The Structure of Evolutionary Theory

by Stephen Jay Gould

  Today I have visited Darwin; I am happy that it happened and I must say that Darwin was so very cordial and friendly . . . The conversation was quite easy; they all spoke very slowly and clearly and they gave me the time to speak up; thus I did better in speaking English than I expected ... In the garden there were hothouses with peaches and grapes. Darwin told me a long story about the peaches and immediately offered me one of them; it was delicious.

  During our scientific conversation, there was the same laughing mania as you have seen with Sachs; Sachs laughs all the time, Darwin some­what less but as merrily. He was very interested in what I have done lately...

  He puts a footstool on a chair before he sits down on it, for he gets headaches if he sits low — the poor soul! Mr. Farrer told me that today [Page 423] Darwin felt exceptionally well and happy and that I were lucky. Mrs. Darwin takes good care of him and will never allow him to become too tired; she simply sends him to bed!

  He has deepset eyes and in addition very protruding eyebrows, much more than one would say from his portrait. He is tall and thin and has thin hands, he walks slowly and uses a cane and has to stop from time to time... His speech is very lively, merry and cordial, not too quick and very clear.

  It is remarkable how soon one feels at home with people who are friendly and cordial. What a difference with Hooker and Dyer; they were cold and I did not care about them. But I enjoyed my visit with Darwin and I feel much more happy these last days. It is such a pleasure to find that somebody is really interested in you and that he cares about what you have discovered.

  Third, and most importantly, Darwin also directly inspired de Vries' shift from physiological to evolutionary and genetic studies. With fond memories in old age, de Vries told an interviewer in 1925 (quoted in Van der Pas, 1970, p. 192): “I was led to the study of heredity by my love for Darwin.”

  The source of de Vries' inspiration did not lie in the Origin of Species or the Descent of Man, but rather in Darwin's speculation on heredity, the “provi­sional hypothesis of pangenesis” as Darwin characterized his own proposal, published as the last chapter of his two-volume 1868 treatise on Variation in Plants and Animals Under Domestication. In his last letter to Darwin (who died six months later), de Vries wrote, up to date as ever in commenting on Darwin's last book The Formation of Vegetable Mold Through the Action of Worms, but also mentioning a stronger interest in Darwin's older views on pangenesis: “After reading the first chapter of your book, I have been attend­ing to the habits of worms, and had the good fortune of repeating some of your interesting observations . . . For some time I have been studying the causes of the variations of animals and plants, as described in your treatise ... I have always been especially interested in your hypothesis of Pangenesis and have collected a series of facts in favor of it” (de Vries to Darwin, Octo­ber 15,1881).

  Darwin's hypothesis of pangenesis served as a speculation that could val­idate Lamarckian inheritance, a mode of transmission that Darwin deem-phasized but did not contest. According to pangenesis, the basis of hereditary characters resides within tiny cellular particles called gemmules. All cells pro­duce gemmules during growth and later life. Gemmules then migrate from so­matic to germ cells, where they collect to pass inherited characters to the next generation. The germ cells therefore store “actual physical representatives of all the cells which have existed during the whole life of the parent body” (Kellogg, 1907, p. 218). Since gemmules become modified in somatic cells by conditions of life and the actions of organisms, acquired characters can be in­herited.

  De Vries suggested a fundamental (and correct) modification that turned [Page 424] Darwin's theory into something quite different. He abandoned Darwin's key notion of the migration of gemmules across cell boundaries — thus removing the rationale for Lamarckian inheritance. In de Vries' revised concept, the hy­pothesized hereditary particles behaved so differently that they required a dif­ferent name; thus, still honoring Darwin, de Vries rechristened the gemmules as “pangenes.”

  In de Vries' concept of Intracellular Pangenesis (the title of his 1889 book), the nucleus of each cell contains all particles (pangenes) needed to construct an organism. But only some pangenes are expressed in each cell, thus explain­ing the differential morphogenesis of parts. Expressed pangenes migrate out of the nucleus into the cytoplasm, where they orchestrate the appropriate em­bryology. In no case can pangenes move between cells. De Vries wrote: “The hypothesis that all living protoplasm is built up of pangenes, I call intra­cellular pangenesis. In the nucleus every kind of pangene of the given individ­ual is represented; the remaining protoplasm in every cell contains chiefly only those that ought to become active in it” (1889, in 1910 translation, p. 215).

