The Structure of Evolutionary Theory

by Stephen Jay Gould

  Darwin (loc. cit.) then epitomizes the solution that he named “the principle of divergence” and ranked with natural selection as a foundation of his theory: “The solution, as I believe, is that the modified offspring of all dominant and increasing forms tend to become adapted to many and highly diversified places in the economy of nature.”

  Darwin's principle of divergence has puzzled many biologists: why did Darwin rank the concept so highly, and as a principle separate from natu­ral selection? May we not view divergence as a logical consequence or sim­ple spin-off from natural selection itself? Yet when one considers the issue in Darwin's terms, both his separation of divergence from natural selection, and his joy in resolution, make excellent sense. Natural selection, as formu­lated under the Malthusian insight of 1838, states a principle of anagenetic change within phyletic lines — an argument about adaptation to local cir­cumstances (biotic and abiotic). This principle says nothing, by itself, about diversification, or splitting of one lineage into two or several descendant [Page 226] taxa. So much of what Darwin needed to explain — plenitude in ecology, branching models in phylogeny, the hierarchical structure of taxonomy, to name just a few items of obvious centrality — rested upon the fact of diversi­fication, not adaptation (see Mayr, 1992, on Darwin's several theories of evo­lution).

  One might say — indeed many of us do say, thus leading us to downgrade and misinterpret Darwin's explanation of diversity — that “divergence of character” requires no separate principle beyond adaptation, natural selec­tion, and historical contingency. After all, the earthly stage of evolution pro­vides ecological and biogeographical prerequisites for diversification. Cli­mates alter; topography changes; populations become isolated, and some, adapting to modified environments, form new species. What more do we need? Insofar as Darwin considered the issue at all between 1838 and the early 1850's, his thinking followed this general line (Sulloway, 1979; Ospovat, 1981). But Darwin grew dissatisfied with a theory that featured a general principle to explain adaptation, but then relied upon historical acci­dents of changing environments to resolve diversity. He decided that a fully adequate theory of evolution required an equally strong principle of diversity, one that acted intrinsically and predictably. If adaptation and diversification specify the central phenomena of evolution, each must have its principle, and their union would then define his complete theory.

  (In modern evolutionary parlance, we may relate the growing intensity of Darwin's search for a general, “law-of-nature” explanation of divergence to his changing views about allopatric and sympatric speciation. During the 1840's, when diversity did not greatly trouble him as a theoretical issue, Dar­win tended to view speciation as allopatric, and therefore as a consequence of historical accidents in geography and ecology. When a population becomes spatially isolated, he reasoned, natural selection can act independently upon it, and eventually accumulate enough divergence from the ancestral form to establish a new species. But Darwin's preferences then shifted to sympatric views of speciation — and he therefore developed a conviction that some gen­eral law, and not just historical accidents of isolation, must promote the mul­tiplication of species. A complete theory of natural selection required that this elusive “law” of speciation or divergence also be based on the predictable op­eration of organismic selection. In the light of our current preferences for allopatric speciation, Darwin's shift may seem ironic, but our opinions and certainties, as presently defined, must be deemed irrelevant to such historical analysis.)

  In the context of this book and its principal theme of hierarchical selection, I stress the centrality of Darwin's changing views on divergence because I think that I have made a small discovery about the structure of his argument. I shall try to show that this most brilliant of all theorists, this rigorously hon­est thinker who worked so diligently to explain all evolution as a conse­quence of organismic struggle, tried mightily to render his second touchstone, his “principle of divergence,” by ordinary natural selection — and he failed. He could not succeed because the logic of his argument demands a major role [Page 227] for sorting and selection at the species level — and Darwin, with characteristic honesty, faced his distress head on.

