Unofficial SJG Archive

The Unofficial Stephen Jay Gould Archive

Unofficial SJG Archive

The Confusion over Evolution

Review of The Ant and the Peacock by Helena Cronin, The Miner's Canary by Niles Eldredge, and On Methuselah's Trail, by Peter Douglas Ward.

by Stephen Jay Gould

liver Cromwell delivered history's most famous rebuke to the hero-worshiping that irons all subtlety into flawless cardboard:

Mr. Lely, I desire you would use all your skill to paint my picture truly like me, and not flatter me at all; but remark all these roughnesses, pimples, warts, and everything as you see me, otherwise I will never pay a farthing for it.

Helena Cronin, in The Ant and the Peacock, displays a raw talent clearly equal to that of our finest portraitists, but has placed herself into a position even worse than Mr. Lely's. Cromwell's painter at least faced the subject himself; Cronin has produced an uncritical gloss upon a false and simplistic view that never was more than a caricature of Darwinian theory.

As its most deliciously radical component, Darwin's original theory proposed a causal mechanism for evolution by natural selection among organisms struggling for personal reproductive success—and nothing else. Consider the impact of this cleansing upon the older tradition of natural theology—the creationist principle that sought to prove not only God's existence, but also his attributes of power and goodness, from the excellent design of organisms and the intrinsic harmony of ecosystems. Darwin acknowledged these aspects of nature, but labeled them as sequelae, or side consequences, of the only causal force operating in evolutionary change: organisms struggling for themselves alone. Quite a contrast: up from below in the "selfish" interest of organisms vs. down from above as directly imposed by a wise creator.

Inevitably, I suppose, Darwin's success in pulling down the level of causality from an overarching God to a struggle among organisms led some evolutionists to explore a kind of ultimate reductionism in viewing genes themselves as the struggling units, and organisms as mere vehicles constructed for their machinations. Under such a view, called "gene selectionism," nature's truly causal competition takes place among different forms of a gene, each "struggling" to leave more copies of its own version in future generations of a population. In classical Darwinism, organisms struggle for reproductive success. (If, for example, short plants are favored by natural selection, then the runts in Mendel's pea patch produce more surviving offspring, per individual and on average, than the tall plants.) In gene selectionism, the plants are passive vehicles and the struggle occurs among genes. (If you can dredge up your high school biology, you will remember that T and t ["big t" and "little t" even in biological jargon] are different forms [called alleles] of a gene at a chromosomal position [called a locus] influencing the height of the resulting pea plants. Under gene selectionism, little t is struggling with big t to leave more copies of itself in the next generation. Selection is then viewed as working for little t alleles, not for short plants.)

Several of my colleagues toyed with this formulation during the 1970s, while Richard Dawkins provided a popular version in his book The Selfish Gene (1976). This hyper-Darwinian reductionism (and pervasive adaptationism, though from the gene's point of view) contained some interesting ideas and made a stir within the field. But gene selectionism—as a hard causal claim rather than a colorful metaphor—also received sharp and devastating criticism both from biologists and philosophers.[1] Even Richard Dawkins backed away in his next book (The Extended Phenotype, 1982), which opened with the fatal concession that natural selection among genes and ordinary Darwinian selection among organisms may be viewed as equally valid modes of description for the same causal phenomenon. (This stunning admission of relativism flatly contradicted Dawkins's previous claim for true and exclusive causality at the genic level.)

Helena Cronin, a philosopher by original profession, has gathered much interesting material in The Ant and the Peacock, but her book suffers grievously from the curious and vociferously advocated scheme that she has chosen as her vehicle of presentation. In short, she has somehow received the impression that genic selectionism has accomplished the greatest revolution since Darwin and has swept away all opposition within the field (she proclaims "revolution" as often as Marx or Thomas Kuhn, and labels the new orthodoxy "modern Darwinism").

Now I freely confess my own strong preference for the other side of this debate—for a model that views selection as operating simultaneously at several levels of a genealogical hierarchy including genes, organisms, local populations, and species. In other words, I argue that no natural entity can properly be described as the exclusive "unit of selection"—as Cronin and Dawkins would claim for genes, and classical Darwinians for organisms. Nature is organized as a hierarchy—genes in organisms, organisms in populations, and populations in species. Entities at each level of the hierarchy can act as biological "individuals," and Darwin's process of selection can therefore occur at all levels, with none dominant in all situations. Genes may "struggle" for increased representation in the gene pool of a population, but species may also "struggle" for increased membership of their branches in the "species pool" of an evolutionary lineage.

But whatever one's personal inclinations, no one can deny the sociological fact that relatively few experts accept the theory of near exclusivity for gene selection, and no amount of blithe verbal assurance about the validity of the theory can convert it into a successful revolution. Most of my colleagues continue to defend Darwin's view that selection works nearly exclusively on organisms.

