These two principles have always dwelled together in exquisite tension. Any complete account of morphology must call upon both phenomena, for most organisms are well adapted to their immediate environments, but also built on anatomical ground plans that transcend any particular circumstance. Yet the two principles seem opposed in a curious sense — for why should structures adapted for particular ends root their basic structure in homologies that do not now express any common function (as in Darwin's example of mammalian forelimbs)?
The designation of one principle or the other as the causal foundation of biology virtually defines the position of any scientist towards the organic world and its causes of order (see, especially, Russell's superb 1916 book on this dichotomy). Shall we regard the plan of high-level taxonomic order as primary, with local adaptation viewed as a set of minor wrinkles (often confusing) upon an abstract majesty? Or do local adaptations build the entire system from the bottom up? This dichotomy set the major debate of pre-Darwinian biology: does God reveal himself in nature primarily by the harmony of taxonomic structure, or by the intricacies of particular adaptations (see Section II, this chapter)? This dichotomy continues to define a major issue in modern evolutionary debates: does functional adaptation or structural constraint maintain priority in setting evolutionary pathways and directions (see Chapters 10–11)?
This issue of primacy between the two principles has held the central stage of natural history for so long that national traditions have developed, with continental preferences usually emphasizing unity of type (despite important exceptions like Georges Cuvier), and mainstream anglophonic science generally favoring adaptation (with exceptions for a few important pluralists like Richard Owen, or dissenters like William Bateson or D'Arcy Thompson). We often blunder in our historical understanding by assuming that evolution must be an ultimate watershed, marking a complete break between a bad before and an enlightened after. In fact, much continuity pass right through Darwin's rupture of history, with evolution only providing a different explanation for unaltered principles and phenomena. The good ship Dichotomy — Unity of Type vs. Conditions of Existence — entered the Darwinian current by converting its terms from a debate about God's primary mode of self-expression in nature to an argument about constraint and adaptation in evolution.
We cannot understand Darwin without grasping this fundamental continuity [Page 253] in national styles. As a young man, Darwin adored Paley's Natural Theology (see p. 116); later, in a courageous act of intellectual parricide, he constructed a theory that subverted Paley's mode of explanation. But Darwin never abandoned Paley's conviction that adaptation must be designated as the primary phenomenon of natural history. Darwin remained true to an English tradition stretching at least as far back as Robert Boyle and John Ray in the late 17th century of Newton's founding generation for modern science, running through Paley, the Bridgewater Treatises, Wallace, and Poulton in Darwin's own time, on to R. A. Fisher and finally to E. B. Ford, A. J. Cain, and R. Dawkins in the later 20th century.
When we properly place Darwin in this lineage, a genealogy unfractured by evolutionary theory, we can make sense of his fateful decision for resolving Unity of Type vs. Conditions of Existence at the end of Chapter 6 — a choice faithful to Paley and the English tradition in reaffirming the primacy of adaptation. Darwin writes, in words that define the causal basis of his theory (and continuing from the previous quotation on p. 25):
On my theory, unity of type is explained by unity of descent. The expression of conditions of existence, so often insisted on by the illustrious Cuvier, is fully embraced by the principle of natural selection. For natural selection acts by either now adapting the varying parts of each being to its organic and inorganic conditions of life; or by having adapted them during long-past periods of time: the adaptations being aided in some cases by use and disuse, being slightly affected by the direct action of the external conditions of life, and being in all cases subjected to the several laws of growth. Hence, in fact, the law of the Conditions of Existence is the higher law; as it includes, through the inheritance of former adaptations, that of Unity of Type (1859, p. 206).
Darwin's brilliant intellectual move clearly expresses the revolutionary impact of evolutionary explanations against the previous range of creationist paradigms. Creationist biology saw Unity of Type and Conditions of Existence, homology and adaptation, as opposite, but equally contemporary (or timeless), poles in a dichotomy of originating forces. Darwin literally added a new dimension to the debate — the axis of history. (And no intellectual expansion can be more profound than the introduction of a new dimension, orthogonal to previous modes of explanation.)