  This remarkably prescient theory comes as close to the secret of heredity as anyone had managed in the speculative tradition before the elucidation of genes and chromosomes. Whiggish historians nearly always regard Intra­cellular Pangenesis as de Vries' greatest book. In abstract concept, his nuclear pangenes differ little from the particles of heredity that would soon be recog­nized and named as genes, especially since de Vries viewed his pangenes as a minimal set of basic instructions, not naively as a collection of items for speci­fying each overt phenotypic part. His notion of active and latent pangenes re­calls dominant and recessive alleles — and one might justly argue that de Vries had therefore been “preadapted” to appreciate Mendel. Fortune, as Pasteur famously said, favors the prepared mind. Moreover, the notion that all in­structions reside in the nucleus (with passage to the cytoplasm, at appropriate times and places, for transmission of local messages) bears remarkable iso­morphism with our modern mechanism of DNA, RNA, and the differentia­tion of cells.

  Two further aspects of Intracellular Pangenesis play important roles in this story. First, de Vries' theory became the source of our modern term “gene” — for Johannsen explicitly derived the shortened name directly from de Vries' “pangene.” Moreover, since de Vries' “pangene” honored Darwin's name for his speculative particle of heredity, Darwin himself becomes the ultimate source (via de Vries) for this basic biological term. Few evolutionary biolo­gists recognize this curious terminological odyssey, making Darwin himself the ultimate, if indirect, source of our modern term “gene.”

  Second, we note in de Vries' treatment of Darwin a microcosm of the strange and almost painfully ambivalent fealty that tied him emotionally (and verbally) to Darwin even while he devised a contradictory theory — the source of Seward's anger, as described in my opening remarks. De Vries' theory, despite its personal source in Darwin's pangenesis, became a fundamentally different intellectual entity. In Darwin's pangenesis, gemmules move from [Page 425] somatic to germ cells and provide a mechanism for Lamarckian inheri­tance. In de Vries' intracellular pangenesis, pangenes move from the nucleus to the cytoplasm of the same cell and specify a theory of cellular differentia­tion.

  Yet de Vries insisted on downplaying this difference as a minor variation. For rhetorical purposes, he asserted that his denial of intercellular movement for gemmules constituted only a minor reform in Darwin's ideas. His new theory could therefore remain entirely in Darwin's spirit. Throughout his life, de Vries could not break verbal fealty with the primary hero and inspiration of his youth. In a late work of 1922, de Vries wrote:

  Freed from the assumption of a transportation of gemmules through the organism, the conception of Pangenesis is the clear basis of the present manifold theories of heredity. An organic being is a microcosm, says Darwin, a little universe, formed of a host of self-propagating organisms, inconceivably minute, and numerous as the stars of heaven. In honor of Darwin, I have proposed to call these minute organisms Pangenes, and this name has now been generally accepted under the shortened form of genes. They are assumed to be the material bearers of the unit characters of species and varieties (1922, p. 222).

  The mutation theory: origin and central tenets

  Evolutionists usually assume that, since de Vries ranks wi
thin the trio of Men­del's resurrectionists, his “mutation theory” — with its genetic title and de­served status as the greatest challenge to Darwinism from the early 20th cen­tury — must be traceable to a Mendelian inspiration. But de Vries always insisted that his theory, and almost everything else he valued, could boast a Darwinian source. In particular, he asserted later in his career that the root of the Mutation Theory lay in an insight about two distinctly different kinds of variation that he had obtained from Darwin's theory of pangenesis, and then developed within his own Intracellular Pangenesis of 1889. I am not con­fident that this link can be defended, for considerable (and rather tortured) exegesis must be applied to so interpret the actual text of de Vries' 1889 book, whatever his later memories. But de Vries' debt and psychological fe­alty to Darwin can only be called pervasive, while the timing of de Vries' in­terpretation can also be defended (for the Mendelian discovery postdated the genesis of the mutation theory).