For Cronin, ants and peacocks are synecdoches for two great issues mentioned in her subtitle—altruism, epitomized by the behavior of ants in their communities, and sexual selection, the alleged raison d'être of the peacock's flamboyant and burdensome tail. In Cronin's view both altruism and sexual selection are explained by the theory of selfish genes; and I agree that the gene's perspective has been useful in dealing with these two substantial problems. But I shall argue that the peacock only needed classical Darwinism to account for its tail, while the key question evoked by the ant's altruism has not been resolved. If the approach of gene selectionism is false, then Cronin's title makes little sense and all her fascinating flowers of insight (primarily on the differences between Darwin and Wallace) languish in barren soil.

This attempt to validate gene selectionism by applying it to ants and peacocks fails for three main reasons (which I consider in turn in the rest of this review): 1) the general theory is bankrupt; 2) the two chosen examples form a false and disparate pairing that either does not need or does not fully illustrate the theory; 3) the theory, even if valid in its own limited realm (which it is not), cannot serve as a paradigm for all, or even much, that evolutionary theory must explain. The fine books of Ward and Eldredge illustrate why this is so.

Fallacy of the General Theory

Since Darwinism is a theory about differential reproductive success ("survival of the fittest" in the old cliché of limited utility), and since organisms are plainly doing the struggling and reproducing "out there" in nature, why would anyone want to relocate the action at the level of genes encased within these organisms? This question engages a central issue in Darwinian theory: On what kind of object does natural selection work? What, in short, is a "unit of selection"? Cronin gives her answer in no uncertain terms:

So when is an "adaptive unit" really an adaptive unit? When is a category that's seen by us, seen by nature, too? The answer must be: When it's a unit that selection can work on. For classical Darwinism this would have been difficult to specify precisely. But for modern Darwinism, a unit is obviously a gene and the ramifying tree of all its phenotypic effects [by "phenotypic effects," she means the manifest characteristics of the organism including its anatomy, etc.].

But if gene selectionism is so self-evidently true, why hasn't it swept the field, smiting all opposition before it? In a remarkable passage, Cronin admits the stubborn persistence of alternative interpretations, but brands them as obtuse because she so clearly grasps the true logic of genuine Darwinism—and it says what she says it says, period.

Let me forestall the mutterings of disagreement that can already be heard in the background. By no means all modern Darwinians would accept my characterisation. But I am dealing with the theory, not with how individuals have chosen to interpret it. One must distinguish between the fundamental tenets of a theory (what the theory actually says) and how it is viewed by some practitioners (what is said about it). I am dealing with the former.

Cronin's confidence arises from her misuse of an important distinction between "replicators" and "interactors" made by the philosopher of science David Hull and others. Natural selection is a theory of "differential reproductive success"; therefore, according to one school of thought followed by Cronin, only natural objects that replicate themselves faithfully can be units of selection. For if an object doesn't replicate itself faithfully, then it cannot be a reliable transmitter of the characteristics that make for superior reproductive success. Now an organism, the traditional "unit of selection" in Darwinism, fails by this criterion because, in sexual reproduction, offspring contain only half the genes of each parent. What good is a replicator that dilutes itself by half in each generation?

The genes themselves, on the other hand, replicate faithfully (except for rare mutation) into future generations. A fecund organism is passing copies of its genes, not its body, into the next generation. Under this view, genes are replicators, while bodies are, in a sense, their servants. Bodies interact with the environment and engage in the "struggle for existence" via differential reproductive success. Bodies are interactors (Richard Dawkins prefers the more loaded and almost pejorative term "vehicles"); genes are replicators. Therefore, only genes are units of selection. Cronin remarks.

Genes, then, can be replicators whereas organisms, groups and other levels of the hierarchy cannot. Natural selection is about the differential survival of replicators. So genes are the only serious candidates for units of selection.

This superficially attractive argument collapses from two major fallacies. First, it is simply not true that only genes replicate with adequate faithfulness. I accept the point that sexual reproduction dilutes the integrity of organisms in replication. But adequate replication returns at higher levels of the hierarchy—populations and species—because splitting at these levels is analogous to asexual reproduction. For example, species split into daughter species that resemble their parental populations far more than any other (descendant dogs are more like ancestral wolves than like any other species). Species are therefore good replicators, and some evolutionary lineages can be more successful than others because their species give rise to more successful branches.

Second, the replicator criterion is at best insufficient, and at worst entirely mistaken. A simple appeal to vernacular usage tells us that a lower unit (a gene, for example) can't be an exclusive agent if all the action occurs at higher levels (organisms, for example)—and the properties that generate this action are "emergent" characters of the higher level—that is, not a simple summation of features built by the lower units (genes).[2] Now, manifestly (and gene selectionists do not deny this), organisms are primary objects struggling for reproductive success in nature. How, then, can "hidden" genes be the true agents if organisms are doing the fighting, cooperating, generating, and dying? Gene selectionists respond that all the relevant properties of organisms can be described as results of the various genes involved in their construction. Such properties, the argument continues, are therefore only the complex manifestation of genetic action.

But many, undoubtedly most, properties of organisms are not simple summations of contributions from several genes. They are products of interactions among genes and therefore they cannot, in principle, be adequately predicted or known at the level of genes. Since selection acts on such emergent properties of organisms, genes cannot be exclusive units of selection.

