For over 150 years, the theory of natural selection has inspired an ever-expanding investigation into the world of adaptation—that critical element of biodiversity that draws the twin matters of ecological and evolutionary causality face to face. The focus has always been on understanding function within the natural world, and how to trace it backward through time to the origin of species. We envision, as did Charles Darwin and Alfred Russel Wallace, a “tree of life” that phylogenetically connects present forms back to their ancestors, and imagine that this tree represents not only the historical linkages between forms but also an actual coming-into-being process.
There can be no doubt that these links represent real evolutionary associations; beyond our increasing knowledge of DNA sequences, which seemingly proves this outright, one needs look no further than Wallace's “Sarawak Law” essay of 18551, which pointed to an otherwise unexplainable connection between most closely related species and their distributions in space (geographical range) and time (the fossil record). Nothing other than a diverging—evolving—pattern of relations could explain such a thing. For its own part, the concept of natural selection is based on elements that themselves can hardly be denied: there really is variation within natural populations, and a limited resource base that could in theory be over-run by the high native rates of procreation within species. Unless one argues that what would generally be understood as “less fit” individuals on the average should compete as well as more fit ones—and one cannot—it seems inescapable logic that the latter will tend to prevail and preferentially pass their genes along to their progeny.
However, natural selection has always found itself under attack, and sometimes for good reasons. Although lending itself perfectly well to interpretations of many immediate relationships—that is, to the facts of adaptation—it has proved largely ineffectual in contextualizing the larger scale: especially, the causes of variation, divergence, and speciation2, other key (and empirically evident) products of biological evolution. There is evidently a disconnect in the theory between its ecological enactment and its historical “accumulations” (as both Darwin and Wallace referred to them), recapitulated both in the DNA molecule and its manifest expressions as functioning individuals and populations. Darwin was largely oblivious to this difficulty but Wallace was not; this is perhaps not surprising as the former looked at the entirety largely from a geologist's historical vantage point, whereas Wallace was more the ecologist and geographer. The Darwinian version of natural selection soon found itself attacked as a tautology. As Lewontin once put it, “The process is adaptation and the end result is the state of being adapted…. The problem is how species can be at all times both adapting and adapted3.”
Generations of biologists and historians have identified various differences between Darwinian and Wallacean understandings of natural selection. There are many particulars, but for now two main ones may be emphasized: (1) Darwin viewed competition as occurring mainly between individual organisms, whereas Wallace emphasized the dynamics between varieties, and (2) Wallace tended to regard environmental pressures such as climate or geological change as the main selection-generating forces, whereas Darwin looked more to individual competition for resources, including sexual selection, as of primary import. In what follows I will, perhaps surprisingly, not play to a favorite: I believe both discussions represent red herrings. Instead, I would like to start by re-examining the basic question of what natural selection is—or perhaps better yet, what it is not—and then consider how a more limited view of natural selection—a more Wallacean view—might help us to identify some interesting causalities within the evolutionary process.
2. NATURAL SELECTION AS THE ELIMINATION OF THE UNFIT
In 1888, C. Lloyd Morgan, in some quarters referred to as the father of comparative psychology, made a presentation entitled “Elimination and Selection” to the Bristol Naturalists' Society. Despite Morgan's fame, this is a little known work, as it was published in the Society's obscure “Journal” series4. As the first three paragraphs of the paper well introduce the present thread, they may be reproduced in full:
Those who have read the recently published “Life of Charles Darwin” may remember a footnote in which Mr. A. R. Wallace criticizes the phrase “Natural Selection.” “The term ‘Survival of the Fittest,’” he says, “is the plain expression of the fact; ‘Natural Selection’ is a metaphorical expression of it, and to a certain degree indirect and incorrect, since Nature does not so much select special varieties as exterminate the most unfavourable ones.” Mr. Darwin, while admitting with his wonted candour the force of this criticism, urges in support of the use of his own phrase, first, that it can be employed as a substantive governing a verb; secondly, that it serves to connect artificial and natural selection; and thirdly, that its meaning is not obvious, and that this leads men to think the matter out for themselves.
I propose here briefly to consider Mr. Wallace's criticism; to suggest provisionally the use of the phrase, “Natural Elimination,” which can be employed as a substantive “governing a verb”; and to indicate the advantages which would attend the use of such a term, not the least of which is, that it serves to distinguish between artificial selection and “natural selection.”