Thus, in this passage, Darwin makes a stunningly simple suggestion to break the impasse between Unity of Type and Conditions of Existence. (And yet, to be able to see anything at all in this clear and simple light, one must first grasp the revolutionary implications of evolution itself — the truly difficult intellectual transition out of Paley's world!) To be sure, the homologies of Unity of Type do not embody, and seem actively to oppose, current functions. Must Unity of Type therefore represent a principle of order dichotomously contrary to adaptation? In a world without history, where all features of organisms express their initially created state, the answer must be “yes.” But the addition of history, by a theory of genealogical connection, permits [Page 254] (and even privileges) another interpretation. Suppose that Unity of Type records no mysterious groundplan of created design, but only the actual, retained form of a common ancestor at the base of a bush of descent? Then homology can be simply explained as passive retention in the genealogy of diversified descendants — not an archetype of intelligent design, but only the signature of history.
In this context of evolutionary reform, we may then inquire about the causes of these common ancestral structures in distant pasts. And Darwin now makes his fundamental choice by affirming fealty to the English lineage of adaptationist thought. He argues that ancestral structures, forming the great homologies of Unity of Type, initially arose, by natural selection, as adaptations to “organic and inorganic conditions of life” in ancestral environments. Thus, the dichotomous poles of Unity of Type and Conditions of Existence achieve a single and unified explanation under natural selection — as immediate adaptations to present environments (Conditions of Existence), or as adaptations to ancient environments, transmitted by inheritance to diversified descendants (Unity of Type). The old dichotomy, in fact, expresses no clash of opposites at all, but only marks the temporally sequential representations of one dominant principle in evolution — adaptation by natural selection. Thus, since adaptation embodies the principle of Conditions of Existence, and since adaptation builds both ends of the old dichotomy, Conditions of Existence becomes the victorious pole of the old contrast, in Darwin's own words the “higher law; as it includes, through the inheritance of former adaptations, that of Unity of Type.”
Yet Darwin, far too sophisticated a thinker to embrace extreme positions, could not claim that natural selection and adaptation — though responsible for both poles of the old dichotomy — reigned exclusively in nature. Darwin knew that primary judgments in natural history must be rendered in terms of relative frequencies. Indeed, he had written as his last line in the Introduction to the Origin of Species, first edition: “I am convinced that Natural Selection has been the main but not exclusive means of modification” (1859, p. 6). He also reacted as strongly as his genial temperament ever permitted against those who charged him with false claims of exclusivity. In such cases, he usually cited this line from the Origin in vindication — as in his famous, almost rueful statement (Origin, 6th ed., 1872b, p. 395): “As my conclusions have lately been much misrepresented, and it has been stated that I attribute the modification of species exclusively to natural selection, I may be permitted to remark that in the first edition of this work, and subsequently, I placed in a most conspicuous position — namely, at the close
of the Introduction the following words: 'I am convinced that natural selection has been the main but not the exclusive means of modification.' This has been of no avail. Great is the power of steady misrepresentation.”
Thus, while extending natural selection to cover both poles of the old dichotomy between unity of type and conditions of existence, Darwin also listed the main supplements to selection among causes of evolutionary change: use and disuse, direct action of external conditions, and laws of [Page 255] growth. We reject the first two today, and Darwin also grants them little space by his qualifiers: “in some cases” and “being slightly affected.” But Darwin put more store by the third — laws of growth — as indicated by his only positive qualifier: “being in all cases subjected to the several laws of growth.” And we would offer the same judgment today, since laws of growth, under the more fashionable designation of “developmental constraints,” have become a “hot topic” in evolutionary biology once again (see Chapter 10). And now we come to the Darwinian trope of argument, the ploy that makes this chapter (and, to a large extent, this entire book) necessary.