Moreover, emergence occurs frequently at all levels of biological organization. Selection acts simultaneously on all levels of nature's hierarchy—on genes (Cronin's "exclusive" level), on cell lineages, on organisms (Darwin's "nearly exclusive" level), on local populations, and on species. Our intellectual task as evolutionary biologists is to determine the relative importance and complex interactions of these levels. Claims for theoretical exclusivity of one chosen level are false and blinkering.

Why have some scientists been attracted to exclusive gene selectionism in the light of these criticisms? I believe that the appeal of the idea rests upon a central fallacy, one embraced by Cronin: the confusion of bookkeeping with causality. Gene selectionists have correctly noted, but fundamentally misinterpreted, an important property of evolving systems: all evolution by selection, whatever its level of causation, is recorded by change in the frequencies of genes (the lowest level of the causal hierarchy). Since genes record all changes, some evolutionists have been fooled into assuming that genes therefore cause all changes. But scribes are not agents, and bookkeeping is not causality.

This recording of all change by genes reflects a general property of hierarchies, not a statement about the locus of causality. Disturb a hierarchy at any level, and all units at that level and below must be shuffled—while higher-level units may be unaffected. For example, suppose that the lineage of cats once contained two groups of five species each. They compete entirely at the level of species selection and, 10 million years later, all species in group A are eliminated, while group B has flourished and now contains fifteen species. The genetic makeup of the entire lineage has altered as a result (for species in group A had different genes in different proportions from species in group B)—but no causal process has operated at the gene level.

But the obverse does not hold: lower-level impacts on genes need not affect higher-level units at all. For example, some genes may increase their number of copies within organisms by genic selection alone—but organisms need not "notice" and need not be affected in any way.[3] Now this asymmetry in hierarchies—upper-level disturbances felt at all lower levels, but lower-level impacts potentially invisible to higher-level units—makes the lowest level an attractive place for bookkeeping, because all changes, whatever their causal locus, are recorded there.

Bookkeepers are slighted in our metaphors as mere scribes and recorders of action occurring elsewhere. What magnificent revenge the error of gene selectionism must promise them! For their ledgers—the tables of changes in genetic composition—have been misread by gene selectionists as the fundamental cause of life's history. But revenge based on error is both short and ultimately frustrating, for the deprecatory metaphor turns out to be true in this case.

Fallacies of Cronin's Particular Arguments

Cronin's entire book promotes what I like to call the Senator Aiken strategy for untenable positions. This fine legislator once proposed a wonderfully simple solution for the morass of our military involvement in Vietnam: Why don't we simply declare victory and get out! Cronin does much the same. She proclaims victory, dogmatically and vociferously, over and over again, for the gene-selectionist version of strict adaptationism ("modern Darwinism" in her neologism). In one remarkable passage she even tells us that Darwinism has triumphed on other unknown planets because evolution can work in no other way!

We have seen why Darwinism was in 1859, and still is, the best explanation of why living things are as they are—not only, it turns out, on this planet, but in any world that resembles ours in several fundamental respects.

In essence, Aiken's strategy must mask failure with a claim for triumph. How then does Cronin manage to defend such a flawed and discredited approach as pure adaptationism from the gene's point of view? She snatches rhetorical victory from the jaws of defeat by a series of false arguments and uncritical assertions. I give examples in just a few categories:

1) False or misleadingly incomplete citation of empirical data. To support her panadaptationist world view, the belief that virtually all heritable changes in organisms are the result of adaptation, Cronin tells several classical tales of natural history as triumphs of selection (when the actual story is far more complex and ambiguous). For example, she cites color banding in the land snail Cepaea as "just one example of natural selection rescuing phenomena from the explanatory clutches of genetic drift."[4] (Genetic drift refers to a random process of increase or decrease in the frequencies of genes in populations. Suppose that only ten individuals exist in a species of beetles, and that three of them carry a favorable gene subject to positive Darwinian selection. An elephant rambles by and squashes half the beetles, including [by chance] all three with the favorable gene [which is now randomly eliminated from the population, despite its Darwinian value].)

Now A.J. Cain and others demonstrated the power of selection (based on visual discrimination among differently banded snails by predatory birds in different habitats) where drift had previously been assumed—and this work was a genuine triumph for Darwinism. But Cronin never mentions the second chapter of this story—Cain's unsuccessful attempts to explain so-called area effects (abrupt changes in banding types from one region to another, but correlated with no evident change in habitat) by selection based upon "cryptic environmental differences." Most snail workers (I am one) now regard area effects as nonadaptive vestiges of former historical movements of populations and habitats.[5]

2) Relegation of powerful and important exceptions to peripheries. Cronin admits the vital principle that "some side effects of adaptations, which become positively useful when conditions change, are until then just lying around dormant." But she cautions against overuse of this principle: "Such arguments, unless they are applied with discrimination, could end up peppering the world with a multitude of characteristics that have no Darwinian purpose (even though they eventually get put to good use)." But the world is so peppered—and this seasoning is a fundamental (and nonadaptive) feature of evolution. In fact, Cronin actually admits the primary example in the very next sentence—features in the human brain, arising as nonadaptive sequelae of its computing power, as in our ability to read and write—and then buries the subject without further commentary.

