The Structure of Evolutionary Theory

by Stephen Jay Gould

  J. S. HUXLEY: PLURALISM OF THE TYPE

  As with Haldane, Huxley also credited a well-received lecture that he had presented on Darwinism as the stimulus for writing his much longer book — a 1936 presidential address to the British Association on “Natural selection and evolutionary progress.” Huxley maintained the focus of this lecture in presenting a thoughtful, but partisan, defense of Darwinism throughout Evo­lution, The Modern Synthesis, beginning with a wry comment on the exten­sive pessimism so common before the movement he christened: “The death of Darwinism has been proclaimed not only from the pulpit, but from the bio­logical laboratory; but, as in the case of Mark Twain, the reports seem to have been greatly exaggerated, since today Darwinism is very much alive” (1942, p. 22).

  Huxley encapsulates the central logic of Darwinism in much the same way, and with the same intent, that I advocate in this book. He recognizes the three main characteristics of variation as central (pp. 22-24) — copiousness (though not pervasive enough for mutation pressure to overwhelm selection), small-ness of phenotypic effect, and nondirectionality — and he credits Mendelism [Page 517] with providing the physical explanation for what Darwin could only deduce from first principles of natural selection, while hoping for later confirmation from discoveries about the basis of heredity.

  In an interesting discussion on the nature of theories and their central logic, Huxley disputes Lancelot Hogben's claim that the Mendelian fusion had so altered Darwin's own notion of mechanics, that the reformulation of Fisher, Haldane, and Wright should neither bear Darwin's name nor even retain the term “natural selection” for its central mechanism. Huxley replies that all theories must change by growth, but that the proper standard for mainte­nance of a name must be defined by continuity in key precepts in a central logic:

  Hogben is perfectly right in stressing the fact of the important differences in content and implication between the Darwinism of Darwin or Weismann and that of Fisher or Haldane. We may, however, reflect that the term atom is still in current use and the atomic theory not yet rejected by physicists, in spite of the supposedly indivisible units having been di­vided. This is because modern physicists still find that the particles called atoms by their predecessors do play an important role, even if they are compound and do occasionally lose or gain particles and even change their nature. If this is so, biologists may with a good heart continue to be Darwinians and to employ the term Natural Selection, even if Darwin knew nothing of mendelizing mutation (1942, p. 28).

  Huxley also follows the English tradition (see pp. 116-119) for central emphasis upon adaptation in the definition of evolutionary mechanisms. He speaks of “a functionally-guided course of evolution” (p. 39), and almost claims an a priori status for panadaptationism: “Our enumeration will also serve as a reminder of the omnipresence of adaptation. Adaptation cannot but be universal among organisms, and every organism cannot be other than a bundle of adaptations, more or less detailed and efficient, coordinated in greater or lesser degree” (1942, p. 420).

  But as further evidence for pluralism in the early synthesis, and despite this emphasis upon the ubiquity of adaptation, Huxley then speaks favorably of the same challenges and exceptions that intrigued Haldane — orthogenesis and nonadaptation. Whereas he does claim (correctly) that most cases of sup­posed orthogenesis only represent instances of phyletic constraint, he also provides an interesting taxonomy of genuine examples. Mirroring our mod­ern distinction between positive and negative meanings of constraint (see Chapter 10, pp. 1025–1061, and Gould, 1989a), Huxley speaks of dominant and subsidiary orthogenetic restriction:

  True orthogenetic restriction depends on a restriction of the type and quantity of genetic variation. When dominant it prescribes the direction of evolution: when subsidiary it merely limits its possibilities... Domi­nant orthogenetic restriction [is] very rare, if indeed it exists at all... [Page 518] Subsidiary orthogenetic restriction is probably frequent, but we are not yet able to be sure in most cases whether a limitation of variation as ac­tually found in a group is due to a limitation in the supply of mutations or to selection, or to other causes. It is, however, certain that some mutational effects recur regularly in some allied species, and probable that this phenomenon is widespread (1942, p. 524).

