The Structure of Evolutionary Theory

by Stephen Jay Gould

  In fact, when interviewed late in life, as both Provine and I can attest, Wright complained bitterly that his views on the evolutionary role of genetic drift had been consistently misinterpreted (Wright died in 1988 at age 98, sharp as ever to the very end). Since genetic drift describes stochastic change in gene frequencies by sampling error, one might assume that Wright had ad­vocated a radically non-Darwinian approach to evolutionary change by de­moting selection and adaptation, and boosting the importance of accident. But Wright strongly denied such an interpretation of his views. He argued, with evident justice apparent to anyone who reads the works of his last thirty years, that his theory of “shifting balance,” while providing an important role for genetic drift, remains strongly adaptationist — though adaptation generally arises at a level higher than the traditional Darwinian focus on organisms.

  In brief (see p. 555 for a fuller account), Wright asserted that he had invoked genetic drift primarily as a generator of raw material to fuel an adaptationist process of interdemic selection. If the founding deme of a new species occupies one adaptive peak on a complex landscape (to use standard Wrightian imagery), movement to additional peaks requires genetic drift — for this stochastic process permits small demes to descend slopes and enter valleys, where selection can then draw a deme up to another peak. When demes within a single species populate several peaks, interdemic selection can operate as a powerful mechanism of adaptation.

  Wright therefore (and accurately) depicted his later shifting balance theory as adaptationist, and as invoking drift only for a source of variation among demes. But Wright, though estranged in many ways from the developing synthesis (see Section 4), followed its trend toward increasingly exclusive emphasis upon adaptation in evolutionary change. The version of shifting balance that Wright advocated during the last 30 years of his life did not orig­inate by sudden creation, complete in this final form. Shifting balance em­phasized different themes and arguments in Wright's earlier work, and these articles, written during the pluralistic phase of the synthesis, granted a much greater role to randomness and nonadaptation in evolutionary change. In fact, Wright often, and explicitly, invoked drift as a non-Darwinian agent of change in articles written during the early pluralistic phase of the syn­thesis.

  Wright presents a striking example of the principle that later recollections may be inferior, as historical sources, to written testimony from the time in question. Provine (1986) has catalogued Wright's ambiguities and multiple intents during the crucial period of 1929-1932. The later selectionist view al­ready stands in the wings, but most passages of these early articles advocate the nonadaptationist role for drift that Wright would later reject (and deny he ever held). Wright wrote in 1931 (p. 158), for example, that shifting balance “originates new species differing for the most part in nonadaptive respects.” In the following year, he stated (1932): “That evolution involves nonadaptive [Page 524] differentiation to a large extent at the subspecies and even the species level is indicated by the kinds of differences by which such groups are actually distinguished by systematists. It is only at the subfamily and family levels that clear-cut adaptive differences become the rule. The principal evolutionary mechanism in the origin of species must then be an essentially nonadaptive one” (pp. 363-364). Provine (1986) concludes: “The careful reader in 1932 would almost certainly conclude that Wright believed nonadaptive random drift was a primary mechanism in the origin of races, subspecies, species, and perhaps genera. Wright's more recent view that the shifting balance theory should lead to adaptive responses at least by the subspecies level is found nowhere in the 1931 and 1932 paper.”

  INCREASING EMPHASIS ON SELECTION AND ADAPTATION

  BETWEEN THE FIRST (1937) AND LAST (1951) EDITION OF

  DOBZHANSKY'S GENETICS AND THE ORIGIN OF SPECIES

  Dobzhansky's original probe (1937) toward synthesis operated more as a methodological claim for the sufficiency of genetics than a strong substantive advocacy of any particular causal argument — although he clearly states his general Darwinian preferences in this first edition. Dobzhansky held, con­trary to his own Russian mentor Filipchenko, that the methods of experi­mental genetics can provide enough principles to encompass evolution at all levels. But Dobzhansky did not play favorites among the admitted set of legit­imate principles. He did not, in particular, proclaim the pervasive power of natural selection leading to adaptation as a predominant style and outcome of evolutionary change.