3) Mis-citation of critics. Cronin quotes a line from me, for example, and delights in her discovery: "If we are programmed to be what we are, then these traits are ineluctable. We may, at best, channel them, but we cannot change them, either by will, education, or culture." She then makes the following sarcastic comment, assuming that these words, from an article I wrote in 1978, represent my own view. "That's die-hard intransigence for you! But, actually, those quotes come not from some ardent proponent of an all-in-our-genes view but from Stephen Gould, a voluble critic of selfish gene-ery in general and of its application to humans in particular." I will admit to writing with less than optimal clarity on occasion, but there can't be much doubt that in this passage I was characterizing my opponents' views, not my own. Earlier, in the very paragraph Cronin quotes, I labeled this view as "a crude biological determinism." Of course the words convey "die-hard intransigence"—for they are my description, my caricature I will even admit, of the opposition.

4) Ignoring opponents. As I have noted, the pure gene selectionism championed by Cronin is a marginal position among evolutionists (this, of course, doesn't make it wrong). Yet Cronin falsely depicts this view as a consensus. She performs this astonishing turnabout by simply not discussing, usually not even mentioning at all, the numerous and devastatingly effective critiques that invalidated gene selectionism after its brief run of incipient popularity in the 1970s (see my first footnote).

If Cronin's general account of gene selectionism is so awry, then the chosen examples (ant and peacock), and attendant problems (altruism and sexual selection), don't fit together either, for even well-crafted pictures may jar when juxtaposed in a single false frame. She claims that both are classical problems of old-style Darwinism (selection on organisms), now triumphantly solved by the modern gene-selectionist version.

In epitome, the peacock's tale (also tail) is a story of delayed vindication for selectionism. Darwin developed an ancillary mechanism, which he called "sexual selection," to explain competition among members of the same species for access to reproduction, in contrast with the usual form of "natural selection," or competition for limited resources to sustain life. (Darwin developed the term and concept in The Origin of Species [1859], but covered the subject most thoroughly in his 1871 treatise on The Descent of Man and Selection in Relation to Sex—a work often read only for its short and speculative thoughts on human evolution, but, in the main, a long and copiously documented treatise on sexual selection throughout the animal kingdom.)

Darwin delineated two modes of sexual selection, called "male competition" and "female choice." In male competition—e.g., among antlered deer—males fight like hell and the winners get the females. In female choice males strut and preen, display and bellow, and females choose to mate with the individuals that impress them most. Peacocks, in other words, do not evolve their showy tails for direct victory in battle over other males, but to win a beauty contest run by females.

Male competition never sparked any controversy, for it looks so much like good old natural selection. What does it matter if two male deer fight for access to food or to females? They still need good weapons and nature remains red in tooth and claw. (I usually avoid this clichéd line from In Memoriam; but 1992 is the one hundredth anniversary of Tennyson's death, so I make an exception.) Female choice, however, elicited a firestorm of criticism. Most of Darwin's contemporaries rejected the concept, often vehemently. It was similarly ignored, and curiously so, throughout the early excitement in twentieth-century studies of animal behavior. Neither Julian Huxley nor the German ethologists had any use for the idea. But female choice has roared back to acceptability and prominence during the past twenty years—and I certainly agree with Cronin that this reversion to Darwin's original concept represents one of the most important contemporary themes in evolutionary theory.

But I strongly disagree that gene selectionism lies behind this renaissance; hence, this half of Cronin's book, while full of insight and interesting documentation, does not support or illustrate her argument. I think that she has fallen into the classic error of equating correlation with causality. It is true that gene selectionism had its fling in the 1970s and that sexual selection began its renaissance at the same time. But, during the same years, Watergate unfolded and The Godfather won an Academy Award—and I really don't think that these coincident events are causally related either.

You don't need gene selectionism to validate female choice; plain old Darwinian selection on organisms works perfectly well (as Darwin himself recognized in establishing the concept): females, in choosing the most healthy and vigorous males, are bolstering their personal reproductive success—the essence of the Darwinian game.

If female choice did not need gene selectionism, then why did its vindication occur so recently? When this interesting history is sorted out, I believe that the record will show a renaissance based primarily on the removal of two longstanding impediments (both mentioned by Cronin, but treated as incidental), rather than the emergence of any new (and ultimately fallacious) theory such as gene selectionism.

Disrespect for the cognitive capacity of nonhuman animals formed the first impediment: Male competition is just "doin' what comes naturally," but female choice requires an additional mental step that seemed too close to cognitive abilities supposedly unique to humans: that is, females must survey a field and make a judgment based on some aesthetic criterion of beauty in sight or sound. Most biologists weren't willing to grant such capacity to animals. Now we know better, but the insight was a long time coming.

