The Structure of Evolutionary Theory

by Stephen Jay Gould

  This conflation came easily (and probably unconsciously) to Darwin, in large part because gradualism stood prior to natural selection in the core of his beliefs about the nature of things. Natural selection exemplified gradualism, [Page 155] not vice versa — and the various forms of gradualism converged to a sin­gle, coordinated view of life that extended its compass far beyond natural se­lection and even evolution itself. This situation inspired Huxley's frustration as he remonstrated with Darwin (see the famous quote on p. 151): you will have enough trouble convincing people about natural selection; why do you insist upon uniting this theory with an unnecessary and, by the way, false claim for gradualism?

  We can best sense this overarching Darwinian conviction in a lovely pas­sage that conflates all three senses of gradualism — the rationalist argument against creationism, the validation of natural selection by insensible intermediacy, and the slow pace of change at geological scales — all in the context of Darwin's homage to his guru Lyell, and his aesthetic and ethical convic­tions about the superiority of these “noble views” about natural causation and the nature of change:

  I am well aware that this doctrine of natural selection ... is open to the same objections which were at first urged against Sir Charles Lyell's no­ble views on “the modern changes of the earth, as illustrative of geol­ogy;” but we now very seldom hear the action, for instance, of the coast-waves, called a trifling and insignificant cause, when applied to the exca­vation of gigantic valleys or to the formation of the longest lines of in­land cliffs. Natural selection can act only by the preservation and accu­mulation of infinitesimally small inherited modifications, each profitable to the preserved being; and as modern geology has almost banished such views as the excavation of a great valley by a single diluvial wave, so will natural selection, if it be a true principle, banish the belief in the contin­ued creation of new organic beings, or of any great and sudden modifica­tion in their structure (pp. 95-96).

  The adaptationist program

  Darwin's three constraints on the nature of variation form a single conceptual thrust: variation only serves as a prerequisite, a source of raw material in­capable of imparting direction or generating evolutionary change by itself. Gradualism, in the second meaning of insensible intermediacy, then guaran­tees that the positive force of modification proceeds step by tiny step. There­fore, the explanation of evolution must reside in specifying the causes of change under two conditions that logically entail a primary focus on adapta­tion as a canonical result: we know the general nature of change (gradual­ism), and we have eliminated an internal source from variation itself (the ar­gument for isotropy). Change must therefore arise by interaction between external conditions (both biotic and abiotic) and the equipotential raw mate­rial of variation. Such gradual adjustment of one to the other must yield ad­aptation as a primary outcome.

  Adaptational results flow logically from the mechanisms defining all other subbranches on the limb of Darwinism designated here as the “creativity of natural selection.” But Darwin constructed this limb in reverse order in the [Page 156] psychological development of his theory. For he had long viewed an explana­tion of adaptation as the chief requirement of evolutionary theory. He sought the causes of evolution within his patrimony — the English tradition in natural theology — and he attempted to subvert this patrimony from within by ac­cepting its chief empirical postulate of good design and then providing an in­verted theoretical explanation (see p. 125).

  When Darwin permits himself to make one of his rare forays into lyrical prose, we can grasp more fully (and dramatically) the extent of his feelings and the depth of his conviction. Consider the following passage on why the basic results of evolution and variation teach us so little about the origin of species, and why an understanding of mechanism requires an explanation of adaptation:

  But the mere existence of individual variability and of some few well-marked varieties, though necessary as the foundation for the work, helps us but little in understanding how species arise in nature. How have all those exquisite adaptations of one part of the organization to another part, and to the conditions of life, and of one distinct organic being to another being, been perfected? We see these beautiful co-adaptations most plainly in the woodpecker and missletoe; and only a little less plainly in the humblest parasite which clings to the hairs of a quadruped or feathers of a bird; in the structure of the beetle which dives through the water; in the plumed seed which is wafted by the gentlest breeze; in short, we see beautiful adaptations everywhere and in every part of the organic world (pp. 60-61).

  Pursuing the theme of rare Darwinian lyricism as a guide to what he viewed as essential, consider his convictions about the overwhelming power of natural selection — a point that he usually conveyed by comparison with the limitations of artificial selection in breeding and agriculture:

  Man can act only on external and visible characters: nature cares noth­ing for appearances, except in so far as they may be useful to any being. She can act on every internal organ, on every shade of constitutional dif­ference, on the whole machinery of life. Man selects only for his own good; Nature only for that of the being which she tends. Every selected character is fully exercised by her; and the being is placed under well-suited conditions of life. Man keeps the natives of many climates in the same country; he seldom exercises each selected character in some pecu­liar and fitting manner; he feeds a long and a short beaked pigeon on the same food; he does not exercise a long-backed or long-legged quadruped in any peculiar manner; he exposes sheep with long and short wool to the same climate. He does not allow the most vigorous males to struggle for the females. He does not rigidly destroy all inferior animals, but pro­tects during each varying season, as far as lies in his power, all his pro­ductions... Under nature, the slightest difference of structure or consti­tution may well turn the nicely balanced scale in the struggle for life [Page 157] and so be preserved. How fleeting are the wishes and efforts of man! how short his time! and consequently how poor will his products be, compared with those accumulated by nature during whole geological pe­riods. Can we wonder, then, that nature's productions should be far “truer” in character than man's productions; that they should be in­finitely better adapted to the most complex conditions of life, and should plainly bear the stamp of far higher workmanship? (pp. 83-84).