  Some inkling of the chaotic and depressed state of evolutionary theory be­fore the Synthesis can be glimpsed in a simple list of previously popular argu­ments that Dobzhansky regarded as sufficiently important to refute — claims that denied his hope for synthesis by treating Mendelian processes observed in the laboratory as different from the genetic modes for regulating “impor­tant” evolutionary change in nature. Dobzhansky rebuts the following argu­ments explicitly: Continuous variation in nature is non-Mendelian and differ­ent in kind from discrete mutational variation in laboratory stocks (p. 57); Mendelian variation can only generate differences between taxa of low rank (races to genera), while higher taxa owe their distinctions to another (and un­known) genetic process (p. 68); chromosomal changes are always destructive and can only lead to degeneration of stocks (p. 83); differences between taxa of low rank are directly induced by the environment and have no genetic or evolutionary basis (p. 146); Johannsen's experiments on pure lines prove the ineffectiveness of natural selection as a mechanism of evolutionary change (p. 150); selection is too slow in large populations to render evolution, even in geological time (p. 178); genetic principles cannot account for the origin of reproductive isolation (p. 255).

  Dobzhansky's fifth chapter, on “variation in natural populations,” stresses the pluralism of the early synthesis. Observable genetic phenomena provide [Page 525] a source for all evolution; we can trace full continuity from studies in the laboratory, to variation within natural populations, to formation of races and species:

  It is now clear that gene mutations and structural and numerical chromosome changes are the principal sources of variation. Studies of these phenomena have been of necessity confined mainly to the laboratory and to organisms that are satisfactory as laboratory objects. Nevertheless, there can be no reasonable doubt that the same agencies have supplied the materials for the actual historical process of evolution. This is at­tested by the fact that the organic diversity existing in nature, the differ­ences between individuals, races, and species, are experimentally resolv­able into genic and chromosomal elements, which resemble in all respects the mutations and the chromosomal changes that arise in the laboratory (1937, p. 118).

  But what forces mold and preserve this variation in nature? Dobzhansky stresses natural selection (p. 120), but he does not grant this process the dom­inant role that later “hard” versions of the synthesis would confer. He em­phasizes genetic drift (which he calls “scattering of the variability”) as a fun­damental mode of evolutionary change in nature, not as an odd phenomenon occurring in populations too small to leave any historical legacy. He argues that local races can form without influence from natural selection, and he supports Crampton's (1916, 1932) interpretation of the nonadaptive and in­determinate character of substantial racial differentiation in the Pacific land snail Partula. He emphasizes that evolutionary dynamics depend, in large measure, upon the size of populations because selection does not always con­trol the outcome (and we therefore need information about numbers of indi­viduals and their mobility in order to assess the effects of drift, migration, and isolation). He coins the term “microgeographic race” and argues that most group distinctions at this level may be both nonadaptive and genetically based, contrary to the opinions of many naturalists who then regarded such races as adaptive and nongenetic.

  The sixth chapter then treats natural selection explicitly. Dobzhansky be­gins by clearing away some early Mendelian misconceptions about the impo­tence of natural selection (logical errors in inte
rpreting Johannsen's experi­ments on pure lines, for example). He then poses a central question: Darwin devised the theory of natural selection to explain adaptation; admitting Dar­win's success in this area, may we then extrapolate and argue that selection controls the direction of all evolutionary change (p. 150)? Dobzhansky an­swers that we cannot defend such an extension of selection's power. He then criticizes the strict selectionism of Fisher (p. 151), and praises a book that would later be castigated by all leading synthesists as a remnant of older and unproductive ways of thought — Robson and Richards (1936), with their de­fense of a nonadaptive origin for most subspecific and even interspecific dif­ferences in closely related forms.