  Huxley also cites overcoiling in Gryphaea (Trueman, 1922) — the classic case of his time, though since invalidated (Gould, 1972) — as a primary puz­zlement and most promising example for “dominant orthogenesis”:

  We must provisionally face an explanation in terms of orthogenesis — i.e. of evolution predetermined to proceed within certain narrow limits, irrespective of selective disadvantage except where this leads to total extinc­tion. It should be noted that, even if the existence of orthogenesis in this cause [sic, for case] be confirmed, it appears to be a rare and exceptional phenomenon, and that we have no inkling of any mechanism by which it may be brought about. It is a description, not an explanation. Indeed its existence runs counter to fundamental selectionist principles (1942, p. 509).

  Despite his general commitment to adaptation, Huxley also granted some importance (beyond mere existence) to Wright's genetic drift in the formation of species with small population sizes (p. 58). He even extended the power of this non-adaptational force to the origin of generic differences, though not beyond: “It may be presumed, on somewhat indirect evidence, that 'useless' non-adaptive differences due to isolation of small groups may be enlarged by the addition of further differences of the same sort to give generic distinction, though it seems probable that differences of family or higher rank are always or almost always essentially adaptive in nature” (1942, p. 44).

  Thus, the early synthesis, in the view of both its founders and its namegiver, reinstated Darwinism as the centerpiece of evolutionary theory by rejecting any substantial role for the full spate of previously popular alternatives. (I should say “instated,” for Darwinism had never before attained majority ap­peal as a mechanism, even during Darwin's lifetime.) But the early synthesists, with Fisher's exception, also left a few facets intact on Galton's polyhedron. Their interest lay in showing that our increasing knowledge of the Mendelian world could establish natural selection as the primary cause of evolutionary change, not in staking a claim for Darwinian exclusivity.

  Synthesis as Hardening

  THE LATER GOAL OF EXALTING SELECTION'S POWER

  Evolutionists have generally depicted the second phase of the Synthesis as a gathering of traditional subdisciplines under an umbrella constructed during [Page 519] the first phase by fusing Mendel with Darwin. I learned something fundamen­tal about this second phase as a participant at the conference, entitled Work­shop on the Evolutionary Synthesis that Ernst Mayr convened in Boston in 1974. This conference — an amazing experience for a young evolutionist at the beginning of a career — included every major living participant in the Syn­thesis except Bernhard Rensch, who was ill; G. G. Simpson, who was angry; and Sewall Wright, whom Mayr simply would not invite, despite pleas from yours truly and several others. I don't think I ever experienced a greater mo­ment of pure “academic awe” than my first impression, when I looked across from “our” side of the table (where Mayr had placed the “young” historians and evolutionists) and saw Dobzhansky, Mayr, and Stebbins, Ford, and Darling­ton all together on the other side.

  This marvelous conference was marred (in terms of its stated purpose) only by a severe difficulty in keeping these men to the intended subject of their reminiscences about past accomplishments. They all remained so passion­ately involved in modern research that, whenever the planned reminiscences began, someone would make a reference to the latest paper revising some view or another — and they would immediately begin a learned discussion about current events, fueled by delight at new findings that forced revisions of their old certainties! (A difficulty for the conference's stated aim perhaps, but personally one of the most memorable events that I have ever witnessed. If the best practitioners can maintain such openness an
d involvement to the end of their lives, then scholarship need not fear ossification. Such traits do not, however and alas, represent the norm in science — so I did come to under­stand the special excellence of these extraordinary men, and I did achieve some visceral grasp of why they, and not others, made the Synthesis.)

  I had always viewed the books of the second phase as coequal. But the conference discussions emphasized a major point previously unclear to me: the preeminence of Dobzhansky's 1937 book, Genetics and the Origin of Species. This volume did not merely happen to enjoy the luck of first publication in a series — a temporal primus inter pares, so to speak. Dobzhansky's volume provided a direct and primary inspiration for the books that followed. Speaker after speaker rose to state that his own contribution had been prod­ded by reading Dobzhansky's account first.

