Second, copiousness must also be asserted in the face of a powerful argument about limits to variation following modal departure from “type.” To use Fleeming Jenkin's (1867) famous analogy: a species may be compared to a rigid sphere, with modal morphology of individuals at the center, and limits to variation defined by the surface. So long as individuals lie near the center, variation will be copious in all directions. But if selection brings the mode to the surface, then further variation in the same direction will cease — and evolution will be stymied by an intrinsic limitation upon raw material, even when selection would favor further movement. Evolution, in other words, might consume its own fuel and bring itself to an eventual halt thereby. This potential refutation stood out as especially serious — not only for threatening the creativity of natural selection, but also for challenging the validity of uniformitarian extrapolation as a methodology of research. Darwin responded, as required by logical necessity, that such limits do not exist, and that new spheres of equal radius can be reconstituted around new modes: “No case is on record of a variable being ceasing to be variable under cultivation. Our oldest cultivated plants, such as wheat, still often yield new varieties: our oldest domesticated animals are still capable of rapid improvement or modification” (p. 8).
I cannot here provide a full history for the subsequent odysseys of these key Darwinian precepts. But a few cursory comments indicate how these claims have remained central and contentious throughout the history of post-Darwinian thought, and how they continue to underlie important debates within Darwinism today.
The argument about copiousness, particularly as expressed in the claim for limits to further variability after intense selection, dogged the 19th century [Page 143] literature and emerged as a key issue in the biometrician vs. Mendelian debates early in our century (see Provine, 1971). Castle (1916,1919) pursued his famous experiments on selection in hooded rats in order to test the hypothesis of limits imposed by variability upon continued change. One of the most appealing features of Mendelism — and a strong reason for acceptance following its “rediscovery” in 1900 — lay in the argument that mutation could restore variation “used up” by selection. Nor has the issue abated today. In another form, copiousness underlay the great debate between Dobzhansky and Muller (see Lewontin, 1974) — the classical vs. the balance view in Dobzhansky's terminology. Kimura's (1963, 1983) modern theory of neutralism may be invoked to acknowledge the fact of copiousness while avoiding the pitfalls of genetic load — and therefore becomes “neoclassical” in Lewontin's terminology.
SMALL IN EXTENT. If the variations that yielded evolutionary change were large — producing new major features, or even new taxa in a single step — then natural selection would not disappear as an evolutionary force. Selection would still function in an auxiliary and negative role as headsman — to heap up the hecatomb of the unfit, permit the new saltation to spread among organisms in subsequent generations, and eventually to take over the population. But Darwinism, as a theory of evolutionary change, would perish — for selection would become both subsidiary and negative, and variation itself would emerge as the primary, and truly creative, force of evolution, the source of occasionally lucky saltation. For this reason, and quite properly, saltationist (or macromutational) theories have always been viewed as anti-Darwinian — despite the protestations of de Vries (see Chapter 5), who tried to retain the Darwinian label for his continued support of selection as a negative force. The unthinking, knee-jerk response of many orthodox Darwinians whenever they hear the word “rapid” or the name “Goldschmidt,” testifies to the conceptual power of saltation as a cardinal danger to an entire theoretical edifice.
Darwin held firmly to the credo of small-scale variability as raw material because both poles of his great accomplishment required this proviso. At the methodological pole of using the present and palpable as a basis, by extrapolation, for all evolution, Darwin longed to locate the source of all change in the most ordinary and pervasive phenomenon of small-scale variation among members of a population — Lyell's fundamental uniformitarian principle, recast for biology, that all scales of history must be explained by currently observable causes acting within their current ranges of magnitude and intensity. “I believe mere individual differences suffice for the work,” Darwin writes (p. 102). At the theoretical pole, natural selection can only operate in a creative manner if its cumulating force builds adaptation step by step from an isotropic pool of small-scale variability. If the primary source of evolutionary innovation must be sought in the occasional luck of fortuitous saltations, then internal forces of variation become the creative agents of change, and natural selection can only help to eliminate the unfit after the fit arise by some [Page 144] other process. Darwin, again using domestication as an analog, passionately defends the central role of variation so small as to pass beneath nearly everyone's notice (p. 32):
If selection consisted merely in separating some very distinct variety, and breeding from it, the principle would be so obvious as hardly to be worth notice; but its importance consists in the great effect produced by the accumulation in one direction, during successive generations, of differences absolutely inappreciable by an uneducated eye — differences which I for one have vainly attempted to appreciate. Not one man in a thousand has accuracy of eye and judgment sufficient to become an eminent breeder. If gifted with these qualities, and he studies his subject for years, and devotes his lifetime to it with indomitable perseverance, he will succeed, and may make great improvements; if he wants [that is, lacks] any of these qualities, he will assuredly fail.