  I am fascinated that the exegetical literature on Darwin's attitude to supra-organismal selection (Ghiselin, 1974; Ruse, 1980, for example) has focused entirely on putative cases of group selection (sterility in plant hybrids; neuter castes in Hymenoptera) and has quite properly concluded that Darwin, with a possible exception for invoking family or clan selection to explain human moral traits, doggedly and consistently carried through his program for the exclusivity of organismic selection (see Chapter 2, pp. 125–137). In so doing, these scholars have missed the one area — the heart of Darwin's argument about diversity — where his logic falters because he needs (but hesitates to em­brace in his distress) the apparatus of species selection. I suspect that the in­ternal problems in this centerpiece of Darwin's thought have not been ad­dressed, or even recognized, because species selection itself did not become a subject of importance (or even an acknowledged subject at all) until recently, while debate about conventional group selection has long raged. Darwin has therefore been well combed for comments about interdemic selection, while his main engagement with supraorganismal selection on species went un­noticed.

  In any case, whatever our attitude or ignorance today, Darwin clearly regarded his solution to the problem of divergence as his second great achieve­ment (after natural selection), and as the capstone to his theory. As Ernst Mayr notes (1985, pp. 759-760): “He referred to it always with great excite­ment, as if it had been a major departure from his previous thinking.” On June 8,1858, Darwin wrote to Hooker after completing his extended discus­sion of the principle of divergence for Chapter 6 of Natural Selection (the “big species book” that would never be completed because Wallace's paper, arriving within 10 days of this letter to Hooker, derailed his leisurely plans and led him to compose the “abstract” (in his own description) that we call The Origin of Species). “I am confined to the sofa with boils,” he begins, “so you must let me write in pencil.” He then goes on to describe “the 'Principle of Divergence,' which, with 'Natural Selection,' is the keystone of my book” (in F. Darwin and Seward, 1903, volume 1, p. 109).

  A year before, in September 1857, Darwin wrote his first complete account of the principle of divergence in a famous letter to Asa Gray at Harvard University. Gray had explicitly asked Darwin for an epitome of his evolution­ary theory (previously revealed only to Darwin's closest confidants, Hooker and Lyell in particular): “It is just such sort of people as I that you have to sat­isfy and convince and I am a very good subject for you to operate on, as I have no prejudice nor prepossessions in favor of any theory at all” (quote in Kohn, 1981, p. 1107). Darwin responded positively with a lucid summary of his theory in six points:

  • The power and effect of artificial selection.

  • The even greater power of natural selection working on all characters at once and over vastly longer spans of time. [Page 228]

  • The operation of natural selection at the organismal level, powered by the Malthusian principle that all species produce far more offspring than can possibly survive.

  • A description of how natural selection works in nature.

  • A defense of gradualism as the solution to standard problems in accept­ing the factuality of evolution.

  • An explication of the principle of divergence.

  This account of the principle of divergence also became the first published version because Lyell and Hooker included this letter to Gray among the documents published in the Linnaean Society's journal for 1858 — the “delicate arrangement” that presented Darwin and Wallace jointly, stressing Darwin's priority but publishing Wallace's paper on the independent discovery of natu­ral selection in toto. Darwin's sixth point neatly summarizes his ideas on di­vergence:

  Another principle, which may be called the principle of
divergence, plays, I believe, an important part in the origin of species. The same spot will support more life if occupied by very diverse forms. We see this in the many generic forms in a square yard of turf, and in the plants or in­sects on any little uniform islet, belonging almost invariably to as many genera and families as species. We can understand the meaning of this fact amongst the higher animals, whose habits we understand. We know that it has been experimentally shown that a plot of land will yield a greater rate if sown with several species and genera of grasses than if sown with only two or three species. Now, every organic being, by prop­agating so rapidly, may be said to be striving its utmost to increase its numbers. So it will be with the offspring of any species after it has be­come diversified into varieties, or sub-species, or true species. And it fol­lows, I think, from the foregoing facts, that the varying offspring of each species will try (only a few will succeed) to seize on as many and as di­verse places in the economy of Nature as possible. Each new variety or species, when formed, will generally take the place of, and thus extermi­nate its less well-fitted parent. This I believe to be the origin of the classi­fication and affinities of organic beings at all times; for organic beings al­ways seem to branch and sub-branch like the limbs of a tree from a common trunk, the flourishing and diverging twigs, destroying the less vigorous — the dead and lost branches rudely representing extinct genera and families (from the 1858 published version, often reprinted, as, for example, in Barrett et al., 1987).