  And now the irony — and the key point about disjunction between the two phases of the Synthesis. If we wish to argue that the first phase of synthe­sis featured the construction of population genetics by Fisher, Haldane and Wright, while the second phase brought traditional subdisciplines into this framework, we should expect the primary translator to be fluent in the lan­guage of transfer. In one sense, Dobzhansky did possess the requisite flu­ency — uniquely (at least for English-speaking scientists), and for an interest­ing reason of national traditions. As I also learned at the 1974 conference, only in Russia had Mendelian experimental work been merged, extensively and successfully, with traditional taxonomy and natural history. Dobzhansky, after all, had developed expertise as both a skilled Drosophila experimentalist [Page 520] and a specialist on the taxonomy of coccinellid beetles (ladybirds). In America and Western Europe, experimentalism and field biology occupied two different and largely hostile worlds. Could the second phase of the syn­thesis have emerged from a Western Drosophila lab like T. H. Morgan's (where field biology held low status and enjoyed no practice — see p. 532), or a museum program in comprehensive systematics (with virtually no experi­mental facilities)? Dobzhansky exported a fusion that Western science, in ig­norance of the Russian language and in hostility to communist politics, had failed to recognize — even though H. J. Muller had brought the first Dro­sophila stocks to Russia, thus fueling Dobzhansky's optimal training with a Western trigger.

  But if Dobzhansky could integrate the Mendelian experimental world with natural history, what about the supposed centerpiece of mathematical popu­lation genetics? Here, by his own repeated, almost gleeful, admission, Dob­zhansky remained a near dunce. He did not study, nor could he even under­stand, the details of this literature. Of his long and fruitful collaboration with Sewall Wright, Dobzhansky simply said that he had followed the principle of “father knows best” — that is, he bypassed Wright's mathematical manipula­tions and accepted his English explanations on faith. In fact, of all the great second-phase synthesists only G. G. Simpson possessed sufficient mathemati­cal background to read and understand these papers.

  Dobzhansky's willingness to accept an incomprehensible literature, and the later acquiescence of so many leaders from other subdisciplines (largely via Dobzhansky's “translation”), testify to a powerful shared culture among evolutionists — a set of assumptions accepted without fundamental question­ing or perceived need to grasp the underlying mechanics. Such a sense of community can lead to exhilarating, active science (but largely in the accu­mulative mode, as examples cascade to illustrate accepted principles). As a downside, however, remaining difficulties, puzzles, anomalies, unresolved corners, and bits of illogic may retreat to the sidelines — rarely disputed and largely forgotten (or, by the next generation, never learned). This situation may sow seeds of an orthodoxy that can then become sufficiently set and un­challenged to verge on dogma — as happened in many circles, at least among large numbers of epigones, at the acme of the Synthesis in the late 1950's and 1960's.

  In this section, I shall try to illustrate one example in extenso — the central and defining case, I believe — of the narrowing suffered by a synthesis that be­came augmented in power but downgraded in the art and tactic of question­ing. I call this increasing confidence, bordering on smugness, the “hardening” of the Synthesis. Thus I contrast the positive restriction of the first phase — the elaboration of a generous and comprehensive theory, and the invalidation of false and fruitless alternatives — with the negative tightening that occurred during the ontogeny of the second phase. This hardening — still our legacy to­day — must serve as a starting point for any current attempt to introduce more amplitude into evolutionary theory. The hard version of the Synthesis pro­vides a standard for judging (by contrast) the interest and importance of [Page 521] modern revisions — from neutralism,* to punctuated equilibrium, to a com­mon feeling that the theme of developmental constraints not only gives sub­stance to an old truth, but also confutes the hardened version's commitment to Darwin's (I should really say Fisher's) billiard ball against Galton's poly­hedron.

  My example shall trace the transformation of adaptation from an option to be ascertained (albeit favored and granted a dominant relative frequency) to an a priori assumption of near ubiquity (save in trivial or derivative situa­tions without evolutionary importance) — in other words the burnishing of Galton's polyhedron to the billiard ball of pure functionalism (allowing no significant pushing back from internal structure upon the direction of evolu­tionary change). This hardening buttressed (or rather, in my view, overly rigidified and sclerotised) one leg on the essential Darwinian tripod of sup­port — the second theme of functionalism against internalist and structuralist forces (see Chapters 2, 4, and 5).