  In the English version (1910) of Intracellular Pangenesis, de Vries wrote a note to his translator, pointing to a passage that he identified as the source of the Mutation Theory: “An altered numerical relation of the pangenes already present, and the formation of new kinds of pangenes must form the two main factors of variability” (1910, p. 74). De Vries interpreted this passage as pres­aging the key claim of his later mutation theory — that new species arise suddenly by a distinct and special kind of saltational variation (called muta­tion), while ordinary, imperceptible, omnipresent, Darwinian variability can­not forge evolutionary novelties. Late in his career, de Vries wrote (1922, [Page 426] p. 222): “Species and varieties have originated by mutation, but are, at pres­ent, not known to have originated in any other way. Originally this concep­tion has been derived from the hypothesis of unit characters as deduced from Darwin's Pangenesis, which led to the expectation of two different kinds of variability, one slow and one sudden.”

  Whatever the intellectual roots, de Vries eventually centered his illustration and defense of the mutation theory upon a single source, the evening prim­rose, Oenothera Lamarckiana — so we can identify a particular empirical ba­sis for the defense of his views. (This strategy, as mentioned previously, ulti­mately backfired when researchers explained the unusual mutability in O. Lamarckiana as a peculiarity of the plant's hybrid nature and chromosomal system, and not as the generality that de Vries required.) In 1886, de Vries found odd and distinct mutational variations growing among a wild field of evening primroses at Hilversum, near Amsterdam. He later described his mix­ture of good fortune and conscious preparation (1905, p. 27):

  Cultivated plants of course, had only a small chance to exhibit new qualities, as they have been so strictly controlled during so many years. Moreover, their purity of origin is in many cases doubtful... For this reason I have limited myself to the trial of wild plants of Holland, and have had the good fortune to find among them at least one species in a state of mutability. It was not really a native plant, but one probably in­troduced from America or at least belonging to an American genus. It was the great evening primrose or the primrose of Lamarck. A strain of this beautiful species is growing on an abandoned field in the vicinity of Hilversum, at a short distance from Amsterdam. Here it has escaped from a park and multiplied. In doing so it has produced, and is still pro­ducing quite a number of new types . . . This interesting plant has af­forded me the means of observing directly how new species originate, and of studying the laws of these changes.

  De Vries' method for finding and propagating Oenothera mutants included a mixture of experimental care and hard work in the Burbankian mode. To find new mutants, he sowed prodigious numbers of seeds. For example, in his 1888 sowing, he tested 15,000 seedlings and found 10 mutations. To propa­gate and breed his new forms, and to test for their purity in inheritance, de Vries stringently followed the obvious rules for tracing pedigrees: fertilize each plant with known pollen, prevent insect pollination, save and sow all seeds separately.

  De Vries, in crisp summary, presented the essence of his theory as exhibited by the Oenothera mutants — sudden, fully constituted, nonadaptive, observ­able, experimentally ascertainable origin of new species: “They came into ex­istence at once, fully equipped, without preparation or intermediate steps. No series of generations, no selection, no struggle for existence was needed. It was a sudden leap into another type, a sport in the best acceptation of the word. It fulfilled my hopes, and at once gave proof of the possibility of the direct [Page 427] observation of the origin of species, and of the experimental control thereof” (1905, p. 550).

