The Structure of Evolutionary Theory

by Stephen Jay Gould

  To explain these discontinuities, Simpson relied, in part, upon the classical argument of an imperfect fossil record. But he also conceded that such a prominent pattern could not be interpreted as entirely artificial — and he rec­ognized that his favored process of gradualistic Darwinian selection in the phyletic mode would not provide a full explanation. He therefore proposed his book's only major departure from explanations based upon selection lead­ing directly to adaptation — and thus, in his most striking and original contri­bution, framed the hypothesis of quantum evolution.

  Simpson clearly took great pride in this novel theory, for he ended his book with a twelve-page defense of quantum evolution, identified as “perhaps the most important outcome of this investigation, but also the most controversial and hypothetical” (p. 206). Faced with the prospect of abandoning strict se­lection in the gradual, phyletic mode, he framed a hypothesis that adhered rigidly to his more important goal — the proviso that macroevolution must be rendered by genetical models and mechanisms operating within species, and amenable to study in living populations. Thus, he focused upon the only ma­jor phenomenon in the literature of population genetics that permitted a mechanism other than selection to serve as a basis for directional change — Sewall Wright's genetic drift.

  He envisaged major transitions as occurring within small populations (where drift might be effective and preservation in the fossil record virtually inconceivable). He chose the phrase “quantum evolution” because he con­ceived the process as an “all-or-none reaction” (p. 199) propelling a small population across an “inadaptive phase” — explicitly so named — from one stable adaptive peak to another. Since selection could not initiate this depar­ture from an ancestral peak, he called upon drift to carry the population into an unstable intermediary position, where it must either die, retreat, or be drawn rapidly by selection to a new stable position. Simpson felt that, with quantum evolution, he had carried his consistency argument to completion by showing that genetical models could encompass the most resistant and mysterious of all evolutionary events — the rapid origin of novel phenotypes at high taxonomic levels. Quantum evolution, he wrote, is “believed to be the dominant and most essential process in the origin of taxonomic units of relatively high rank, such as families, orders, and classes. It is believed to include circumstances that explain the mystery that hovers over the origins of such major groups” (p. 206). Simpson could, therefore, conclude: “The materials for evolution and the factors inducing and directing it are also believed to be the same at all levels and to differ in mega-evolution only in combination and in intensity” (p. 124).

  Simpson's emphasis on quantum evolution underscores a central feature of his explanatory preferences in 1944 — his pluralistic view of evolutionary mechanisms. He wished to render all of macroevolution as the potential con­sequence of microevolutionary processes, not to rely dogmatically upon any [Page 530] single process. Although he favored selection leading to adaptation as a pri­mary theme, he explicitly denied that all evolution could be adaptive and un­der selective control. He concluded: “The aspects of tempo and mode that have now been discussed give little support to the extreme dictum that all evolution is primarily adaptive. Selection is a truly creative force and not solely negative in action. It is one of the crucial determinants of evolution, al­though under special circumstances it may be ineffective, and the rise of char­acters indifferent or even opposed to selection is explicable and does not con­tradict this usually decisive influence” (1944, p. 180).

  When pressured for a new edition of Tempo and Mode, Simpson realized that evolutionary theory had developed too much in the intervening ten years to permit a reissue or even a simple revision. The field that he pioneered had stabilized and flourished: “It was [in the late 1930s] to me a new and exciting idea to try to apply population genetics to interpretation of the fossil record and conversely to check the broader validity of genetical theory and to extend its field by means of the fossil record. That idea is now a commonplace” (1953, p. ix). Thus, Simpson followed the outline of Tempo and Mode, but wrote a new book more than double the length of its ancestor — The Major Features of Evolution, published in 1953.

