative leads organisms to maximize their own reproductive success, such internal limitation can only be achieved by mechanisms of group selection powerful enough to counteract the personal gains of individual organisms from conventional Darwinian selection.
The ingenuity of Wynne-Edwards's theory lies largely in the range of behavioral phenomena that he interprets as devices evolved by group selection for limitation of population size. In fact, Wynne-Edwards ascribes the origin of social organization itself to this need for limitation upon the size of populations. Note that by “conventional competition” he does not mean the vernacular “orthodox” or “ordinary” (which would then become Darwinian, or the opposite of his personal intention), but rather apparent competition by bluff, ritual and display — convention in this sense — rather than actual (and potentially destructive) fighting:
Undisguised contest for food inevitably leads in the end to overexploitation, so that a conventional goal for competition has to be evolved in its stead; and it is precisely in this — surprising though it may appear at first sight — that social organization and the primitive seeds of all social [Page 549] behavior have their origin ... Putting the situation the other way around, a society can be denned for our purposes as an organization capable of providing conventional competition: this, at least, appears to be its original, most primitive function, which indeed survives more or less thinly veiled even in the civilized societies of man (1962, p. 14).
Almost all the rich repertoire of putative Darwinian behaviors become, for Wynne-Edwards, devices evolved by groups of organisms to limit their population size. Dominance hierarchies and pecking orders become group-selected controls, exercised by denying reproductive rights to large numbers of potential breeders. The chorusing of frogs, insects and birds become censusing devices, whereby populations may judge their numbers and trigger appropriate behaviors of regulation.
Such homeostatic adaptations exist in astonishing profusion and diversity, above all in the two great phyla of arthropods and vertebrates. There we shall find machinery for regulating the reproductive output or recruitment rate of the population in a dozen different ways — by varying the quota of breeders, the number of eggs, the resorption of embryos, survival of the newborn and so on; for accelerating or retarding growth-rate and maturity; for limiting the density of colonization or settlement of the habitat; for ejecting surplus members of the population, and even for encompassing their deaths in some cases in order to retrieve the correct balance between population-density and resources (1962, p. 9).
Such massive suppression of the Darwinian game could only be achieved by group selection — that is, by the differential success of groups with emergent social behaviors that debar reproduction for many members, thus limiting population size from within, and winning temporal persistence by avoiding collapse through overexploitation: “We have met already with a number of situations — and shall later meet many more — in which the interests of the individual are actually submerged or subordinated to those of the community as a whole” (1962, p. 18).
Wynne-Edwards surely understood the stringent requirements for such a mechanism. He recognized, for example, that demes or social groups must be persistent and genealogically exclusive in order to act as higher-level “individuals” in a selective process — as in this epitome of his views on group selection (1962, p. 144).
To understand group-selection we ought first to recognize that normally local populations are largely of common descent, self-perpetuating and potentially immortal. They are the smallest subdivisions of the species of which this is true, and can be adapted to safeguard their own future. What is actually passed from parent to offspring is the mechanism for responding correctly in the interests of the group in a wide range of circumstances. What is at stake is whether the group itself can survive or will become extinct. If its social adaptations prove inadequate, the stock will decline or disappear and its ground be colonized by neighboring [Page 550] stocks with more successfu
l systems: it must be by this process that group-characters slowly evolve.
The abstract logic of this argument cannot be faulted, but we must ask if the required conditions are encountered frequently enough in nature. Do social groups remain sufficiently exclusive; is group selection strong enough to overcome Darwinian organismic selection; do social behaviors originate by organismal or group selection? Nearly all evolutionists would now agree that groups rarely maintain the required cohesion, and that group selection (in Wynne-Edwards's mode) will usually be far too weak a force to prevail over the conventional Darwinian mechanism of organismic selection.
George Williams's brilliant book, Adaptation and Natural Selection (1966), provided the historical focus for general rejection of Wynne-Edwards's theory. Williams wrote with other sources and targets in mind as well. (He told me, for example, that he had originally been most strongly motivated by the false arguments of Allee, Emerson and the Chicago school.) But Wynne-Edwards stood out as the main group-selectionist game in town when Williams wrote his book.
Williams's book won deserved influence by its incisiveness of logic and argument, and for its persuasive style of composition. (I know no better example of a work that prevailed primarily by the entirely honorable sense of the unfairly maligned word “rhetoric,” properly defined as “the effective use of language.”) Williams begins by characterizing adaptation as an “onerous” concept that should be invoked only when all simpler explanation fails. We should then become all the more impressed when we find that we need to invoke adaptation so often! Having established one “tough” criterion by permitting the invocation of adaptation only when all else fails, Williams then proposes another — this time governing the advocacy of levels higher than the conventional Darwinian focus upon organisms. In short, Williams states, don't make a claim about higher levels unless both logic and empirics permit no other alternative. Adaptation is onerous enough in any case; if we must call upon such a mechanism, we should do so at the lowest possible level of the genealogical hierarchy. This appeal to some form of parsimony or reduction leads Williams to reject all claims for group selection, so long as Darwinian organismic selection can render the same phenomenon in principle. Williams presents his argument largely as a theoretical proposition, and only rarely as an empirical claim. If the phenomenology of a situation can be rendered by an organismic interpretation, he asserts, one should then advocate this lower level of causality — even if a group selectionist scenario violates no tenet of logic or plausibility.