  De Vries reported different numbers and names for new Oenothera species in various publications, but the seven cited in his 1904 Berkeley lectures pro­vide a good feel for his categories and criteria (see Fig. 5-9). Above all, the mutants appeared suddenly and bred true (other mutants reverted, hybrid­ized, or segregated in only a proportion of progeny). De Vries placed his seven new species into three categories. First, he designated two “true elemen­tary species” — the red-veined O. rubrinervis and the giant O. gigas (a tetra-ploid by later discovery). De Vries described these new forms as “robust and stark species, which seem to be equal in vigor to the parent plant, while di­verging from it in striking characters” (1905, p. 533). In a second category of “retrograde varieties,” de Vries identified the smooth-leaved O. laevifolia, the short-styled O. brevistylis, and the dwarf O. nanella, “a most attractive little plant” (1905, p. 531). These new forms also arose with abrupt distinctness, and bred as true as the two “elementary species,” but these three mutants dif­fered from the parent O. Lamarckiana by loss or diminution of an ancestral character, not by addition of novelty — hence their separate, and less admira­ble, category. (I am intrigued by our cultural bias that designates increased bulk as a novelty (O. gigas), while ranking shortness as mere subtraction (O. nanella).) De Vries then placed two forms into a third (and inconsequential) class of “weak species” that “have no manifest chance of self-maintenance in the wild state” (1905, p. 537). The whitish O. albida “grows too slowly and is overgrown,” while the oblong-leaved O. oblongata “bear small fruits and few seeds.”

  All three central tenets of the mutation theory work in direct opposition to Darwinian gradualism and sequential shaping by natural selection in the ori­gin of species — hence the widespread and proper interpretation of de Vries' theory as a powerful refutation of Darwinism (Kellogg, 1907, who lists the views of de Vries as an alternative, not an auxiliary, to Darwinism).

  1. Above all, the mutation theory embodies the most unabashedly saltational notion ever seriously regarded as an evolutionary mechanism. New species arise in a single step by a sudden, discontinuous, fully formed and true breeding leap in phenotype. De Vries could not have been clearer in his intro­ductory comment to the Mutation Theory (1909a, p. 3): “Species have arisen from one another by a discontinuous, as opposed to a continuous process. Each new unit, forming a fresh step in this process, sharply and completely separates the new form as an independent species from that from which it sprang. The new species appears all at once; it originates from the parent spe­cies without any visible preparation and without any obvious series of transi­tional forms.”

  De Vries explicitly contrasts his new view with Darwinian gradualism: “A current belief assumes that species are slowly changed into new types. In con­tradiction to this conception the theory of mutation assumes that new species and varieties are produced from existing forms by sudden leaps” (1905, p. vii). Such sudden inception precludes any role for natural selection in the [Page 428] origin of species. Taking the traditional anti-Darwinian line, and employing a striking metaphor, de Vries claims that selection cannot construct anything new, but can only operate as a sieve to preserve favorable forms produced by some other process: “Natural selection is a sieve. It creates nothing, as is so often assumed; it only sifts. It retains only what variability puts into the sieve. Whence the material comes that is put into it should be kept separat
e from the theory of its selection. How the struggle for existence sifts is one question; how that which is sifted arose is another” (1909a, volume 2, p. 609).

  2. If new species originate in single leaps, then their origin must be non-adaptive, however much their future survival may require a fortuitous match with local environments: “It explains in a very simple way the existence of the vast number of specific characters which are quite useless or as to the use of which we have no idea at all... According to the commonly accepted theory of selection only characters advantageous to their possessors should arise; according

  5-9A. Oenothera Lamarckiana contrasted with two of De Vries' mutations. From Volume 2 of De Vries' Mutation Theory.

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  to the theory of mutation on the other hand useless or even disadvan­tageous ones may also appear” (1909a, volume 1, pp. 209-210)

  3. Slow Darwinian changes cannot be observed on human and experimen­tal time scales, but the mutation theory brings evolution into the domain of observational science; “the origin of species may be seen as easily as any other phenomenon” (1905, p. 26). Emphasizing a direct contrast between the vir­tues of his operational theory and the fatal intractability of Darwinian gradu­alism (here attributed to Wallace, for de Vries could not bear to saddle his hero with such a negative assessment), de Vries brands gradualism as obstruc­tionist, and compliments his own view as liberating: “I shall try to prove that sudden mutation is the normal way in which nature produces new species and new varieties. These mutations are more readily accessible to observation and experiment than the slow and gradual changes surmised by Wallace and his followers, which are entirely beyond our present and future experience.