  The two books differ in many ways (see p. 522 for my personal and professional introduction to the distinctions), most notably in Simpson's increasing confidence that selection within phyletic lineages must represent the only important cause of substantial change. Consider the following addition to the 1953 book, a speculative comment on trends in titanothere horns, with its prompt dismissal — tinged with impatience, if not incipient dogmatism — of the venerable argument that no evident function can be ascribed to the incipi­ent stages of useful structures: “This long seemed an extremely forceful argu­ment, but now it can be dismissed with little serious discussion. If a trend is advantageous at any point, even its earliest stages have some advantage. Thus if an animal butts others with its head, as titanotheres surely did, the slightest thickening as presage of later horns already reduced danger of fractures by however small an amount” (p. 270).

  But the most dramatic difference between the two books lies in Simpson's demotion to insignificance of the concept that had formerly been, by his own reckoning and explicit announcement, his delight and greatest pride — quan­tum evolution. This hypothesis embodied the pluralism of his original ap­proach — a reliance on a range of genetical models. For he had advocated ge­netic drift to propel small populations off adaptive peaks into an ultimately untenable inadaptive phase. And he had explicitly christened quantum evolu­tion as a mode different in kind, not only in rate, from phyletic transforma­tion within lineages. But now, as the adaptationist program of the Synthesis hardened, Simpson decided that genetic drift could not trigger any major evo­lutionary event: “Genetic drift is certainly not involved in all or in most ori­gins of higher categories, even of very high categories such as classes or phyla” (p. 355).

  In an “intermediate stage” of his personal ontogeny — his presentation to [Page 531] the Princeton conference on genetics, paleontology and evolution — Simpson (1949, p. 224) had emphasized the dominance of selection in quantum evolu­tion, while not denying other factors. But by 1953, he had completed his per­sonal transition. Quantum evolution now merits only four pages in an en­larged final chapter on modes of evolution. More importantly, this concept has now mutated to a meaning that Simpson had explicitly denied before: merely a name for phyletic evolution when the process operates at a maximal rate — an evolutionary tempo differing only in degree from the leisurely, grad­ual transformation of populations in ordinary geological time. Quantum evo­lution, he now writes, “is not a different sort of evolution from phyletic evo­lution, or even a distinctly different element of the total phylogenetic pattern. It is a special, more or less extreme and limiting case of phyletic evolution” (p. 389). He lists quantum evolution as one category among the four styles of phyletic evolution (p. 385) — with all four characterized by “the continuous maintenance of adaptation.” The bold hypothesis (1944) of an absolutely inadaptive phase has been replaced by the semantic notion of a relatively inadaptive phase (an intermediary stage inferior in design to either the ances­tral or the descendant Bauplan). But relative inadaptation poses no threat to the adaptationist paradigm. Even the strictest Darwinian will feel no Angst if the fit of phenotype to environment decreases for an intermediate form in a new habitat, relative to the ancestor in a different original place; (the two forms, after all, cannot directly compete). Even less Angst will then accom­pany an acknowledgment that this intermediate form may be less well de­signed than its own future descendant (for selection should engender increas­ing adaptation through time, especially as a population adjusts to a strikingly new environment). In short, such relatively inadaptive populations can only be regarded as adequately adapted to their own environments at their own time (unsubjected, as they must be, to competition with better adapted ances­tors in a different habitat, or with improved future desc
endants in this new world). Quantum evolution, by linguistic redefinition, therefore moves com­fortably under the umbrella of the adaptationist program. Simpson now even suggests that quantum evolution may be more rigidly controlled by selection than any other mode of evolution (though he still invokes inadaptation for the initial trigger): “Indeed the relatively rapid change in such a shift is more rigidly adaptive than are slower phases of phyletic change, for the direction and the rate of change result from strong selection pressure once the thresh­old is crossed” (p. 391).