The second impediment arose from an unwillingness to place females in the driver's seat of evolutionary change. Again, male competition just represents the big boys in ordinary control, but female choice argues that males go to enormous lengths of adornment and posturing—all to await the judgment of females. Like nearly every science, evolutionary biology was almost entirely a male preserve until this generation. You don't have to be an active sexist to ignore female choice in such a male-dominated world. You may be the kindest male on earth and still fall prey to a social and intellectual atmosphere that doesn't include the concept of females in such control. (Sometimes, however, the source of bias is more overt. In a line cited by Cronin, the prominent British biologist and Darwinian opponent St. George Mivart proclaimed: "Such is the instability of a vicious feminine caprice, that no constancy of coloration could be produced by its selective action.")

I don't mean to sound like a mouthpiece of contemporary political correctness, but I do feel that the delay in acceptability for Darwin's well-formulated concept of female choice lies in the social impediments of sexism and speciesism. And I suspect that this concept's recent rise to prominence largely reflects the social and political questioning of such biases, as well as the most important and salutary sociological shift in recent science: the entrance of so many women into the profession.

If the peacock doesn't fit into Cronin's chosen setting of gene selectionism because the problem has indeed been solved, although not by her particular approach, then the issue of the ant (altruism) is quite different—for the ant does fit, but the problem has not been solved. Ants and other social insects produce mostly sterile, though genetically female, offspring—the "soldiers" and "workers" of hives and hills. But how can such sterility evolve if the Darwinian game is fundamentally about personal reproductive success? (Evolutionary biologists define altruism in this limited and operational sense as behavior that decreases one's own reproductive potential in the service of others. The sterility of worker ants may represent an extreme example, but animal behavior is rife with other cases that merely endanger an altruist for the apparent benefit of others—warning calls issued by birds who sight a predator, for example. Thus, the problem of altruism, so defined, has been central in Darwinian theory.)

On this issue, I agree with Cronin up to a point, and I greatly appreciate her incisive treatment. A solution to the problem of altruism has provided the greatest success for viewing evolution from the gene's point of view, while directly departing from Darwin's own focus on organisms. The key insight, usually called "kin selection theory," was provided by W.D. Hamilton in the mid-1960s, though many hints and half-formulations can be found in earlier literature.

What is the "individual reproductive success" of which Darwin speaks? It cannot be the passage of one's body into the next generation—for, truly, you can't take it with you in this sense above all! "Reproductive success" can only mean the passage of more copies of one's own genes into future generations. Such success is usually best achieved by bearing a maximal number of surviving offspring oneself—hence the usual Darwinian struggle for personal reproduction. Usually, but not always. We share, on average, a certain percentage of genes with our relatives, depending on closeness—one half with each of our parents and full sibs, one fourth with our grandchildren and half-sibs, one eighth with our first cousins.

Now suppose that I am in a position where I can either die to save three full sibs or survive at the cost of their death. What should I do in the Darwinian calculus? Die for the three sibs, of course, for they represent, in sum, 150 percent of my genes, while I hold only 100 percent. Better for my genes if I go in order to let three of them live to reproduce. My act may look altruistic from the organism's point of view, but it is properly selfish and Darwinian from the gene's perspective. In short, the theory of kin selection explains apparent acts of sacrifice as evolved Darwinian adaptations in the cardinal interest of passing more copies of one's genes to future generations.

The model is powerful because it suggests an eminently testable research program: study the context of altruistic acts and see if they are performed for the benefit of enough close relatives to overbalance, through fecundity of kin, any individual loss of reproductive success. The model has been tested and confirmed in a wide variety of cases, including sterility in social insects—as among ants, where the sterile females known as workers forgo their own reproduction to help their mother, the queen, raise fertile sisters.

But we now come to the crucial, if admittedly parochial, limit. We are primarily interested in the problem of altruism because human beings seem so singularly capable of behavior in the apparent interest of others. Manifestly, this behavior is frequently not directed toward close relatives (especially since we don't choose to describe sacrificial acts between parents and children as altruistic)—and therefore can't be encompassed by the gene-centered argument of kin selection. Biologists may choose an operational redefinition of the vernacular word "altruism" as apparent sacrifice for actual genetic good, but this concept does not apply to most human acts deserving the word (and one might even argue that the vernacular notion demands no hidden selfishness at any level).

One might reply that the introduction of vernacular human altruism into the argument is unfair. After all, if gene selectionism has been successful for ants and other animals, then grant the victory and leave us out of it (for the professional enlightenment would still be great, even if the subject then failed to touch popular interest in our own condition). But Protagoras was apparently right (even if he only spoke for half of us) when he proclaimed that "man is the measure of all things," and few writers for general audiences can resist the temptation of trying to extend their perspective to this greatest prize of all. The longest chapter in Cronin's book is titled: "Human altruism: A natural kind?"

