The Structure of Evolutionary Theory

by Stephen Jay Gould

  The boldest version of the formalist argument for vertebrates, strongly up­held and extended by Geoffroy, hypothesizes a comprehensive unity of type across the entire phylum — with all elements present in all species (if only in embryos, or fused in adults), and with no new elements originating for spe­cific functions. This strict account embodies both meanings of constraint in their strongest versions — the negative sense of limitation in restriction of ele­ments to pieces of the archetypal jigsaw puzzle; and the positive sense of di­rected channels providing numerous, though ordered, possibilities for modi­fied shapes (including forms as yet unrealized on our planet, but predictable from the channels, and implied by observed developmental pathways).

  Geoffroy wrote in 1807 (quoted in Appel, 1987, p. 89): “It is known that nature works constantly with the same materials. She is ingenious to vary only the forms... One sees her tend always to cause the same elements to re­appear, in the same number, in the same circumstances, and with the same connections.” [Page 300]

  Talk is cheap, and romantic notions of abstract, overarching unity can eas­ily be verbalized. Lorenz Oken, the leader of German Naturphilosophie, wrote wondrous aphorisms (1809-1811, English translation, 1847), and pro­duced solid empirical work early in his career (1806), but never established a methodological program or built a factual foundation for his formalist phi­losophy. Meckel, Carus, and other Naturphilosophen extended the empirical side, but we rightly honor Geoffroy as the legitimate focus of this move­ment by our primary scientific criterion of fruitful utility. Geoffroy won his fame as a formalist because he managed to “cash out” the common ideas of transcendentalism in a workable program of research. His program included the two elements demanded of any good theory in natural history: a method for identifying the central phenomenon, and a reasonable explanation for ex­ceptions.

  The paradox and pitfall of unity of type as a working research program lies in the vast range of modifications that the archetype experiences under the widely varied adaptive regimes of our planet. Elements of the archetype should, in principle, be named and identified by their form, but the idealized archetype may be modified into incompatibility and unrecognizability along the copious adaptive pathways of concrete earthly biology — and we therefore face the dilemma that archetypal elements cannot always be identified by their shapes, or even by their discreteness (for elements fuse, or appear in em­bryos and then drop out during ontogeny). Some other criterion must be de­veloped.

  Geoffroy's major productive insight (still a favored basis for recognizing anatomical homologies — see Riedl, 1978) lay in his “principle of connec­tions” — the claim that homology must be identified by the relative positions and spatial interrelationships of elements, rather than primarily by form. Parts may expand and contract according to utility, but topology remains un­altered, and the archetype can be traced by unvarying spatial order.

  Yet, as so often happens amidst the exuberant diversity of natural history, the criterion must be nuanced as “traced by unvarying spatial order ... ex­cept when you can't.” Just as Haeckel bolstered recapitulation by bounding and taxonomizing exceptions (heterochronies and heterotopies in his termi­nology — see Gould, 1977b), and as Darwin specified forces other than, but clearly subsidiary to, natural selection (1859, p. 6), Geoffroy recognized a key class of exceptions to the principle of connections in his concept of metas­tasis (we use the word in a different, medical sense today, but the general meaning of movement to anomalous places has not altered). Connections can break and blocks of elements can move (though topology within blocks does not alter). For example, the shoulder girdle attaches to the rear of the head in fishes. But, in tetrapods, this connection breaks and several vertebrae may be interposed between skull and forelimbs (see p. 320 for the central role of this metastasis in Owen's interpretation of the vertebral archetype).

  In addition, Geoffroy tried to codify rules for secondary adaptive modifica­tion of archetypal form. Why do elements vary so much in size, and why can they fuse or even disappear? Geoffroy relied primarily upon a loi de balancement, or principle of compensation. Only so much general material [Page 301] can be commandeered to construct the archetypal elements. If one part be­comes hypertrophied by utility, others must atrophy to secure the constancy of the common fund. Geoffroy wrote succinctly in 1829 (quoted in Russell, 1916, p. 72): “There is only a single animal modified by the inverse reciprocal variation of all or some of its parts.”

  Most systems of thought achieve their exemplification in a canonical document; how would natural selection be defined without the Origin? Geoffroy's formalism received its codification in an 1818 book with a majestic title — Philosophie anatomique (or Anatomical Philosophy, explicitly not the less grandiose Anatomie philosophique, or Philosophical Anatomy). Geoffroy's subtitle brought the subject down to earth and bone with the best test case that vertebrates can offer — Pieces osseuses des organes respiratoires (the bony elements of the respiratory organs). Geoffroy began this work with an interesting example that highlights the contrast of formalism and functionalism, and that sowed the seeds for his later public debate with Cuvier.