  MAYR AT THE INCEPTION (1942) AND CODIFICATION (1963):

  SHIFTING FROM THE “GENETIC CONSISTENCY” TO THE “ADAPTATIONIST” PARADIGM

  If we consider the synthesis as a fusion of three equally robust disciplines — experimental genetics, population genetics, and studies of natural history ex­pressed primarily by systematics (and not as an imposition of the first two, as modernisms, upon a hidebound, or even moribund, third mode of study) — [Page 532] then the role played by Mayr and other field naturalists in building the syn­thesis becomes fully constitutive and not only derivative. Mayr (1980), wear­ing his historian's hat, has strongly defended such an account of the Synthesis against the reductionist tradition that regards genetics as paramount, and the second phase of the Synthesis largely as a whipping of older disciplines into line. I do not deny Mayr's partisan motives in advancing this interpretation, but I also concur with his judgment.

  Dobzhansky, as argued above, became the beacon of the second phase because he represented the only tradition, Russian genetics, that tried to fuse experimental Mendelism with systematics and natural history, rather than im­posing the first upon the second (or ignoring the second entirely). At Mayr's 1974 conference, Dobzhansky vividly recalled the impediments to synthe­sis within American traditions. He had originally left Russia to work with Thomas Hunt Morgan, America's premier experimental geneticist. Dobzhan­sky recalled Morgan's attitude to natural history:

  “Naturalist” was a word almost of contempt with him, the antonym of “scientist.” Yet Morgan himself was an excellent naturalist, not only knowing animals and plants but aesthetically enjoying them . . . Morgan was profoundly skeptical about species as biological and evolutionary realities. The species problem simply did not interest him... Biology had to be strictly reductionistic. Biological phenomena had to be ex­plained in terms of chemistry and physics. Morgan himself knew little chemistry, but the less he knew the more he was fascinated by the powers he believed chemistry to possess. There was no surer way to impress him than to talk about biological phenomena in ostensibly chemical terms (1980, p. 446).

  Morgan, Dobzhansky also remembered, “liked to say that genetics can be studied without any reference to evolution.” Could the Synthesis have taken root in such soil?

  Dobzhansky brilliantly set a different task for evolutionary theory — an enterprise embodied in Darwin's title (but not treated as a major theme in his book), and emerging from traditions of systematics and natural history (while scarcely conceivable for someone with Morgan's, and to a large ex­tent Darwin's, views on the unreality of species): how can a theory originally constructed to describe continuous change in natural populations also ex­plain the discontinuous structure of nature's taxonomic diversity? The central problem of evolution, Dobzhansky asserted, is the origin of discontinuity among species.

  This statement sounds commonplace today, but only because Dobzhansky and the Synthesis moved the question to center stage. Morgan and virtually all experimentalists had argued that the origin and nature of variation, and its manner of spread through populations, defined the key issues in evolutionary theory. Morgan disavowed the species problem as, at best, a hang-up of dull taxonomists and, at worst, a bogus issue because species have no reality in [Page 533] the flow of nature. (We name species, under this view, only because our poor minds can't handle continuity.)

  Dobzhansky didn't deny the importance of Morgan's questions. But he argued that evolution operates on a series of levels, and that the primary gaze of natural history must not be focused upon these lower levels, but upon the broader phenomenon of the origin of species itself (Darwin's title, after all). Diversity represents the primary fact of nature (and the first topic of chapter 1 in Dobzhansky's book). Diversity arises by the splitting of lineages — that is by speciation. Speciation produces discontinuity in nature. How can a continu­ous process of genetic change yield such bounded separations? The origin of discontinuities between species must therefore be recast as the key problem in evolutionary theory. Only a naturalist (better yet, a trained systematist) could have reset the stage for synthesis in such a fruitful way.

  The origin of hereditary variations is, however, only a part of the mechanism of evolution... These variations may be compared with building materials, but the presence of an unlimited supply of materials does not in itself give assurance that a building is going to be constructed ... Mu­tations and chromosomal changes are constantly arising at a finite rate, presumably in all organisms. But in nature we do not find a single greatly variable population of living beings which becomes more and more vari­able as time goes on; instead, the organic world is segregated into more than a million separate species, each of which possesses its own limited supply of variability which it does not share with the others... The ori­gin of species . . . constitutes a problem which is logically distinct from that of the origin of hereditary variation (Dobzhansky, 1937, p. 119).