How then might the acknowledged success of gene selectionism be useful to us in understanding human altruism? Several approaches have been tried, and none have succeeded. One might argue, as Robert Trivers and others have, that the calculus of kin selection won't work, but that a different kind of selfish and adaptive advantage arises through the old principle of "favor banking." If I am perceived as a good altruist through acts that help nonrelatives, then other people are more likely to help me when I am in need—so called "reciprocal altruism." Fine, but we scarcely need Darwinism, or genetic arguments at all, to convince us that humans are smart enough to figure out the advantages of "you scratch my back and I'll scratch yours."

Or we might argue, as Cronin often suggests, that our general altruistic urges evolved long ago by kin selection among small groups of relatives, where neighbors were invariably kin, and the evolutionary rule of "be nice to those close by" would suffice to guarantee the Darwinian calculus. True altruism to nonrelatives would then be a consequence of formerly advantageous behavior, now altered by a changing social setting that makes neighbors of genetic strangers. I find this argument unattractive on two grounds. It is, first of all, an untestable speculation about unrecoverable behavior patterns of distant ancestors. Second, historical origin and current status represent entirely different problems in evolutionary biology. So what if the historical origin of altruism were adaptive via kin selection? If we still do it, after centuries of contexts unfavorable to the Darwinian calculus, then altruism is a currently non-adaptive behavior (in the narrow Darwinian sense) demanding some other explanation, presumably social rather than directly biological.

In sum, the ant and the peacock are apples and oranges. Gene selectionism neither unites the problems nor resolves the issue. We don't require gene selection for the peacock, for Darwin resolved this problem within his system of selection on organisms, though we needed another century to dissolve social barriers impeding the acceptance of his answer. Gene selectionism has been useful in explaining many examples of what we call "altruism" in nonhuman animals (including ants), but it cannot resolve the vernacular human style that remains our ethical glory and our intellectual burden. The ant and the peacock don't belong together, and Cronin's book is incoherent (in the literal, not the pejorative, sense). The problems of sexual selection and altruism are as disparate as the outward appearances of Cronin's chosen synecdoches—ants and peacocks.

The Strictly Limited Domain of Adaptationism, Whether Gene or Organism Based

In praising the power of selection, Cronin writes:

The general point has been to illustrate how resourceful and subtle a tactician natural selection can be…. Once this is appreciated, non-adaptive explanations cannot be treated as other than a last resort. And resolute adaptationists can be confident that "The use of each trifling detail of structure is far from a barren search to those who believe in natural selection." [The last line is a quotation from Darwin's 1862 book on orchids.]

Such confident effusions exemplify two crucial errors: the false claim that selection dominates the domain of organic form, and the flawed inference that this supposed domination provides, by extension, an adequate account of evolution at all scales.

I have argued that gene selectionism is an ultimately incorrect view of evolutionary mechanics. But suppose it were right. Would gene selectionism then be the fully comprehensive theory of biological change that its advocates tout so vociferously? As a paleontologist, working with changes in units of millions of years rather than generations, I find this strange assertion to be the most blinkered and untenable in the entire catalog of strict Darwinian parochialisms.

Darwin himself relied crucially on such an extrapolative vision: smoothly extend the adaptive struggles of generations across millions of years in geological time, and you will obtain the entire, wondrously ramified tree of life. Consider two famous passages from the Origin of Species:

It may be said that natural selection is daily and hourly scrutinizing, throughout the world, every variation, even the slightest; rejecting that which is bad, preserving and adding up all that is good; silently and insensibly working, whatever and wherever opportunity offers, at the improvement of each organic being in relation to its organic and inorganic conditions of life. We see nothing of these slow changes in progress until the hand of time has marked the long lapse of ages.

The inhabitants of each successive period in the world's history have beaten their predecessors in the race for life, and are, in so far, higher in the scale of nature; and this may account for that vague yet ill-defined sentiment, felt by many paleontologists, that organization on the whole has progressed.

If this uniformitarian vision of extrapolation fails, then we must conclude that while adaptationism may control immediate changes in the overt forms of organisms, it cannot render evolution at other scales. The main excitement in evolutionary theory during the past twenty years has not been—as Cronin would have us believe—the shoring up of Darwinism in its limited realm (by gene selectionism or any other patching device), but rather the documentation of the reasons why Darwin's crucial requirement for extrapolation has failed. Selectionism is not a general model for evolutionary change at most scales.

In the world below organisms, at the scale of changes in nucleotides of the DNA code, Motoo Kimura's theory of neutralism (based on the prevalence of genetic drift, as defined earlier), combined with a better understanding of genetic mechanisms, has demonstrated the neutrality of much, if not most, alteration at minimal magnitude. Selectionists often respond, as Cronin does, that their Darwinian preferences are not thereby compromised because such neutral genetic changes do not alter the external forms of organisms, and therefore couldn't be "seen" by natural selection anyway. Cronin writes: "[Kimura's] theory also assumes that chance is an evolutionary force but it is to do with changes at the molecular level that have no phenotypic effects, not evolution in the sense that we are concerned with—adaptive change." But how can you dismiss a process that probably accounts for more than 50 percent of all genetic change by noting that such alterations don't manifest themselves at the level that happens to interest you most? This special interest, after all, is just a parochialism based on human sizes and lifetimes, and on the history of our thinking. Nature, working at so many other scales, takes scant notice and plays no favorites. If we lived in the world of nucleotides, we would see the random ebb and flux as fundamental and view occasional islands of adaptive coagulation at larger scales as peculiar exceptions in an alien domain.