Mr. Herbert Spencer's term, “Survival of the Fittest,” says Mr. Wallace, is the plain expression of the fact; “Natural Selection” is a metaphorical expression of it. Yes; but in the first place, Mr. Spencer's phrase gives no inkling of the process by which such survival is brought about; and, in the second place, it is questionable whether any phrase, which does so indicate the process, can escape the charge of being in some degree metaphorical. The sting of Mr. Wallace's criticism, therefore, would appear to lie (appropriately) in the tail, where he points out that Nature does not so much select special varieties as exterminate the most unfavourable ones. This seems to me a valid criticism; one which Mr. Darwin does not sufficiently meet; and one which still holds good. I would, however, venture to suggest that the word “eliminate,” though somewhat metaphorical, is more satisfactory than Wallace's word, “exterminate”; and I further venture to suggest that the use of the phrase, Natural Elimination, would emphasize the fact that, whereas in artificial selection it is almost invariably the fittest which are chosen out for survival, it is not so under Nature; the “survival of the fittest” under Nature being in the main the net result of a slow and gradual process of the elimination of the unfit. The well-adapted are not selected; but the ill-adapted are rejected; or rather, the failures are just inevitably eliminated.
This was not the only occasion on which Morgan made these points5, nor he was the only one to consider the matter6, but the term “natural elimination” never caught on. Wallace himself apparently became more aware that his view differed from Darwin's as time passed. He had referred in print to this notion of the removal of the unfit at least as early as 18777; it is not known whether Wallace knew of Morgan's essay, but by 1890, in one of his most famous essays, “Human Selection,” he straightforwardly states: “The survival of the fittest is really the extinction of the unfit8.” In an 1894 interview, he remarks “I believe that the unfit will be gradually eliminated from the race, and human progress secured,”9 and a year later, in “The Method of Organic Evolution,” he writes “Without making some numerical estimate of this kind it is impossible to realize the severity of the struggle continually going on in nature and the resultant “elimination of the unfit.”10
If Wallace believed, and surely he did, that “elimination of the unfit” was what “survival of the fittest” really came down to, why did he bother using the second term at all? The reason seems evident from the following passages from two other late works of his:
Herbert Spencer suggested the term “survival of the fittest,” as more closely representing what actually occurs; and it is undoubtedly this survival, by extermination of the unfit, combined with universally present variation, which brings about that marvellous adaptation to the ever-varying environment…11
This continual weeding out of the less fit, in every generation, and with exceptional severity in recurring adverse seasons, will produce two distinct effects, which require to be clearly distinguished. The first is the preservation of each species in the highest state of adaptation to the conditions of its existence; and, therefore, so long as these conditions remained unchanged, the effect of natural selection is to keep each well-adapted species also unchanged. The second effect is produced whenever the conditions vary, when, taking advantage of the variations continually occurring in all well-adapted and therefore populous species, the same process will slowly but surely bring about complete adaptation to the new conditions. And here another fact—the normal variability of all populous or dominant species, which is seldom realized except by those who have largely and minutely compared the individuals of many species in a state of nature—comes into play. There are some writers who admit all the preceding facts and reasoning, so far as the action of natural selection in weeding out the unfit and thus keeping every species in the highest state of efficiency is concerned, but who deny that it can modify them in such a way as to adapt them to new conditions, because they allege that “the right variations will not always occur at the right time.” This seems a strong and real objection to many of their readers, but to those who have studied the variability of species in nature, it is a mere verbal difficulty dependent on ignorance of the actual facts12.
He thus apparently acknowledged that “elimination of the unfit” per se does not well lend itself to the notion of “adapting” in an evolutionary sense. Yet, while “elimination of the unfit” might only serve to keep species in “the highest state of adaptation,” Wallace could fall back on the understanding that changing conditions are what stimulate the kind of directional selection process leading to evolution. This is where, I believe, Wallace goes wrong. “Changing conditions,” on whatever scale, are themselves a function of evolution (not necessarily just biological ones, of course, but the whole system is integrally interconnected), and cannot merely be assumed. A chicken-or-egg situation has been set out in which the initial conditions of causality have not been specified.