  But hardening pervaded all major themes of Darwinian central logic, and the other two legs of the tripod also experienced their own form of petrifac­tion (treated in less detail in Section 4 of this chapter). Pluralistic (and, admit­tedly, often loose) thinking about levels of selection yielded to an explicit pro­mulgation of organismic selection as the only acceptable mode — as a virtual campaign to root out group selection accompanied the battle of Williams (1966) against Wynne-Edwards (1962). Thirdly, a willingness to grant some independence, or at least some puzzlement, to patterns in macroevolution (see Haldane and Huxley's respectful view of orthogenesis, as discussed in the last section), ceded to the hard view that all phenomena measured in millions of years must be explained by smooth extrapolation from palpable causes on generational scales in modern populations — and that the paleontological re­cord can therefore only present a pageant of products generated by known causes, and not provide an independent theory or even a set of additional causal principles.

  I have used a particular method to demonstrate the hardening of the Synthesis — textual comparison of early and later works by key authors. Ontog­eny can be an unconscious trickster. In trying to forge sense and continuity in [Page 522] our own lives, we often forget or “reconstruct” the actualities of our early years — thus subtly recasting our former selves as miniatures of our current beliefs. Therefore, direct interview can be a notoriously unreliable technique (while representing, ostensibly, the most direct and empirical of all scholarly sources) — for an older person may become a very unreliable chronicler of his own past. But written records stand as frozen testimonies, unaltered fossils of a time that may not be personally recoverable with high accuracy.

  I received my first insight into the hardening of the Synthesis by a proper (if gentle) pedagogical correction. During my graduate student years, I presented a report on paleontology in the Modern Synthesis to a seminar at the Ameri­can Museum of Natural History. In the characteristically naive manner of a young and awestruck protoscholar, I explicated the views of Simpson and others as jewels of reforming consistency, lux in tenebris and complete from the first. Bobb Schaeffer, a wonderful teacher, stopped me as I was explaining Simpson's complex idea of “quantum evolution” (see p. 530). I had done well, he said, for the concept as presented in Simpson's 1953 book, but had I ever studied the original version in Tempo and Mode in Evolution (
1944)? I replied that I had not read this initial formulation, for I had assumed that the first account could only represent a less developed, and therefore pale and trifling, version of later subtlety. Schaeffer said that the two discussions dif­fered fundamentally, but that Simpson had minimized the appearance of change by retaining the same terms while profoundly altering their meaning. (Schaeffer also told me that he had argued the issue with Simpson for years, and that the essence of Simpson's change, for which Schaeffer took some credit — a shift from nonadaptionist to selectionist interpretation of interme­diate forms in major phyletic transitions — had only strengthened the general argument, even though Simpson had covered up his changes.) I did not be­lieve that most of the profession could have missed such a major shift, but I checked. Schaeffer was entirely right.

  My personal failure piqued my interest and I began to wonder whether Simpson's change had been idiosyncratic or part of an unrecognized pat­tern. I began to check early and late works of other key figures, particularly Dobzhansky and Mayr. All had moved from pluralism to strict adaptation-ism — and along a remarkably similar path. I began to view this transition as the major ontogenetic event of the Synthesis during its second phase. I chris­tened this change as the “hardening” of the Synthesis and wrote four papers on the subject (Gould, 1980e, 1982d, 1983b and c). The rest of this section documents my three favorite cases — Dobzhansky through the three editions (1937, 1941, and 1951) of his seminal book, Mayr (1942 vs. 1963), and Simpson (1944 vs. 1953) — and reproduces a good deal of material from my earlier articles.

  Several historians have tested my hypothesis by application to other key figures, and have affirmed the adaptational hardening as general (e.g., Beatty, 1988, and Smocovitis, 1996, 2000). Sewall Wright, subject of Provine's mas­sive biography (1986; see also Provine, 1971), provides the most interesting and revealing case. Wright's name, of course, immediately evokes the phe­nomenon of genetic drift, generally called the “Sewall Wright effect” in articles [Page 523] of the early Synthesis. One would therefore regard Wright as the man most likely to speak for the importance of nonadaptation, and against any functionalist hardening.