But the ultimate failure of Cronin's adaptationism, as a general evolutionary model, appears most clearly when we consider the paleontological record. Darwin's vision may prevail in the here and now of immediate adaptive struggles. But if we cannot extend the small changes thereby produced into the grandeur of geological time to yield the full tree of life, then Darwin's domain is a limited corner of evolutionary explanation. New documentation on the rapidity and intensity of mass extinction (including the event that wiped out dinosaurs) has provided the strongest argument for rejecting Darwinian extrapolation. Darwin clearly understood the threat, and he struggled against the implications of mass extinction in the Origin of Species by trying to deny both their extent and rapidity. He endeavored to spread them out in time and diminish their effects. He attempted to render them as an intensification of ordinary competition (inspired, perhaps, by an increase in rates of change for conventional processes like mountain-building and change in sea level). But if mass extinctions are true breaks in continuity, if the slow building of adaptation in normal times does not extend into predicted success across mass extinction boundaries, then extrapolationism fails and adaptationism succumbs.

The Permian extinction (about 225 million years ago) may have wiped out 95 percent of marine invertebrate species. The Cretaceous extinction (about 65 million years ago) was probably set off by the impact of a large extraterrestrial body. The adaptive struggles of millions of previous years, whatever their intensity and the beauty of their results, could not prepare organisms for a random catastrophe. A fish honed to hydrodynamic perfection will still die if the pond dries up. Survival through mass extinction requires the good luck of evolving features for one reason in normal times, and then finding them fortuitously well-suited for survival through unanticipated catastrophe.

Two of my colleagues, Peter Ward and Niles Eldredge, have recently written short and incisive books on mass extinction. Taken together, this pair provides a fine documentation for why Darwinian selection cannot, by extrapolation, encompass the history of life. The books differ greatly in both content and intent. Ward's On Methuselah's Trail is a personal account of the fieldwork that convinced him about the catastrophic character of mass extinctions, particularly the event that occurred at the end of the Cretaceous period. Eldredge's The Miner's Canary strongly doubts scenarios of extraterrestrial impact and focuses on similarities between mass dyings of the past and the current human assault upon biodiversity (hence the metaphorical title, invoking the organic side of our chief industrial symbol for harbingers of death by environmental poisoning). Both books recognize the special and dominant character of mass extinctions as agents that changed the pattern of the history of life.

Consider just one example, supreme in its parochial importance—for I wouldn't be writing and you wouldn't be reading otherwise. Why did mammals survive, but dinosaurs die, in the great Cretaceous extinction, an event almost surely triggered by extraterrestrial impact? The adaptationist and extrapolationist model strives to render such a turnover as intensification of a process already underway in previous normal times—the growing domination of mammals as a result of their success in ordinary Darwinian competition against inferior dinosaurs. But such a comfortable argument cannot hold. Mammals emerged at about the same time as dinosaurs. Mammals lived for more than 100 million years in the interstices of a world dominated by much larger dinosaurs; they made no "progress" against these massive incumbents; no Mesozoic mammal was much larger than a rat. (By contrast, the so-called "age of mammals" since the death of dinosaurs has so far spanned only 65 million years.) The Cretaceous catastrophe removed dinosaurs, but mammals survived and inherited an emptied world—and they surely made the most of it.

If the comet or asteroid had not struck, I suppose that dinosaurs would probably still be in command (why not; they had prevailed for far longer against mammals, and mammals had been making no inroads). Mammals, if they survived at all, would probably still be small creatures no larger than rats, and small size precludes self-conscious intelligence. Dinosaurs were not moving toward higher cognition in our form, and probably could not do so. Thus you must thank the extraterrestrial impact for this copy of the New York Review.

But why did mammals prevail and dinosaurs die? Doesn't this fact point to some intrinsic mammalian superiority? Not necessarily. We do not know the answer, but here is one plausible scenario for a partial explanation: the rules change in mass extinction, and adaptive advantages of the past may become dangerous deficits. Large populations provide a good hedge against extinction, all other things being equal. Dinosaurs, with their massive bodies, must have maintained species of small population size. The world must contain far fewer elephants than ants, far fewer brontosauruses than mouse-sized mammals. So perhaps mammals gained a crucial edge by large populations maintained as a consequence of small body sizes.

Now why were mammals small? Surely not because they knew that a comet would hit 10 million years down the road, and that large populations would then be useful. Presumably they were small for a negative reason in Darwin's immediate world of competition: because dinosaurs had usurped the ecological space of large terrestrial vertebrates, and relegated mammals to a periphery. Yet the reasons for relative failure in normal times may translate fortuitously to the crucial ingredient of success in prevailing through a mass extinction. The Darwinian struggle does not extrapolate to the tree of life.