Another way of putting this is to suggest that just as negentropy is not merely the “opposite” of entropy, neither does evolution imply something that is automatically the opposite of “elimination of the unfit.” Evolution of any kind, including biological in particular, implies a movement away from chaos and toward higher levels of order. The thoughts of the late Stephen Jay Gould and others notwithstanding, evolution as witnessed on this planet, and probably universally (even if only locally), is progressive. Whether it is progressive toward some predestined end, as some would suggest, is quite another matter, but one cannot sensibly argue that insects, for example, whatever their numbers and diversity, individually or as a group display responses to impinging stresses that are as advanced as those by vertebrate species. If Wallace—and the rest of us—wish to show how the “non-unfit” are really contributing to evolution, we must show how their (ecological) actions are producing a net increase in the overall information content of the active earth surface layer.
Unfortunately, while we can prove easily enough that evolution really has taken place, it is not so easy to demonstrate that natural selection as usually conceived is responsible for this progression of complexification (both in individual forms, and doubtlessly at the entire environmental level as well). Actually, and even assuming it operates as Darwin envisioned, at least five related causalities (or lack thereof)—and undoubtedly others—can be posed that might, in the absence of contravening forces, stop it in its tracks.
First, and again, what is there in the natural selection concept that actually argues for a process of complexification over time, as opposed to mere change, or even diversification? That is to say, why is the planet not populated by no more than an endless array of microorganisms that merely morph over time into further endless arrays of microorganisms? (And for that matter, just how effective has natural selection been in explaining speciation into discrete population entities?: not very.)
Second, what is there in the logic of the process of natural selection (as opposed to its supposed observed results, that is) that demonstrates that the physical environment is not so fickle and changeable as to present too difficult a challenge for selection to overcome? And there is beyond this the possibility that as that environment itself evolves into wholly new sets of relationships, it could do so in ways that natural selection is powerless to address.
Further, we may be confident at this point that mutations introduce new diversity into the biological system, but can natural selection tell us whether this diversity is of a productive type frequently enough, or even under what circumstances it might be? Perhaps, the rate of mutation is so great, and its usually evil effects so prevalent, that some other force is needed to steer its results in a productive direction.
Perhaps worst of all, is it actually evolutionarily—as opposed to ecologically—productive in all instances to adapt? More specifically, where adaptation results in highly specific ties to various (physical or biological) elements of the environment, what are the long-term downsides to this kind of association? One, of course, is proneness to extinction, but another perhaps further-reaching one is an unlikelihood of further diversification into forms with an ability to enter into substantially new kinds of associations, or indefinitely perpetuating ones. Insects, for all their great number and diversity, have never given rise to any other class of organized beings since they themselves came into existence. Diversification, in mere terms of speciosity, is only one element of evolution, and perhaps not even its defining element.
Finally, and most interesting, what if there are a priori limitations to the nature of complex structure that natural selection must work around to function at all? The DNA molecule, for example, seems to display a rather similar structure all the way up and down the living world, and we have tacitly assumed that the reason for this lies in an unconstrained random-walk-modified-by-negative-feedbacks kind of evolutionary process—just the same assumption we have made regarding the history of emergence of living variety in general. Even if this is to some extent true, there still may well be overarching constraints on the structure of complex systems that create absolute limits to that process, or that push it in certain directions.
And, as if these suppositions were not enough to cause some worries, many years of diligent study by paleontologists have shown that many or most populations in fact do not change in a manner reflecting the basic Darwinian dictum of slow, continual adaptation. We are now aware of many species that have shown little if any alteration for even many tens of millions of years. It appears to be more common that short bursts of innovation take place that push species into new adaptive equilibrium states for varying periods of time. Wallace suspected as much; in 1880 he wrote: “… the extreme slowness of the action of natural selection, on which Mr. Darwin repeatedly dwells, is by no means an essential characteristic of it… if, as must often have happened, conditions have changed with comparative rapidity, then the enormous amount of individual variation, which would be taken advantage of every year by the survival of the fittest, might effect changes in a single century quite as great as those which distinguish nearly allied species13.”