  Cuvier had named and described four bones in the opercular series of teleost fishes — operculum, preoperculum, suboperculum, and interoperculum. And he, given his functionalist perspective, had treated these bones as unique to fishes and necessarily present for their utility in respiration by gills. Geoffroy developed a contrary interpretation based on his commitment to unity of the vertebral type, and to a primary implication that these bones must be homologues of elements with different functions in other verte­brates — for all vertebrates possess the same archetypal pieces, and none can be gained or lost. Geoffroy worked on the opercular bones from 1809 to 1812, without resolution. In 1812, a good year for wars and overtures, Cuvier argued that he had located, in the skulls of fishes, the homologs for all bones in the mammalian head — leaving no mammalian structures to serve as potential homologues of opercular bones in fishes. Henri de Blainville, Geoffroy's chief formalist supporter, then argued for homology between the opercular elements of fishes and bones of the tetrapod lower jaw. But, in 1817, Cuvier showed Geoffroy a preparation of a pike and convinced him that all bones of the lower jaw could be matched with jaw elements of tetrapods, again leaving no tetrapod bones to interpret as transformations of the opercular series. Geoffroy then returned to this crucial problem and realized, in a flash as he later stated, that he would have to investigate the only remain­ing elements in the tetrapod head for a solution: the opercular bones must be homologs of the mammalian middle ear bones! Geoffroy reminisced in 1830 (quoted in Appel, 1987, p. 97): “I regained courage and recommenced my studies, never to abandon them again.”

  Respiratory bones set the crucial experiment for vertebrate unity of type because such deciding tests must provoke maximal dangers of disconfirmation and grapple with the most difficult issues of validation. The respiratory bones from fish to tetrapods pose prima facie challenges to unity of type — for they present no apparent homology from sea to land, and they also exhibit maximal difference of function within vertebrates. If these bones could be won for formalism, then the rest of the skeleton would fall into order.

  The Philosophie anatomique includes five monographs on homologies [Page 302] between fishes and tetrapods for bones of (and around) the respiratory ele­ments: first on putative homology of opercular and hearing bones (incorrect in retrospect of course), second on the sternum, third on the hyoid, fourth on the branchial arches and their derivates (including the true homologs of the hearing bones, as biologists later learned), and fifth on the shoulder gir­dle. Cuvier, not yet perceiving (or at least not publicly admitting) his col­league's work as a comprehensive threat to his functionalist system, pro­claimed Geoffroy's publication as bold, challenging, and worthy of respect — though almost surely wrong. He strongly doubted Geoffroy's focal homology of opercular and hearing bones, for how could such large, central, and func­tionally necess
ary bones of fishes represent the same elements as tiny, almost superfluous nubbins ensconced within organs of differing utility in tetrapods?

  Geoffroy, who certainly equalled Cuvier in lack of modesty, proclaimed in the introduction to the Philosophie anatomique that his work marked “a new epoch, to which the publication of this book fixes the date” (1818, p. xxxi). He also admitted, tweaking Cuvier's allegiance to the primacy of positive facts, that formalist commitments come first. With such a proper conceptual key, the bones of the skeleton fall into place: “I do not hide it; my direction has been given to me by an a priori principle” (1818, p. 11) — although, he hastens to add, unity of type has worked so well that the principle could now be inferred inductively from the skeleton itself!

  Geoffroy proceeds immediately to battle in defending formalism by explicit contrast with false assumptions in Cuvier's functionalist alternative. He tells us on page 3 that fishes, by virtue of their functional differences from other vertebrates, seem to possess an anatomy of irreducible uniqueness. “It might appear to the observer ... that fishes, in order to exist, must call upon the in­tervention of new organs, and could only be complete in their construction by means of elements destined for them alone, bones created uniquely for their profit” (1818).

  But Geoffroy counterposes formalist unity of type to the functionalist alternative of special organs for novel uses: “I can and will satisfy you by showing you that all the elements used in the composition of fishes are exactly and en­tirely the same as those that enter into the formation of man, mammals, birds, and reptiles” (1818, p. 9).

  Geoffroy then takes up the two key challenges previously mentioned. He must first explicate the undeniable fact that the girdle, forelimbs and trunk organs have shifted back in tetrapods relative to their anterior position in fishes — as a result of the interposition of vertebral elements, and in apparent contradiction to the law of connections. Geoffroy invokes his exceptional principle of metastasis and argues that “the trunk exists under the milieu [sous le milieu] of the vertebral column” as a whole (1818, p. 9), but not un­der any particular element in the series. Second, he acknowledges that respi­ratory organs — with their maximally varying forms and functions in verte­brates — do pose the chief challenge for his system: “In this case, it would be entirely natural to assume in advance that the action of external conditions would impose requirements capable of placing the respiratory apparatus out­side the condition of the other organs. From the two modes so rigidly ordained [Page 303] [imperieusement exiges] for respiration, one might and could con­clude [on a du et pu conclure, in more euphonious French] that two different organic systems must exist... In this situation, respiration sets the most im­portant question to treat under our views” (1818, pp. 12-13).

  After presenting his homological solutions, Geoffroy buttresses his form­alist philosophy by explicit defense of the key claim that internal laws and constraints establish a primary and controlling pattern, with adaptive modi­fication as secondary, consequential and limited: “This influence of the exte­rior world, if ever called upon to become a perturbing cause of organiza­tion, must be bound necessarily within very straight limits: animals must oppose to them [exterior forces] several attributes inherent to their nature ... This struggle cannot fail to end to the advantage of interior organization, which has laws [droits] against which nothing can prevail” (1818, pp. 208-209).