Saltational variation has always served as a rallying point for non-Darwinian evolutionary argument (see Chapters 4 and 5 for a full discussion). T. H. Huxley centered his own doubts about natural selection firmly upon Darwin's preference for change by insensible steps. Bateson (1894), in developing the concept of homeosis, and D'Arcy Thompson (1917), in his ideas on non-continuity in certain geometrical transformations, advanced saltation as an explicitly anti-Darwinian argument. The early mutationists read Mendel as a warrant for discontinuous change, and a disproof of strict Darwinism as espoused by the “biometricians.” Goldschmidt (1940; see Gould, 1982a) joined some interesting views on developmental discontinuity to an untenable genetic theory, all the better to espouse a saltationist view that made him the chief whipping boy of the Modern Synthesis.
Reciprocally, Darwinians countered with strong and explicit support. R. A. Fisher began his great book (1930) by rooting a defense of Darwin in a linkage of copiousness with small-scale variation — specifically, by arguing for an inverse correlation of frequency and effect, and then claiming that variations of large effect therefore become too rare to serve as evolution's raw material.
UNDIRECTED. Textbooks of evolution still often refer to variation as “random.” We all recognize this designation as a misnomer, but continue to use the phrase by force of habit. Darwinians have never argued for “random” mutation in the restricted and technical sense of “equally likely in all directions,” as in tossing a die. But our sloppy use of “random” (see Eble, 1999) does capture, at least in a vernacular sense, the essence of the important claim that we do wish to convey — namely, that variation must be unrelated to the direction of evolutionary change; or, more strongly, that nothing about the process of creating raw material biases the pathway of subsequent change in adaptive directions. This fundamental postulate gives Darwinism its “two step” character, the “chance” and “necessity” of Monod's famous formulation — the separation of a source of raw material (mutation, recombination, etc.) from a force of change (natural selection). [Page 145]
In a sense, the specter of directed variability threatens Darwinism even more seriously than any putative failure of the other two postulates. Insufficient variation stalls natural selection; saltation deprives selection of a creative role but still calls upon Darwin's mechanism as a negative force. With d
irected variation, however, natural selection can be bypassed entirely. If adaptive pressures automatically trigger heritable variation in favored directions, then trends can proceed under regimes of random mortality; natural selection, acting as a negative force, can, at most, accelerate the change.
Lamarckism (defined in the modern sense of “soft” heredity) represents the quintessential theory of directed variability. Variation arises with intrinsic bias in adaptive directions either because organisms respond creatively to “felt needs” and pass acquired features directly to their offspring, or because environments induce heritable variation along favored pathways. Other directional theories differ in viewing intrinsic variation as unrelated to adaptation, but still capable of overwhelming any counteracting selection, and therefore setting the path of evolutionary change. Historically important theories in this mode include various notions of orthogenesis that postulate the inevitable origin of hypertrophied and inadaptive structures; and theories of “racial life cycles” that envision an ineluctably aging protoplasm doomed to extinction despite any effort at “rejuvenation” by natural selection. (I shall discuss such ideas in Chapter 5.)
Darwin clearly understood the threat of directed variability to his cardinal postulate of creativity for natural selection. He explicitly restricted the sources of variation to auxiliary roles as providers of raw material, and granted all power over the direction of evolutionary change to natural selection. Drawing his customary analogy to artificial selection, Darwin writes (p. 30): “The key is man's power of accumulative selection: nature gives successive variations; man adds them up in certain directions useful to him. In this sense he may be said to make for himself useful breeds.”
Darwin also understood that variation could not be construed as truly random in the mathematical sense — and that history did not imply or require this strict form of randomness. He recognized biased tendencies to certain states of variation, particularly reversions toward ancestral features. But he viewed such tendencies as weak and easily overcome by selection. Thus, by the proper criterion of relative power and frequency, selection controls the direction of change: “When under nature the conditions of life do change, variations and reversions of character probably do occur; but natural selection, as will hereafter be explained, will determine how far the new characters thus arising shall be preserved” (p. 15).
We may summarize Darwin's third requirement for variation under the rubric of isotropy, a common term in mineralogy (and other sciences) for the concept of a structure or system that exhibits no preferred pathway as a consequence of construction with equal properties in all directions. Darwinian variation must be copious in amount, small in extent, and effectively isotropic. (Think again of a dynamic sphere, with all radii accessible. The modal form lies at the center and may move by selection along any radius. At any new location, a sphere of comparable size may be reconstituted about the altered [Page 146] modal form.) Only under these stringent conditions can natural selection — a force that makes nothing directly, and must rely upon variation for all raw material — be legitimately regarded as creative.
Gradualism
Darwinism, like most comprehensive and complex concepts, defies easy definition. Darwinism cannot be analogized to an object, like the Parthenon, with a clear criterion of membership for each potential slab (whether now resident in the British Museum or in Athens). Moreover, the various propositions of Darwinism cannot be regarded as either independent or of equal force. Darwinism cannot be construed as a deductive system, with some defining axioms and a set of logical entailments tied together like a classical proof in plane geometry. But neither can Darwinism be viewed as a set of separate stones, all of similar size, and each ejectable from a bag without great disturbance to the others.