In his introductory pages, Williams tells us that claims for group selection have inspired his attempt at cleansing and simplification:
Even among those who have expressed the opinion that selection is the sole creative force in evolution, there are some inconsistent uses of the concept. With some minor qualifications to be discussed later, it can be said that there is no escape from the conclusion that natural selection... [Page 551] can only produce adaptations for the genetic survival of individuals. Many biologists have recognized adaptations of a higher than individual level of organization. A few workers . . . postulate that selection at the level of alternative populations must also be an important source of adaptation, and that such selection must be recognized to account for adaptations that work for the benefit of groups instead of individuals. I will argue . . . that the recognition of mechanisms for group benefit is based on misinterpretation, and that the higher levels of selection are impotent and not an appreciable factor in the production and maintenance of adaptation (1966, pp. 7-8).
This statement includes several interesting features, suggesting useful definitions and frameworks that I will follow throughout this book (while often disagreeing with Williams's own conclusions): (1) The term natural selection shall refer only to Darwin's process at the organismic level; selection at higher levels requires a different name. (2) The logic of group (and higher level) selection cannot be denied; we may only reject the process as impotent relative to natural selection, not as inconceivable. (3) The criterion advanced by group selectionists — the existence of properties that work for the benefit of groups, but at the expense of individual organisms — may be sound in theory but inapplicable in fact, for virtually all proposed cases either have been misinterpreted or remain subject to recasting in terms of advantages for organisms alone.
Williams then states his “doctrine,” frankly so designated: “The ground rule — or perhaps doctrine would be a better term — is that adaptation is a special and onerous concept that should be used only where it is really necessary. When it must be recognized, it should be attributed to no higher a level of organization than is demanded by the evidence. In explaining adaptation, one should assume the adequacy of the simplest form of natural selection, that of alternative alleles in Mendelian populations, unless the evidence clearly shows that this theory does not suffice” (1966, pp. 4-5).
Williams's doctrine then serves as a hammer against group selection. This higher-level process poses no problem in theory, for “there can be no sane doubt about the reality of the process. Rational criticism must center on the importance of the process and on its adequacy in explaining the phenomena attributed to it” (1966, p. 109). But group adaptation is both methodologically onerous (more so than Darwinian adaptation, which is onerous enough already), and theoretically impotent (though potentially operative).
If there are many adaptations of obvious group benefit, which cannot be explained on the basis of genic selection, it must be conceded that group selection has been operative and important. If there are no such adaptations, we must conclude that group selection has not been important, and that only genic selection — natural selection in its most austere form — need be recognized as the creative force in evolution. We must always bear in mind that group selection and biotic adaptation are more onerous principles than genic selection and organic adaptation. They [Page 552] should only be invoked when the simpler explanation is clearly inadequate (1966, pp. 123-124).
(Note that Williams here introduces the ultimate causal reduction to genes as units of selection. He speaks of adaptation at the organismic level — but only as the consequence of genic selection. Thus Williams's book also becomes the manifesto for the ultimate — and, I think, erroneous — Darwinian reductionism still popular today as “selfish gene” thinking in such fields as socio-biology and evolutionary psychology. See Chapter 8 for a critique.)
In closing, Williams waxes messianic in his pointed comparison of natural selection with the teachings of Jesus (see John 8:12 and 14:6): “Perhaps today's theory of natural selection, which is essentially that provided more than 30 years ago by Fisher, Haldane, and Wright, is somewhat like Dalton's atomic theory. It may not, in any absolute or permanent sense, represent the truth, but I am convinced that it is the light and the way” (1966, p. 273).
I love Williams's book; his austere and incisive argument shaped my thinking and that of all evolutionists in my generation. But Williams's central thesis includes a disabling problem in logic, one that produced unfortunate effects in evolutionary practice. Parsimony, or Occam's razor, embodies an important logical principle when properly applied. William of Occam, a 14th century English philosopher and divine (a Franciscan), strongly espoused nominalism against the Platonic concept of ideal types as entities in a realm higher than material existence. (For nominalists, our designations of general categories only have standing as names [nomina] based on abstraction from objects in the material world, not as ideal and “excess” archetypes in a non-material realm.) Occam devised his famous motto, “non sunt multiplicanda entia praeter necessitatem” (entities are not to be multiplied beyond necessity), as a weapon in this philosophical battle — an argument against the existence of an ideal Platonic realm (for nominalists regard names of categories only as mental abstractions from material objects, and not as descriptions of higher realities, requiring an additional set of unobserved ideal entities, or essences).
Occam's razor, in its legitimate application, therefore operates as a logical principle about the complexity of argument, not as an empirical claim that nature must be maximally simple. Williams's key invocation of parsimony — to reject group selection when an explanation based on organismic selection can be devised for the same results — fails as a general argument, and does not use Occam's razor in a valid manner, on two grounds:
1. Whereas Occam's razor holds that we should not impose complexities upon nature from non-empirical sources of human argument, the factual phenomena of nature need not be maximally simple — and the Razor does not address this completely different issue at all. The Lamarckian one-step route to adaptation, for example, operates more simply and directly than the Darwinian two-step process of variation and selection. But nature happens to follow Darwin's path. Similarly, the simultaneous operation of several hierarchical levels in selection may represent a more complex system than the idea that selection [Page 553] works only on organisms. But nature may (and does) work in this hierachical manner.
2. We should recognize Williams's claim as a statement about reductionism, not (as he thought) as an invocation of parsimony. Organismic selection is not intrinsically “simpler” than group or species selection. (One could only call organismic selection “simpler” in the obviously invalid psychological sense of affirming our habits and legacies as Darwin's intellectual children.) Consider Williams's argument: “Various levels of adaptive organization, from the subcellular to the biospheric, might conceivably be recognized, but the principle of parsimony demands that we recognize adaptation at the level necessitated by the facts and no higher. It is my position that adaptation need almost never be recognized at any level above that of a pair of parents and associated offspring” (1966, p. 19).
The Structure of Evolutionary Theory Page 88