  A long concluding section (pp. 185-191) supports Wright's “island model” [Page 526] of selection among semi-isolated demes occupying different peaks of an adap­tive landscape. Dobzhansky pleads for more study of “the physiology of pop­ulations” since Wright's model proclaims three factors as important in differ­ent ways, while not granting inherent predominance to any: genetic drift, migration, and natural selection: “Since evolution as a biogenic process obvi­ously involves an interaction of all of the above agents, the problem of the rel­ative importance of the different agents unavoidably presents itself. For years this problem has been the subject of discussion. The results of this discussion so far are notoriously inconclusive; the 'theories of evolution' arrived at by different investigators seem to depend upon the personal predilections of the theorist” (p. 186). Dobzhansky does, however, suggest that Wright's model may validate the common conviction of naturalists that the morphological differentia of races and species must often be nonadaptive.

  Genetics and the Origin of Species went through three editions (1937, 1941, and 1951). As in the successive versions of Darwin's Origin, the differ­ences among these editions cannot be dismissed as trivial or cosmetic, for they convey a major change in emphasis — an alteration that set the research program for most evolutionary biologists until the past few years. As the Syn­thesis developed, the adaptationist program grew in influence and prestige, and other modes of evolutionary change fell into disrepute, or became rede­fined as locally operative but unimportant in the overall picture.

  Dobzhansky's third edition (1951) clearly reflects this hardening. He still insists, of course, that not all change can be called adaptive. He attributes the frequency of some traits to equilibrium between opposed mutation rates (p. 156) and doubts the adaptive nature of racial variation in blood types. He asserts the importance of genetic drift (pp. 165, 176) and does not accept as proof of panselectionism one of the centerpieces of the adaptationist pro­gram — A. J. Cain's work on frequencies of banding morphs in the British land snail Cepaea (p. 170).

  But inserted passages and shifting coverage convey, as their common focus, Dobzhansky's increasing faith in the scope and power of natural selection, and in the adaptive nature of most evolutionary change. He deletes the two chapters that contained most material on nonadaptive or nonselected phe­nomena (polyploidy and chromosomal changes, though he includes their ma­terial, in much reduced form, within other chapters). He adds a new chapter on “adaptive polymorphism” (pp. 108-134). Moreover, he now argues that anagenesis, or “progressive” evolution, works only through the optimizing, winnowing agency of selection based on competitive deaths; species adapting by increased fecundity in unpredictably fluctuating environments do not con­tribute to anagenesis (p. 283).

  But the most remarkable addition occurs right at the beginning. I label these passages remarkable because I doubt that Dobzhansky really believed what he literally said; I feel confident that he would have modified his words had anyone pointed out how his increasing fascination for adaptationism had led him to downgrade the deepest and oldest of evolutionary themes to effective [Page 527] invisibility (see Chapter 10, pp. 1175–1178 for the modern relevance and refutation of this striking image).

  Dobzhansky poses the key question of organic form and taxonomy: why do organisms form discrete and clearly nonrandom “clumps” in populating morphological space? Why does the domain of mammalian carnivores con­tain a large cluster of cats, another of dogs, a third of bears, leaving so much unoccupied morphological space between? Dobzhansky begins by “promot­ing” Wright's model of the “adaptive landscape” to an inappropriate level. In so doing, Dobzhansky subtly shifts the model's meaning from an explanation for nonoptimality (with important aspects of nonadaptation) to an adaptationist argument about best solutions. Wright devised his model to explain differentiation among demes within a species. He proposed the metaphorical landscape to justify a fundamentally nonadaptationist claim: If a “best solu­tion” exists for the phenotype of a species (the highest peak in the landscape), why don't all demes reside there? But if we “upgrade” the model to encom­pass differences between species within a clade, then metaphorical landscapes mutate into a framework for strict adaptationism. Each peak now becomes the optimal form for a single species (not the nonoptimal form for some demes within a species). And related peaks represent a set of best solutions as the various adaptations of separate evolutionary entities within a clade.