  But Darwin's world also differs strongly from Paley's, and the outcome of natural selection, however great the power of Darwin's mechanism, cannot be perfection, but only improvement to a point of competitive superiority in local circumstances. Natural selection operates as a principle of “better than,” not as a doctrine of perfection: “Natural selection tends only to make each organic being as perfect as, or slightly more perfect than, the other in­habitants of the same country with which it has to struggle for existence” (p. 201). Thus, the signs of history will not be erased; creatures will retain sig­natures of their past as quirks, oddities and imperfections (see pp. 111-116 on methodology). Natural selection will fashion the organic world, while leaving enough signs of her previous handiwork to reveal a forming presence.

  I have called this section “the adaptationist program,” rather than, simply, “adaptation” because Darwin presents a protocol for actual research, not just an abstract conceptual structure. The relevant arguments may be ordered in various ways, but consider this sequence:

  • Adaptation is the central phenomenon of evolution, and the key to any understanding of mechanisms.

  • Natural selection crafts adaptation.

  • Natural selection maintains an overwhelmingly predominant relative frequency as a cause of adaptation. Variation only provides raw material, and cannot do the work unaided.

  Adaptation may be viewed as a problem of transforming environmental (external) information into internal changes of form, physiology and behav­ior. Two forces other than natural selection might play such a role — the cre­ative response of organisms to felt needs with inheritan
ce of acquired charac­ters (Lamarck's system), or direct impress of environments upon organisms, also with inheritance of traits thus acquired (a system often associated with Geoffroy Saint-Hilaire). Darwin regards both alternatives as true causes, and he explicitly contrasts them with natural selection in several passages within the Origin. But, in these statements and elsewhere, he always grants natural selection the cardinal role by virtue of relative frequency — “by far the pre­dominant Power,” he writes on page 43, in upper case for emphasis. “Over all other causes of change, I am convinced that Natural Selection is para­mount” (in Natural Selection, 1975 edition, p. 223).

  In this light, how should evolutionists proceed if they wish to discover the mechanisms of change? Should they study the causes of variation (a vitally important issue, but unresolvable in Darwin's time, and not the cause of [Page 158] change in any case)? Or should they examine the large-scale phenomena of taxonomic order or geographic distribution (issues of great import again, but lying too far from immediate causation)? Instead, the best strategy, Darwin asserts, lies in the study of adaptation, for adaptation is the direct and pri­mary result of natural selection; and the relative frequency of selection stands so high that almost any adaptation will record its forming power.

  Adaptation therefore becomes, for Darwin, the primary subject for practi­cal study of evolutionary mechanisms. Recall the basic methodological prob­lem of a science of history (see p. 102): science aims, above all, to understand causal processes; past processes cannot be observed in principle; we must therefore learn about past causes by making inferences from preserved re­sults. Adaptation is the common and coordinating result of nearly any epi­sode of non-trivial evolutionary change. Adaptation not only pervades nature with an overwhelming relative frequency, but also embodies the immediate action of the primary cause of change — natural selection. The adaptations of organisms therefore constitute the bread and butter objects of study in evolu­tionary biology. Our first order approach to change must pose the following question in any particular case: what adaptive value can we assign; how did natural selection work in this instance? In a revealing statement, Darwin rolls all exceptions, all ifs and buts, into a set of subsidiaries to adaptation forged by natural selection — as either consequences of adaptation, inherited marks of older adaptations, or rare products of other processes: “Hence every detail of structure in every living creature (making some little allowance for the di­rect action of physical conditions) may be viewed, either as having been of special use to some ancestral form or as being now of special use to the descendants of this form — either directly, or indirectly through the complex laws of growth” (p. 200).

  The primary anti-Darwinian argument of late 19th century biology pro­ceeded by denying a creative role to natural selection — but Darwin countered with a strong riposte. If adaptation pervades nature and must be constructed by natural selection, and if the steps of evolutionary sequences are generally so tiny that we may seek their source in palpable events subject to our direct view and manipulation, then we not only gain a theoretical explanation for evolutionary change. We also obtain the practical gift of a workable research program rooted in the observable and the resolvable.

  But nothing so precious comes without a price, or without consequences. Darwin's argument works; no logical holes remain. But the research program thus entailed must embody attitudes and assumptions not necessarily true — or at least not necessarily valid at sufficiently high relative frequency to make the world exclusively, or even primarily, Darwinian. To accept Darwin's full argument about the creativity of natural selection, one must buy into an en­tire conceptual world — a world where externalities direct, and internalities supply raw material but impose no serious constraint upon change; a world where the functional impetus for change comes first and the structural alter­ation of form can only follow. The creativity of natural selection makes adap­tation central, isotropy of variation necessary, and gradualism pervasive. [Page 159]

  But suppose these precepts do not govern a commanding relative frequency of cases? What if adaptation does not always record the primacy of natural selection, but often arises as secondary fine tuning of structures arising in other ways? What if variation imposes strong constraints and supplies pow­erful channels of preferred direction for change? What if the nature of varia­tion (particularly as expressed in development) often produces change with­out insensible intermediacy?