As discussed at length in Chapter 1 (pp. 12–24), I view the conceptual structure of Darwinism much like the metaphor that Darwin himself first used (see Barrett et al., 1987) for depicting evolution (in the “B Notebook” on transmutation kept during the 1830's) — the “coral of life” (later superseded, in Chapter 4 of the Origin, and in other writings, by the tree of life). The central trunk (the theory of natural selection) cannot be severed, or the creature dies (see Fig. 1-4, p. 18). The first-order branches are also so fundamental that any severing of a complete branch converts the theory into something essentially different that must be newly named. (I have suggested that the theory of natural selection includes three major branches, discussed in sections B-D of this subchapter.) Each major branch then divides into smaller sub-branches. (In the present section C, I argue that the second major branch, the claim for “creativity of natural selection,” divides into three important sub-branches of “requirements for variation,” “gradualism,” and “the adaptationist program.”)
As further argued in Chapter 1, this model allows us to address the important question of dispensability. At some level above the base, we may excise a sub branch, deny its premises, and still consider ourselves Darwinians. I envision the central trunk and first-order branches as indispensable. Along the continuum from necessary to avoidable, we may begin to make selective negations at the level of sub-branches, but not without severe stress to the entire structure. Thus, T. H. Huxley could oppose gradualism and still consider himself a supporter of natural selection (though his approbation remained ambiguous and indifferent at best, and his role as “Darwin's bulldog” rested upon his defense of evolution itself, not his explication of natural selection). And a modern developmental saltationist might call himself a Darwinian, though not without an array of “buts” and qualifications.
One other feature of the model requires explicit commentary. I have chosen a coral in preference to the more conventional tree, because the branches of many corals form a network by lateral anastomoses (while each limb of a tree stands free, and may be chopped off without necessarily affecting the others). [Page 147] The premises of Darwin's theory (the branches and sub-branches of the coral model) are organically connected. One might be able to excise a single branch without killing the others, but some pain and readjustment will certainly be felt throughout the entire structure. The three sub-branches of the “creativity” limb, for example, are strongly conjoined in this manner. If variation forms an isotropic sphere (the expectation of sub-branch one), then change by natural selection can only occur a short step at a time (as predicted by the gradualism of sub-branch two). And if variation imposes no constraint upon the direction of change (an inference from isotropy), then natural selection works freely and adaptation prevails (as required by sub-branch three).
Finally, as so often emphasized throughout this book, we must recognize and embrace natural history as a science of relative frequencies. None of these basic Darwinian premises operates without exception throughout nature. Darwin insisted* — explicitly and vociferously — that natural selection only enjoyed a predominant relative frequency, not exclusivity: “the main but not exclusive means of modification,” as he writes at the close of the introduction (p. 6). Darwin then extended his claim for a predominant relative frequency, but not for exclusivity, to all other sub-branches of his essential argument as well. Failure of raw material might occasionally explain a puzzling absence of evolutionary modification — but lack of selective pressure for change surely represents the more likely explanation for stasis by far. Substantial change might occur as a very rare event, but most alteration must be insensible, even on geological scales: “We see nothing of these slow changes in progress, until the hand of time has marked the long lapse of ages” (p. 84).
Understanding Darwin's mode of justification by relative frequency [Page 148] becomes vitally important because selective quotation represents the most common error made by evolutionists in interpreting his work and theory. The Origin, as a volume of single authorship, maintains a stronger plot line and features fewer inconsistencies than the Bible; but Darwin and the Good Lord do share the common trait of sayi
ng something about nearly everything. Wrenched from context and divorced from a crucial assessment by relative frequency, a Darwinian statement can be found to support almost any position, even the most un-Darwinian.
Since Darwin prevails as the patron saint of our profession, and since everyone wants such a preeminent authority on his side, a lamentable tradition has arisen for appropriating single Darwinian statements as defenses for particular views that either bear no relation to Darwin's own concerns, or that even confute the general tenor of his work. Thus, for example, Darwin wrote extensively about variational constraint, and he maintained great interest in this topic (see Chapter 4). But the logic of his work entails adaptive control of evolutionary change and isotropy of variation as generally prevalent — and Darwin ultimately comes down (as he must) on the side of these necessary underpinnings for natural selection. Proper textual analysis requires that general tenor, not selective statement, be presented. Two basic procedural modes, each with distinctive criteria, set the framework for such textual analysis. The empirical mode makes its judgments of importance by relative frequency and interconnectedness of statements. Meanwhile, and simultaneously, the logical mode employs theoretical consistency as an arbiter for judging the validity and power of the structure of argument. We revere Darwin because he unfailingly manifested the two key traits of brilliance and honesty. He knew where his arguments led, and he followed them relentlessly, however unpleasant the consequences. We do him the greatest possible disservice when we approach his work as a superficial grazer, searching for some particular item of personal sustenance, while ignoring the beauty and power of general tenor and logical entailment.
The Structure of Evolutionary Theory Page 25