Ironically, Cronin does seem to grasp this issue in her final paragraph, if only through a glass most darkly. After four hundred pages of panadaptationism, she finally recognizes that evolutionary theory must solve other problems as well—particularly the issue of shifting diversity through time—and that adaptation may not provide the basis for all answers. Darwin did wrestle brilliantly and triumphantly with the problem of adaptation, but he had limited success with the issue of diversity—even though he titled his book with reference to his relative failure: the origin of species. Cronin records and admits this irony in the last line of her book: "But, in the midst of such success, there was one problem that remained just outside his [Darwin's] grasp. It was—poignantly—the problem of the origin of species." When strict Darwinians drop their reliance on adaptation and extrapolation, and when they break bread with paleontologists in the different realm of time in millions, they will then engage this unresolved problem face to face.


  1. See especially E. Sober's The Nature of Selection (MIT Press, 1984), E. Sober and R. C. Lewontin, "Artifact, Cause and Genic Selection," Philosophy of Science, Vol. 49, pp. 157–180; E. Lloyd, The Structure and Confirmation of Evolutionary Theory (Greenwood Press, 1988); and P. Godfrey-Smith and R. C. Lewontin's forthcoming "The Dimensions of Selection," Philosophy of Science.

  2. "Emergence" is a complex and contentious subject, with a long pedigree, in both the philosophical and biological literature. I use the term here in the narrow technical (virtually statistical) sense. A feature is emergent at any level if its construction requires nonadditive interaction among the factors and components that build it. In other words, if I can make a larger-scale entity D by just adding components A, B, and C together, then nothing about D is emergent—and D can be explained by reduction to its components. But if the building of D requires interactions among A, B, and C that are not inherent in the components considered separately, and cannot be predicted from knowing A, B, and C alone, then D has emergent features and cannot be explained by reduction to its component parts. Organisms clearly have emergent properties, since their features of anatomy, physiology, and behavior are products of complex and nonadditive genetic and environmental interactions—and not the summation of genes considered separately. Therefore, selection operating on organisms cannot be reduced to selection upon genes, and the "gene selectionism" of Cronin's self-proclaimed "modern Darwinism" fails.

    Incidentally, the concept of emergence helps us to understand why the nature-nurture issue is such a false dichotomy. Genes influence many aspects of human behavior, but we cannot say that such behavior is caused by genes in any direct way. We cannot even claim that a given behavior is, say, 40 percent genetic and 60 percent environmental, and thereby defend at least a partial old-fashioned genetic determinism. Genes and environment interact in a nonadditive way, yielding emergent features in the resulting anatomies, physiologies, and behaviors.

  3. The best example of legitimate gene selection may be provided by a phenomenon known as "selfish DNA." Some genes can make copies of themselves, and these copies may then move to other locations among the chromosomes (so-called transposons, or "jumping genes"). This process constitutes positive selection for these genes at their own level, since the process augments the number of copies of these genes among the chromosomes of an individual—just as ordinary Darwinian selection on organisms increases the number of offspring of favored individuals within a population. But the organism need not "notice" as the copies of selfish DNA increase, for these additional copies are often without function. In fact, gene selection can be most effective when organisms do not "notice" the increase—for if the increase of genetic copies impedes the organism in any way, negative selection from the ordinary Darwinian level of organisms may bring the process to a halt.

  4. Cronin gives away her biases (and any pretense of balanced argument) in such rhetorical flourishes. Why is genetic drift an "explanatory clutch"? The phenomenon is perfectly respectable and powerful, if not entirely applicable to Cepaea. In other giveaway passages, we learn that "nonadaptive explanations cannot be treated as other than a last resort." (Why? They are also permissible in theory and robustly present in nature.) When Darwin strays from the selectionist straight and narrow, his words "need to be interpreted more generously" so that our chief icon may continue to spearhead the strict and uncompromising version of his theory. (Again, why? Darwin was not a pure selectionist.) When Wallace departs from selectionist principles, "he has a lot to answer for." (But what is his sin?) We learn that Darwin "lets us down" when he proposes group selection for human moral conduct (a proper exception to his general orthodoxy of selection on organisms). When, among the founders of population geneticists, Fisher and Haldane make some invalid statements about group selection, they are excused because they were true Darwinians at heart. But when Sewall Wright, third member of the trinity, speaks in the same vein, he is not exonerated, for he truly believed in a form of group selection. Cronin writes: "I did not include the other major founding father of modern Darwinism, Sewall Wright, among the honorable exceptions." (Now Cronin, Dawkins, and me, bundled all together, couldn't fill Sewall Wright's left pocket insofar as intellectual power is concerned—and it is simply unseemly for any of us to speak of his views in terms of honor or dishonor.)

  5. See S.J. Gould and D.S. Woodruff in "History as a Cause of Area Effects: An Illustration from Cerion on Great Inagua, Bahamas," Biological Journal of the Linnean Society, 1990, Vol. 40, pp. 67–98.

[ Stephen Jay Gould, "The Confusion over Evolution," The New York Review of Books, November 19, 1992, pp. 47-54. ]

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