Structuralist or formalist theories, on the other hand, generally seek to explain the origin of adaptive design in terms of such internal forces as constraint and directed variability. In the strictest versions of these theories, external causes can only act as editors to distill the most workable phenotypes from the full range of potential shapes that structural rules engender. Function may therefore determine what lives and what dies, but not what can (and does) originate.
Chapters 4 and 5 discussed the two major structuralist theories that we now reject for their operation as strict alternatives and denials of Darwinian functionalism: (1) orthogenesis, with its central claim that evolutionary trends follow internal drives in variation, and that selection can only accelerate or retard these inherent and inevitable pathways; and (2) saltation, with its premise that occasional fortuitous discontinuities in variation create new species all at once, and that selection can only intensify the process by preserving lucky sports and eliminating old, superseded designs.
Chapters 4 and 5, and much of Chapter 10 as well, also discuss more acceptable forms of structuralism that do not attempt to replace natural selection, but rather work in concert with known Darwinian mechanisms to channel possible directions of evolutionary change “from the inside” along pathways of variation that record constraints of history or principles of physical construction. I shall return to this theme of internal constraints in the last two sections of this chapter, where I discuss the important structural principle of non-adaptive origin followed by cooptation for a descendant's utility.
This initial section of Chapter 11, however, represents an interlude between historical constraints (Chapter 10) and structural constraints based on mechanically forced (or, at the opposite end of this spectrum, simply inherited) correlations with actively selected features (Sections II and III of this chapter). This interlude also discusses a form of structural constraint — but of a markedly different nature: direct molding by physical laws and forces acting upon the developing organism. This “maverick” theme has played only a small role in the history of evolutionary thought (a fact that should elicit no judgment about actual importance, for we all recognize that today's ignored or ridiculed theme can become the centerpiece of tomorrow's revolutionary theory).
If adaptive phenotypes originate directly and immediately from the imposition of physical forces upon the “yielding putty” (if you will) of organic material, then we need no functionalist account of “that perfection of structure and coadaptation” — for good form emerges automatically from the nature of physical reality (by external forces imposed upon the organism, or internal forces exerted from within as the organism grows). We get, in Kauffman's memorable phrase (1993) “order for free,” and need not posit any explicit organismal mechanisms, as functionalist theories propose (Darwinian selection [Page 1181] or Lamarckian inheritance), for “reading” the selective requirements of local environments and responding by evolutionary change.
Put another way, this structuralist theory of direct imposition asks nothing of organic matter beyond its malleability for passive shaping by physical forces. (One might argue that the malleability itself arose by a functionalist mechanism like natural selection, but the discussion of this section focuses upon current modes of change, not the origin of preconditions that make such changes possible.)
This theory of adaptive design by direct imposition differs from most formalist accounts of evolutionary change in two major ways (while agreeing on the central premise — the basis for my taxonomy of theories in the first place — that structural rules, rather than functional responses, generate organismal phenotypes):
1. Most structuralist theories identify the sources of adaptive order as residing largely “inside” the organism in the form of constraining genetic and developmental homologies, or the allometric and consequential rules that Darwin called “correlations of growth.” (For this reason, I have used “formalist,” “structuralist,” and “internalist” as virtually synonymous terms throughout this book.) But the structuralist theory of direct imposition locates the causes of adaptive order in physical laws of nature lying “outside” (and prior to) the specific architectural blueprints of each particular Bauplan (even though these physical laws may impose their shaping powers “from the inside” during growth).
2. In an even more iconoclastic claim (discussed previously on pp. 1053–1055 as the defining peculiarity of this way of thought), proponents of adaptive design by direct imposition tend to ignore, and often to devalue quite explicitly, the role of phylogeny, or any kind of historical analysis, in setting the Bauplane or developmental rules that channel and constrain patterns of evolution in any particular group. If physical forces shape organisms directly, then their prior histories don't matter, and we need only consider the immediate impress of current circumstances upon malleable organic materials. After all, we don't invoke any aspect of history or genealogical connection to explain why Cambrian quartz from Asia exhibits the same crystal structure as Recent quartz from America. So why should we not attribute the logarithmic spirals of Paleozoic and modern gastropods to the same spatiotemporal in-variance of physical laws?
One might say, in epitome, that the first argument opposes this theory to all other, and more conventional, forms of structuralist thought; whereas the second statement, far more radical in scope, opposes this theory to the central concept of evolutionary biology itself (in both structuralist and functionalist accounts): the role of history, and the importance of phylogeny in understanding both present forms and future prospects.