  Darwin continually awarded his principle of divergence the central role specified in this letter to Gray. Nearly half of the key chapter in the Origin of Species (number 4 on “Natural Selection”) treats the principle of divergence, closing with the celebrated metaphor of the tree of life, sketched out at the end of point 6 to Gray. The only figure in the entire Origin of Species occurs in chapter 4. The intent of this famous diagram (reproduced here as Fig. 3-5 on p. 242) has almost always been misunderstood by later commentators. [Page 229] Darwin did not draw this unique diagram simply to illustrate the generality of evolutionary branching, but primarily to explicate the principle of diver­gence.

  After more than a century in limbo, Darwin's principle of divergence has been exhumed and subjected to careful scrutiny by historians of science. No subject in Darwinian studies has been more actively pursued during the past 25 years, and many excellent analyses have been published on the genesis and utility of the principle of divergence (Limoges, 1968; Sulloway, 1979; Browne, 1980; Schweber, 1980, 1985, 1988; Ospovat, 1981; Kohn, 1981, 1985). Therefore, the importance of this principle has finally been recognized. Ospo­vat, for example, writes (1981, pp. 170-171): “Darwin's 'principle of diver­gence' [is] the most important addition to his theory between 1838 and 1959 [sic, for 1859] and the one most intimately associated with the transforma­tion of his theory after 1844.” In all this literature, however, only Schweber has grasped Darwin's difficulties with divergence as an unresolved struggle between levels of explanation. Yet this theme, particularly Darwin's inability to “cash out” his usual argument about organismal struggle at the level of species birth and death, holds, I believe, the key to Darwin's treatment.

  Darwin's argument about divergence begins with an unquestioned premise that strikes us as curious today (for we are immediately tempted to mount a challenge), but resonates with a central theme of Darwin's century — the clear and inherent “good” of maximizing the amount of life in any given region, and the consequent necessity for a cause to insure this natural goal. Maximi­zation, Darwin argues, arises by diversification: the more taxa in a given area (and the more different), the greater the total quantity of life. This theme can be traced to Darwin's earliest “transmutation notebooks” of the 1830's, the primary documents of his quest to formulate evolution: “The end [that is, goal] of formation of species and genera is probably to add to quantum of life possible with certain pre-existing laws — if only one kind of plant not so many” (C Notebook, p. 146 — in Barrett et al., 1987).

  In the fullest discussion within Natural Selection (written in early 1858), Darwin firmly links maximization of life to diversification of taxa: “I con­sider it as of the utmost importance fully to recognize that the amount of life in any country, and still more that the number of modified descendants from a common parent, will in chief part depend on the amount of diversification which they have undergone, so as best to fill as many and as widely different places as possible in the great scheme of nature” (p. 234 of Stauffer edition, 1975).

  Darwin proposes that the vague concept of “amount” or “maximization” of life be quantified chemically as total metabolic flow through a given area in a given time — and he illustrates the primary dependence of this quantity on diversification:

  The fairest measure of the amount of life [is] probably the amount of chemical composition and decomposition within a given period. Imagine the case of an island, peopled with only three or four plants of the same order all well adapted to their conditions of life, and by three or four insects [Page 230] of the same order; the surface of the island would no doubt be pretty well clothed with plants and there would be many individuals of these species and of the few well adapted insects; but assuredly there would be seasons of the year, peculiar and intermediate stations and depths of the soil, decaying organic matter etc., which would not be well searched for food, and the amount of life would be consequently less, than if our island had been stocked with hundreds of forms, belonging to the most diversified orders (ibid., p. 228).