  Dobzhansky then attempts to solve the problem of clumping with an adaptationist argument based upon the organization of ecological space into preexisting optimal “places” where good design may find a successful home. Evolution has produced a cluster of cats because an “adaptive range,” stud­ded with adjacent peaks, exists in the economy of nature, waiting, if you will, for creatures to move in. In other words, discontinuity in taxonomic space maps discontinuity in optimal form for available environments, with adapta­tion as the agent for mapping.

  The enormous diversity of organisms may be envisaged as correlated with the immense variety of environments and of ecological niches, which exist on earth. But the variety of ecological niches is not only im­mense, it is also discontinuous . . . The adaptive peaks and valleys are not interspersed at random. “Adjacent” adaptive peaks are arranged in groups, which may be likened to mountain ranges in which the separate pinnacles are divided by relatively shallow notches [sic, Dobzhansky does indeed mean “notches” in this passage, not “niches” (as later in the quotation)]. Thus, the ecological niche occupied by the species “lion” is relatively much closer to those occupied by tiger, puma, and leopard than to those occupied by wolf, coyote, and jackal. The feline adaptive peaks form a group different from the group of the canine “peaks.” But the feline, canine, ursine, musteline, and certain other groups of peaks form together the adaptive “range” of carnivores, which is separated by deep adaptive valleys from the “ranges” of rodents, bats, ungulates, pri­mates, and others. In turn, these “ranges” are again members of the [Page 528] adaptive system of mammals, which are ecologically and biologically segregated, as a group, from the adaptive systems of birds, reptiles, etc. The hierarchic nature of the biological classification reflects the objec­tively ascertainable discontinuity of adaptive niches, in other words the discontinuity of ways and means by which organisms that inhabit the world derive their livelihood from the environment (pp. 9-10).

  Thus, Dobzhansky renders the hierarchical structure of taxonomy as a fitting of clades into preexisting ecological spaces. Discontinuity emerges not so much as a function of history, but as a reflection of adaptive topography. But this interpretation cannot hold; surely, the cluster of cats exists primarily as a consequence of homology and historical constraint. All felines share a basic morphology because they arose from the common ancestor of this clade alone. We doubt neither the excellent adaptation of this common ancestor nor the claim that all descendants may fit equally well into their current envi­ronments. But the feline group and the gaps that separate this cluster from other families of carnivores reflect history above all, not the current organiza­tion of ecological topography. All feline species have inherited the unique Bauplan of cats, and cannot deviate far from this commonality as they adapt, each in its own particular way. Genealogy, not current adaptation, provi
des the primary source for clumped distribution in morphological space.

  THE SHIFT IN G. G. SIMPSON'S EXPLANATION OF “QUANTUM EVOLUTION” FROM DRIFT AND NONADAPTATION (1944) TO THE EMBODIMENT OF STRICT ADAPTATION (1953)

  Although Simpson, probably more than Dobzhansky, personally favored selectionist arguments in the initial version of his seminal work (1944), he also adopted a pluralistic stance at first. In fact, at the crux of his book, Simpson proposed an explicitly nonadaptationist theory to resolve the greatest anom­aly in the fossil record; he also considered this theory of “quantum evolu­tion” as the crowning achievement of his book.

  Like Dobzhansky in his first edition (1937), Simpson (1944) espoused consistency of all evolutionary change with principles of modern genetics as his primary assertion for a general and synthetic theory. The major challenge to unity and consistency arose from the infamous “gaps” or discontinuities of the fossil record — particularly at the largest scale of appearances for new Bauplan without fossil intermediates. Simpson wrote:

  The most important difference of opinion, at present, is between those who believe that discontinuity arises by intensification or combination of the differentiating processes already effective within a potentially or really continuous population and those who maintain that some essen­tially different factors are involved. This is related to the old but still vital problem of micro-evolution as opposed to macro-evolution ... If the two proved to be basically different, the innumerable studies of microevolution [Page 529] would become relatively unimportant and would have minor value to the study of evolution as a whole (1944, p. 97).