  All these arguments merge into a structuralist critique that seriously challenges the predominant functionalism of classical Darwinism. As a common thread, these challenges deny exclusivity to natural selection as the agent of creativity, and claim a high relative frequency of control by internal factors. McCosh was right in establishing his pre-evolutionary contrast of a “princi­ple of order” and a “principle of special adaptation” (see p. 116). Darwin was right in translating this distinction into evolutionary terms as “Unity of Type” and “Conditions of Existence,” though he was probably wrong in his fateful decision — the basis of Darwinian functionalism — to yoke the two cat­egories together under a common cause by defining unity of type as the his­torical legacy of previous adaptation, thus asserting the domination of natu­ral selection (1859, p. 206 — see extensive commentary in chapter 4). And E. S. Russell (1916) was also right in contrasting the “formal or transcenden­tal” with the “functional or synthetic” approach to morphology.

  We are children of Darwin, and an English school of adaptation and functionalism far older than evolutionary theory. Darwin's key claim for the creativity of natural selection — and the resulting sequelae of gradualism, adaptationism, and the isotropy of variation — builds the main line of defense for this powerful and venerable attitude towards nature and change. For many of us, these claims lie too close to the core of our deeply assimilated and now largely unconscious beliefs to be challenged, or even overtly recognized as something potentially disputable. Yet a coherent alternative has been pro­posed, and now provides one of the three most trenchant modern critiques of strict Darwinism. I believe that these critiques, taken together, will reorient evolutionary theory into a richer structure with a Darwinian core. But we cannot appreciate the alternatives until we grasp the basis of orthodoxy as an argument of compelling brilliance and power. Important critiques can only operate against great orthodoxies.

  THE THIRD THEME: THE UNIFORMITARIAN NEED TO

  EXTRAPOLATE; ENVIRONMENT AS ENABLER OF CHANGE

  The first two themes — causal focus on organisms as agents of selection and creativity of selection in crafting adaptation — establish the biological core of Darwinian theory. That is, they perform the biological “work” needed to as­sure the third and last essential component of a Darwinian worldview: the uniformitarian argument for full application in extrapolation to all scales and times in the history of life. Mere operation in the microevolutionary here and now cannot suffice. Natural selection must also assert a vigorous claim for [Page 160] preeminence throughout the 3.5 billion years of phylogeny, lest the theory be reduced to an ornamental device, imposing only a fillip of immediate adap­tive detail upon a grand pageant generated by other causes and forces.

  Darwin, who fledged professionally as a geologist (the subject of his first three scientific books in the 1840's, on coral reefs, volcanic islands, and the geology of South America), and who regarded Charles Lyell as his intellectual hero, while embracing his mentor's doctrine of uniformitarianism as the core of his own philosophy as well, fully understood that his revolution would succeed only if he could show how natural selection might act as architect for the full panoply of life's history throughout geological time. The “method­ological pole,” one of the two foci of Darwin's revolution (see Section II of this chapter), brilliantly develops a set of procedures for defending extrapola­tion in various contexts of limited evidence.

  The link of the first two themes (agency and efficacy) to this third theme of extended scope or capacity — thus forming in their
threefold ensemble a minimally complete statement of revolution — received succinct expression in Ernst Mayr's (1963, p. 586) epitome of Darwinism as preached by the Mod­ern Synthesis: “All evolution is due to the accumulation of small genetic changes, guided by natural selection [the first two themes of agency and efficacy], and that transpecific evolution [the third theme of scope, or uniformitarian extension] is nothing but an extrapolation and magnification of the events that take place within populations and species.”

  In this book, my explicit discussion for this third theme of extrapolation (Chapters 6 and 12) shall be shorter than my treatment of the first theme of agency (Chapters 3 and 8–9), leading from Darwin's nearly exclusive focus on the organismal level to the modern revision of hierarchical selection the­ory, and the second theme of efficacy (Chapters 4–5 and 10–11) on older and modern critiques of panadaptationism, with an emphasis on structural prin­ciples and constraints. I allocate my attention in this unequal manner because the first two themes already include, within themselves, the biological argu­ments for extrapolation, as embodied in Darwin's uniformitarian beliefs and practices. For my explicit and separate treatment of the crucial extrapolationist theme in this work, I therefore follow a different strategy, if only to avoid redundancy in a book that we all undoubtedly regard, author and read­ers alike, as quite long enough already! I will not rehearse Darwin's biological arguments for extrapolation, but will rather, as a “place holder” of sorts, concentrate upon the nature of the geological stage that must welcome Dar­win's biological play.