  Finally, Geoffroy cuts to the heart of the deepest philosophical issue in the debate by noting that the realized use of archetypal elements for two such dif­ferent purposes as breathing in air and water requires that the elements them­selves be fashioned with great redundancy in potential utility: “double means have been prepared for a single function” (1818, p. 448). The archetype, by maintaining this potential for a full range of eventual expression, cannot be optimal for any particular role. Since archetypes exert logical and temporal priority over any particular expression, pure form endowed with redundancy of functional expression must hold sway over utility and adaptation: “Nature has conceived her plan for construction of a vertebrate animal under a double point of view: she had to choose a form of composition, so that the ideal ani­mal could accommodate itself equally to the two environments that envelop our globe. Above all, it was necessary ... that these two domains of the exter­nal world, which so rigorously impose two such different modes of respira­tion, must call upon the single and only basis of [morphological] organiza­tion” (1818, p. 448).

  Perhaps Geoffroy had anticipated the forthcoming struggle when he made his florid appeal, in the closing words of his Discours preliminaire (1818, p. xxix), to the attention and approbation of the next generation: “Oh might I learn that [my conclusions] have been useful for the youth of our schools. What group in our beautiful France is more worthy of interest? What devo­tion, what application, what ardor for study! Oh admirable youth, so occu­pied with noble productions of the mind, you seem absorbed in a single thought, in the thought that led Virgil to say: Felix qui potuit rerum cognoscere causas [Happy is he who can know the causes of things].”

  Throughout the 1820's, as events moved to their eventual climax in the 1830 debate, Geoffroy continued to codify and fortify his formalist philoso­phy — while Cuvier, who had once viewed Geoffroy's work with mild interest from a different perspective, moved (or felt pushed) to overt opposition.* [Page 304] Geoffroy emphasized, again and again, the two themes most calculated to rouse Cuvier's ire, and most central to the formalist conviction that adapta­tion for function can only record a secondary matching (following produc­tion by laws of form), not a primary construction.

  1. Function follows form. Consider Geoffroy's favorite motto: “such is the organ, such will be its function.” Or two more specific statements from 1829 (quoted in Russell, 1916, p. 77): “Animals have no habits but those that re­sult from the structure of their organs ... A vegetarian regime is imposed upon the Quadrumana by their possession of a somewhat ample stomach, and intestines of moderate length.”

  2. Final causes cannot serve as explanatory principles. Consider Geoffroy's second favorite motto: “Je me garde de preter a Dieu aucune intention” (I take care not to ascribe any intentions to God).

  Could Cuvier, who thought he knew God's ways (or at least the extent of His freedoms), remain silent against the taunts of such a turbulent priest?

  The debate of 1830: foreplay and aftermath

  Geoffroy, who loved aphorisms amidst his intense wordiness, often stated: “there is, philosophically speaking, only a single animal.” When he applied this radical notion of archetype only within the Vertebrata (as he did in his seminal work of 1818), Cuvier remained at relative peace, albeit in opposi­tion. But, two years later, Geoffroy took the fatal step that first elicited overt opposition from his former friend. Upholding formalism in explicit contrast to the functionalist credo had riled Cuvier to a considerable extent, but so long as this apostasy did not invade the schema of four unbridgeable embranchements, the foundation of Cuvier's taxonomy (1817), Geoffroy could be tolerated.

  In 1820, Geoffroy made a crucial move that filled him with the joy of uni­fication, and struck Cuvier as an act of unbridled imperialism: he extended the vertebral archetype to encompass arthropods as well, thus bringing two of the four embranchements under a common generating form — the vertebra itself. In his key article of 1822, Geoffroy described this “discovery” as “one [Page 305] of the greatest joys that I ever felt in my life” (1822, p. 99), for he had realized that “insects formed another class of vertebrated animals, and that they were, consequently, brought under the common law of uniformity of organization” (1822, p. 99).

  An attempt to homologize the Bauplan of insects and vertebrates implies some wondrous correspondences, and Geoffroy did not shrink from the logi­cally necessary, but inherently curious implications. He argued that both phyla are fundamentally metameric, with the idealized vertebra itself acting as the archetype of each segment — and therefore, in repetition and regio
nal specialization, of the entire animal. If Goethe's leaf could generate all the or­gans of a plant, then Geoffroy's vertebra would prefigure the entire skeleton of animals.

  Since the arthropod skeleton overlies the internal organs, whereas verte­brate bones lie below flesh and blood, their homology implies a remarkable conclusion, endorsed in yet another motto devised by Geoffroy: insects must live within their own vertebrae! Geoffroy wrote in 1822: “Every animal lives outside or inside its vertebral column” (Tout animal habite en debars ou en dedans de sa colonne vertebrate). Continuing the string of surprising implica­tions, all explicitly endorsed by Geoffroy, if exoskeletal body rings must be treated as homologs of vertebrae in the spinal column, then arthropod ap­pendages must be equated with vertebrate ribs — and insects walk on their ribs!