  Darwin then provides examples from agriculture and domestication. Sev­eral varieties of wheat, sown together on a plot, will yield more grain per acre than a monoculture. In one experiment, two species of grass yielded 470 plants per square foot, while a plot of 8 to 20 species produced a thousand plants per square foot (ibid., p. 229): “I presume that it will not be disputed that on a large farm, a greater weight of flesh, bones, and blood could be raised within a given time by keeping cattle, sheep, goats, horses, asses, pigs, rabbits and poultry, than if only cattle had been kept” (ibid., p. 229).

  But why was Darwin so wedded to a principle of maximization that would strike most of us today as both metaphysical and indefensible (ecosystems, af­ter all, can work perfectly well with far fewer species and lower chemical “yield” per spot)? Schweber (1980), I think, has provided the correct answer by stressing Darwin's allegiance to one of the most popular philosophical ap­proaches of his day — the “Benthamite optimization calculus” promoted by Jeremy Bentham, and many other prominent thinkers in several disciplines, as the utilitarian principle in philosophy and political economy, the “greatest good for the greatest number.” William Paley, the intellectual hero of Dar­win's youth (see p. 116), spoke for a utilitarian consensus in writing (quoted in Schweber, 1980, p. 263): “The final view of all rational politics is, to pro­mote the greatest quantity of happiness in a given tract of country ... and the quantity of happiness can only be augmented by increasing the number of percipients or the pleasure of their perceptions.” In other words, make more objects and make them better. Nature achieves this desired maximization and progress by diversifying the number of species in each region of the globe.

  Darwin explicates and defends the maximization of life with his favorite rhetorical device — analogy — and by invoking another fundamental tenet in the political economy of his era: the division of labor. As taxa specialize ever more precisely to definite and restricted roles in local ecologies, more species can be supported (leading to maximization of life as measured by chemical throughput). In a note of September 23, 1856, Darwin drew a direct parallel between diversification in nature and the economic principle of division of la­bor: “The advantage in each group becoming as different as possible, may be compared to the fact that by division of labor most people can be supported in each country.” For the public presentation in the Origin three years later, Darwin retained the centrality of division of labor, but chose a biological analogy drawn from the French
zoologist Henri Milne Edwards (who had, himself, credited Adam Smith and the political economists, and who charac­terized his own view as an extension [Page 231] of their principle):

  The advantage of diversification in the inhabitants of the same region is, in fact, the same as that of the physiological division of labor in the or­gans of the same individual body — a subject so well elucidated by Milne Edwards. No physiologist doubts that a stomach by being adapted to di­gest vegetable matter alone, or flesh alone, draws most nutriment from these substances. So in the general economy of any land, the more widely and perfectly the animals and plants are diversified for different habits of life, so will a greater number of individuals be capable of there support­ing themselves (Darwin, 1859, pp. 115-116).

  Consider the form of the classic argument in Darwin's two analogical sources. Adam Smith began the Wealth of Nations by discussing pinmaking to illustrate the advantages of division of labor. Smith states the basic argu­ment in the very first words of his classic book: “The greatest improvement in the productive powers of labor, and the greater part of the skill, dexterity, and judgment with which it is anywhere directed or applied, seem to have been the effects of the division of labor.” Pinmaking, Smith tells us, may be “a trifling manufacture,” but “18 distinct operations” are still needed to make the final product. If a single worker performed all these tasks, he “certainly could not make twenty” pins in a day, but allocation of separate tasks to 10 people (with some individuals continuing to perform 2 or 3 of the 18 opera­tions) allowed one small factory to make 48,000 pins per day, or 4800 per man. Now who benefits from this division of labor? In part, the workers who hone their skills and participate in the resulting prosperity. But primarily the larger polity — the factory through profits, or society itself in the availability of moderately priced goods. Similarly, in Milne Edwards' physiological divi­sion of labor, the prime beneficiary cannot be the organ (an omnivore's stom­ach works perfectly well qua stomach), but again the larger polity, in this case the organism.