  Mayr (1942) then furthered Dobzhansky's program by dedicating an entire book to modes of speciation, and to realigning taxonomic practice with in­sights of the developing Synthesis. He even formulated his title in conscious parallel to Dobzhansky's (while both, of course, also claim and honor Dar­win) — and as a manifesto for the centrality of his field: Systematics and the Origin of Species. Mayr's first paragraph (1942, p. 3) sets his theme and tone:

  The rise of genetics during the first thirty years of this century had a rather unfortunate effect on the prestige of systematics. The spectacular success of experimental work in unraveling the principles of inheritance and the obvious applicability of these results in explaining evolution have tended to push systematics into the background. There was a ten­dency among laboratory workers to think rather contemptuously of the museum man, who spent his time counting hairs or drawing bristles, and whose final aim seemed to be merely the correct naming of his speci­mens. A welcome improvement in the mutual understanding between ge­neticists and systematists has occurred in recent years.

  Mayr (1942) follows the characteristic pluralism of the early synthesis in listing all valid evolutionary principles that can explain the data of systemat­ics. His major aim therefore follows the program of “healthy restriction” — [Page 534] the focus of the first phase of the Synthesis (see pp. 503–508). Thus, Mayr explicitly rejects such fallacies as Larmackian inheritance, and the idea that higher taxa arise by different and mysterious routes — thereby invoking an ar­gument by elimination to make evolutionary change at all levels fully consis­tent with principles of genetics at work in modern populations and subject to experiment in the laboratory or observation in the field. Whereas Mayr's ma­jor themes remain Darwinian, he still invokes the full panoply of legitimate genetic forces. Note in particular that selection (leading to adaptation), while listed first, represents only one force in an array collectively responsible for the formation of species. Adaptation holds no exclusivity, or even any partic­ular pride of place: “First, there is available in nature an almost unlimited supply of various kinds of mutations. Second, the variability within the small­est taxonomic units has the same genetic basis as the differences between the subspecies, species, and higher categories. And third, selection, random gene loss, and similar factors, together with isolation, make it possible to ex­plain species formation on the basis of mutability, without any recourse to Lamarckian forces” (1942, p. 70).

  Mayr reemphasizes this pluralistic theme at the end of his book in asserting the essential integra
tive claim that all phenomena of macroevolution can also be subsumed by the Synthesis. Inclusion within the Synthesis implies explana­tion by principles of modern genetics, not a commitment to any particular mode of genetic change: “It is feasible to interpret the findings and generali­zations of the macroevolutionists on the basis of the known genetic facts (random mutation) without recourse to any other intrinsic factors” (1942, p. 292). Mayr then lists the eight key principles of modern genetics that he re­gards as necessary for accomplishing the integration. Only one, number seven on the list, mentions selection and adaptation (p. 293).

  As a more positive argument against adaptationist exclusivity, Mayr's own taxonomy of “factors involved in speciation” (p. 216) grants explicit and equal weight to adaptation and nonadaptation as the two primary categories of divergence. He writes (p. 216): “We may classify these factors as (1) those that either produce or eliminate discontinuities and (2) those that promote or impede divergence. The latter may be subdivided further into adaptive (selec­tion) and non-adaptive factors.”

  Within this important category of nonadaptation, Mayr includes many prominent phenomena that he would later ascribe to selection.

  1. Nearly all polymorphism within species:

  There is, however, considerable indirect evidence that most of the characters that are involved in polymorphism are completely neutral, as far as survival value is concerned. There is, for example, no reason to believe that the presence or absence of a band on a snail shell would be a notice­able selective advantage or disadvantage. Among the many species of birds, which occur in several clear-cut color phases, there is, with one or two exceptions, no evidence for selective mating or any other advantage of any of the phases (p. 75). [Page 535]