I doubt that this theory of adaptive design by direct physical imposition could ever stand as a complete, or even a dominant, explanation of evolution. (We shall see that even the most celebrated exponent of this view, D'Arcy Wentworth Thompson in On Growth and Form, ultimately ceded the major turf of explanation, at least for complex organisms, to phylogeny and heredity [Page 1182] rather than to immediate physical imposition.) But I suspect that direct physical assembly or imposition may supply an important, perhaps even a controlling, theme in two major and rather different arenas of evolutionary theory: (1) The origin of life and the initial assembly of basic and universal components of cellular organization and genetic structure. Do we not sense that much of life's initial history falls into the domain of “universal chemistry” and the general physics of self-organizing systems, whereas the actual, divergent pathways of metazoan phyla then fall under the control of historical contingency? (2) Broad predictabilities of life's pattern through time, transcending the contingent particularities of any individual lineage. The structure of ecological pyramids must display some physical predictability, whereas the occupation of the top carnivore apex by lions or tigers or bears (or phorusrhachids or borhyaenids) demands knowledge of historical particulars. The increasingly right skewed distribution of life's complexity, with stability of the bacterial mode throughout (Gould, 1996a), speaks more to the general physics of reflecting boundaries (of minimal complexity in this case), the physically necessary origin of life at this minimal complexity, and the stochasticity of random walks, than to any historical detail of uniquely earthly existence.
I am a historian at heart, and although the theme of immediate physical assembly intrigues me — and no one with literary pretensions could remain unmoved by the coincidence that D'Arcy Thompson's Growth and Form, the most stylish book in the history of anglophonic biology, also happens to be the “Bible” of this particular view of life — I don't think that the hypothesis of direct physical construction will play a large part in the expansion of Darwinian theory advocated as my central argument in this book. I therefore view this section as a “place holder” in the logic of my case, and not at all as a complete or even adequate account of an important subject. I will occupy this particular place in an idiosyncratic manner by analyzing D'Arcy Thompson's great work (1917, 1942) and then discussing, much more briefly, the most important modern expressio
ns of this view of life in the works of Goodwin (1994) and Kauffman (1993). But method does lie in the sanity of this choice, for one could not ask for a better vehicle than D'Arcy Thompson's brilliant argument and stunning prose. His magisterial (if idiosyncratic and, at times, even cranky) book embodies an entire worldview within its ample scope. His specific examples may be wrong or dated, but no one has ever presented a more complete and coherent version of this approach to the explanation of evolution, including explicit discussion of all major implications for general theory. In this sense, an exegesis of D'Arcy Thompson may well represent the most modern and relevant way to discuss this important corner of evolutionary thought.
D'ARCY THOMPSON'S SCIENCE OF FORM
The structure of an argument
In 1945, the Public Orator of Oxford lauded D'Arcy Thompson as unicum disciplinae liberations exemplar (the outstanding example of a man of liberal [Page 1183] education — at the ceremony for his receipt of an honorary degree as Doctor in Civil Law). In 1969, the Whole Earth Catalog, the commercial bible of the “green” movement in America, called his major work “a paradigm classic.” Few people can list such diverse distinctions in their compendium of honors. But then, few people have displayed so wide a range of talent. D'Arcy Wentworth Thompson (1860-1948), Professor of Natural History at the Scottish universities of Dundee and St. Andrews, translated Aristotle's Historia animalium, wrote glossaries of Greek birds and fishes, compiled statistics for the Fishery Board of Scotland and contributed the article on pycnogonids to the Cambridge Natural History.
But D'Arcy Thompson's current reputation rests almost entirely upon a book of a thousand pages, revered by artists and architects as well as by engineers and biologists — the “paradigm classic,” On Growth and Form (1917, 2nd edition, 1942). P. B. Medawar (1967, p. 232) lauded this volume as “beyond comparison the finest work of literature in all the annals of science that have been recorded in the English tongue.” G. Evelyn Hutchinson (1948, p. 579) regarded Growth and Form as “one of the very few books on a scientific matter written in this century which will, one may be confident, last as long as our too fragile culture.”
Although I have studied D'Arcy Thompson's wonderful book throughout my career (see Gould, 1971b, for my first, and in retrospect embarrassingly puerile, publication in a journal of the humanities), I originally made a major error in siting him within the history of biology. All intellectuals love a courageous loner, and I had been beguiled by D'Arcy Thompson's seemingly anachronistic peculiarities — his flowery, sometimes overblown, but often soaring and powerful, Victorian prose; his expertise at fully professional levels in Latin and Greek; even his lifelong residence in an outlying region that, in my false mental geography, might well have been located above the Arctic Circle. In retrospect, I had unthinkingly conflated my sense of his intellectual distance from conventional thought with an assumption about physical isolation as well. When I finally visited the University of St. Andrews (for the humbling experience of receiving an honorary degree in D'Arcy Thompson's own bailiwick), I recognized its proximity to Edinburgh, and its easy access by rail. (As a further confirmation of St. Andrews's central location within the contemporary world, I began to write this section on the very day that Tiger Woods won the British Open on the world's original, and still most famous, golf course of St. Andrews.)
I had therefore viewed D'Arcy Thompson as the ultimate man out of time — a Greek geometer and classical scholar, a Victorian prose stylist at the dawn of modernism's lean and cynical attitude (for the first edition of Growth and Form appeared in 1917 in the midst of Word War I, while another and even more destructive war greeted the second edition of 1942; many historians have noted that, in a meaningfully ideological, rather than an arbitrarily calendrical, reckoning, the 20th century really begins with World War I and the end of illusions about progress and the benevolent hegemony of European control).