Now understand that this is not to try to suggest that any of these forces necessarily have unduly complicated, or impeded, the evolutionary process. Instead, the point I am trying to make is that in our efforts “to make natural selection work” a lot of potentially interesting irregularities are merely being explained away. The Darwinian approach to natural selection tacitly assumes that all of these possibly extenuating influences must have been overcome—thus, natural selection emerges as a transcendental force that simply supersedes all and any such agencies. Yet, it provides limited insight into how this is accomplished.
Such considerations should make us wary of attempts to conceptualize natural selection as a process model. It may be more fruitful to begin with the unassailable—the facts of super-ample rates of procreation, limited resources, and genetics—and agree with Wallace that natural selection represents no more than the notion of the elimination of the unfit, and its consequence of the “highest state of adaptation to the conditions of its existence; and, therefore, so long as these conditions remained unchanged, the effect of natural selection is to keep each well-adapted species also unchanged14.” This fairly exact starting point allows us to ask without fear of circularity: what conditions surrounding those that do survive are tending to push the overall state of negentropy on the planet's surface to higher levels?
While it is undoubtedly true that there are genetic differences between those individuals in any population that do not survive very long and those that do, it is arguably not these differences per se that drive evolution. Instead, and technically speaking, it is the fact that the second group has a greater opportunity to engage with its environment (defined broadly) in a nonrandom fashion that ultimately drives phylogenesis. So, we are speaking most fundamentally of assembly rules here. On the average, adaptive arrays that better suit ecological conditions (again, physical and/or biological) will more likely be embraced by them, but this is not a tautological statement because the causalities that are coming together are quite distinct in nature. The individual organism, once in existence, is little more than an automaton, programmed by its DNA. The environment, by contrast, is infinitely complex, offering varying and continually changing probabilities of success of engagement over time—and beyond this there is the further complication that such probabilities are spatially autocorrelated: all of them are the more or less so in an actual spatial context. Evolution takes place as this two-way set of relationships works out ever more intricate intercausalities.
I am not alone in thinking that some fresh approaches are in order. Bowler has recently expressed some reservations about the “Darwin industry,” stating: “modern Darwinians may actually benefit from diverting some of their energy to uncovering and making more visible the work of those evolutionists who looked for other ways of trying to explain the development of life on Earth29.” In another recent column, historian and sociologist Stephen Shapin aptly writes:
‘Adaptationists’ take it as securely established that organic change proceeds through the natural selection of individual traits, each of which improves the organism's reproductive chances, that each trait's evolutionary end-point represents an optimum, and that no other process is needed for an evolutionary lineage to move along through time. But adaptationism has distinguished critics within biology departments—Richard Lewontin, Niles Eldredge, and the late Stephen Jay Gould among them—and they have argued that there is a difference between asserting adaptation as a possible means of getting smoothly from evolutionary point A to point B and establishing that this is in fact how organic change has occurred. Maybe there are developmental constraints on how traits change, and change with respect to other traits; maybe some traits are accidental by-products of changes in other traits; maybe evolutionary change is in fact discontinuous; maybe there is a dialectical causal relationship between organisms and the environmental niches to which they ‘adapt’; maybe processes other than adaptation are at work but we just don't know much about them yet. The adaptationist camp includes Dawkins, Dennett, and Pinker—some of the most enthusiastic Darwin Year celebrants. Adaptationists tend to give spectators a misleading picture of the scientific state of play, while at the same time laying claim to a founding father who in fact had reservations about the power and sufficiency of natural selection. There is a struggle among scientists for Darwin's soul. It is understandable that modern evolutionists should configure history as best suits present purposes, but truth in advertising should be part of the exercise30.
Chomsky31, Deacon32, and others, meanwhile, have expressed reservations with the Darwinian approach to the evolution of language. Similar reservations may be found in works regarding other adaptationism-related evolutionary subjects33. Meanwhile, in his study of explanation in Darwinian evolutionary theory Bock34 agrees with me that “Natural selection is better treated as either survival of the fit (i.e., not fittest), or as elimination of the unfit.”
Despite the basically critical nature of my remarks here, I feel that a “demoted” natural selection—Wallace's “elimination of the unfit”—is likely to result in a clearer understanding of how selection promotes an evolutionary agenda. In particular, a greater focus on longer term, larger-scale environmental interdependencies, should invigorate ecological and biogeographical studies, and give us new kinds of insight into those natural processes that have made us who and what we are.