I shall not try to rob D'Arcy Thompson of his genuine singularities, but [Page 1184] when we place his biological views into the context of evolutionary debate in his own time, we find, underneath his quirky stylistic uniqueness, a standard critique of Darwinism based upon the common argument that natural selection cannot fashion novel features, but can only eliminate the unfit, bolstered by a claim for saltation as a common mode in the origin of highly distinct taxa and anatomical groundplans. D'Arcy Thompson did link this standard critique to an uncommon solution — his central claim that physical forces shape adaptive form directly — but we should regard his theory as an unusual solution to the standard conundrums of his time, and not as an anachronistic importation from Pythagorean Greece, clothed in the prose of Dickens or Thackeray.
On Growth and Form is a weighty tome (793 pages in the original edition of 1917, enlarged to 1116 pages in 1942), but D'Arcy Thompson presents his central thesis as a tight argument, expressed in clear logical order, with proper attention to inherent difficulties — and, above all, artfully developed throughout. (My analysis here, with two labeled exceptions, follows the first edition.)
In a common conceit (in the non-pejorative sense of a fanciful device), scientists often clothe a truly radical idea in the falsely modest garb of merely useful technicality. Thus, D'Arcy Thompson asserts that he wrote Growth and Form only to make biologists a bit more comfortable with the mathematical description of morphology. He states in his epilog (1917, p. 778):
The fact that I set little store by certain postulates (often deemed to be fundamental) of our present-day biology the reader will have discovered and I have not endeavored to conceal. But it is not for the sake of polemical argument that I have written, and the doctrines which I do not subscribe to I have only spoken of by the way. My task is finished if I have been able to show that a certain mathematical aspect of morphology, to which as yet the morphologist gives little heed, is interwoven with his problems, complementary to his descriptive task, and helpful, nay essential, to his proper study and comprehension of Form. Hie artem remumque repono.*
Beginning his assault upon biological traditions of explanation, D'Arcy Thompson reminds us that we feel no discomfort in ascribing the elegant and well-fitting forms of inorganic objects to physical forces that can mold them directly, and that also embody the advantage (for our comprehension) of simple mathematical description. Why, then, when organic forms display equally elegant and simple geometries, and when these biological shapes also match the expected impress of physical forces, do we shy from invoking the same explanation of direct production that we apply without hesitation to identical forms in nonorganic nature? (1917, pp. 7-8): [Page 1185]
The physicist proclaims aloud that the physical phenomena which meet us by the way have their manifestations of form, not less beautiful and scarce less varied than those which move us to admiration among living things. The waves of the sea, the little ripples on the shore, the sweeping curve of the sandy bay between its headlands, the outline of the hills, the shape of the clouds, all these are so many riddles of form, so many problems of morphology, and all of them the physicist can more or less easily read and adequately solve: solving them by reference to their antecedent phenomena, in the material system of mechanical forces to which they belong, and to which we interpret them as being due...
Nor is it otherwise with the material forms of living things. Cell and tissues, shell and bone, leaf and flower, are so many portions of matter, and it is in obedience to the laws of physics that their particles have been moved, molded and conformed . . . Their problems of form are in the first instance mathematical problems, and their problems of growth are essentially physical problems, and the morphologist is, ipso facto, a student of physical science.
Our reluctance, D'Arcy Thompson claims, arises largely from conventional beliefs about the “special” character of life, based on a traditional assumption that organic shapes embody purposes and therefore demand teleological explanation, whereas inorganic forms exert no action of their own, and can only be ex
plained as passive records of physical forces. We assert organic uniqueness by invoking both an active and passive argument. The passive argument sets living things apart, without specifying any uniquely biological causes or processes (p. 2):
The reasons for this difference lie deep, and in part are rooted in old traditions. The zoologist has scarce begun to dream of defining, in mathematical language, even the simpler organic forms. When he finds a simple geometrical construction, for instance in the honey-comb, he would fain refer it to psychical instinct or design rather than to the operation of physical forces; when he sees in snail, or nautilus, or tiny foraminiferal or radiolarian shell, a close approach to the perfect sphere or spiral, he is prone, of old habit, to believe that it is after all something more than a spiral or a sphere, and that in this “something more” there lies what neither physics nor mathematics can explain. In short he is deeply reluctant to compare the living with the dead, or to explain by geometry or by dynamics the things, which have their part in the mystery of life.
Biologists then advance the active argument to posit a set of distinctively organic causes that, in their outcomes, mimic the same forms that physical forces, left to their own devices, would impose upon any plastic material. At this point, D'Arcy Thompson introduces his critique of Darwinism and of functionalist evolutionary thought in general. In the paragraph following the last citation, D'Arcy Thompson identifies the two main culprits in our erroneous convictions about special biological forces behind good organic design: phyletic solutions (or any kind of historical explanation), and adaptationist [Page 1186] speculation leading to false assumptions about the need for such functionalist mechanisms as natural selection (pp. 2-3):
The Structure of Evolutionary Theory Page 188