Darwin wrote his crucial closing paragraph of Chapter 6 to argue that Unity of Type should be subsumed under Conditions of Existence — for Unity of Type, he asserted, only expresses past episodes of ordinary adaptation and natural selection, subsequently inherited by numerous modern descendants. Unity of Type has always defined the main arena for naturalists who view adaptation as secondary, and some principle of morphological order (for many versions exist) as primary. Darwin removed the rationale for a separate principle of Unity of Type by noting that ancient adaptations would, if inherited throughout a subsequent lineage, become sources of deep homology. Yet he could not deny — and had no desire to subvert — the idea of morphological principles working separately from natural selection, and building exceptions to adaptation. In this sense, Darwin supported the concept of constraint, but only if this principle could be carefully circumscribed within a category distinctly subsidiary to natural selection in relative frequency and biological importance. Darwin fully understood the crucial role of relative frequency in evolutionary arguments, and he rested his case for natural selection squarely upon such a judgment of quantitative importance. In so doing, he pursued the following strategy: take the old dichotomy, and show that both poles arise as products of natural selection. Then, having removed constraint as the primary cause of one pole (where a high relative frequency could not have been denied), allow constraint to reenter as a subsidiary force to natural selection (with a consequent guarantee of low relative frequency). Natural selection then becomes the primary force of evolution. Recall the full title of Darwin's book: On the Origin of Species by Means of Natural Selection, or the Preservation of Favored Races in the Struggle for Life.
The classical form of a relative frequency argument upholds a favored position and then degrades an alternative by two strategies, both used by Darwin in making constraint subservient to natural selection.
Nooks and crannies. Argue that your principle works nearly all the time, while the alternative occupies just a few subordinate holes of absence. By attributing both poles of the classic dichotomy (unity of type and conditions of existence) to natural selection as a primary cause, thereby robbing constraint of its potentially largest domain, Darwin granted dominance to adaptation.
Sequelae. Argue that your principle works as a prior and primary cause (in both temporal order and effect), and that the alternative only produces [Page 256] secondary modifications upon this fundamental action. In the closing paragraph of Chapter 6, all forces other than selection become sequelae to its primary action.*
Thus, Darwin invoked relative frequency to uphold his evolutionary world view: a theory of trial-and-error externalism, with natural selection as the only major creative force for change, and with internal variation restricted to the role of generating raw material for selection's perusal, and not of supplying important or consistent direction. Why, then, do many evolutionary biologists continue to demur? Darwin's basic argument in closing Chapter 6 can only be judged both brilliant and undoubtedly correct. Most homologies of Unity of Type are, indeed, adaptations inherited from a distant past, not fodder for constraint theorists who wish to demote the relative frequency and importance of natural selection. (Homologies of Unity of Type do act as phyletic constraints upon present possibilities — elephants will never fly — but such current limitations exist as consequences of initial adaptations, and therefore cannot stand against natural selection in any toting of relative frequencies.)
Modern constraint theorists, myself included, balk at Darwin's resolution because his argument demotes a large chunk of biology to a chink in a corner. The old Unity of Type theorists, lacking the alternative of “just history,” did falsely assume that deep homology must stand against adaptation. But much validity still attends their cardinal insight that principles of design, laws of growth, rules of architecture, nature of materials — generalities transcending the particulars of specific genealogical pathways — work as important interior channels of constraint in the positive sense of that undervalued word: for constraints not only prevent evolutionary motion by failing to supply variation; they also act positively to set preferred channels of change. Internal forces do not only present isotropic raw material to the fully creative externality of natural selection. Constraint does not exist in subservience to adaptation under the nooks-and-crannies and sequelae arguments of relative frequency. Constraint may never again (and rightly so) be able to claim primacy, [Page 257] as the old Unity of Type theorists held, but partnership with adaptation remains a reasonable and minimal demand.
We may epitomize Darwin's brilliant reconstruction of causation in natural history, the new dimension that he added, and the one that we need to reinsert, in diagrammatic form. Pre-evolutionary theorists, entirely lacking the concept of historical change, attributed created form to a dichotomous distinction of causes: immediate and functional vs. deeper and architectural (Fig. 4-1). Darwin literally added the dimension of history, but removed a previous axis of explanation by redefining constraints of Unity of Type as consequences of past adaptation (ancient Conditions of Existence) — Figure 4-2. Yet Darwin understood that he had not abolished the concept of constraint in undermining the primary example — homologies of Unity of Type — by real-location to the opposite camp. He therefore, in the same passage, established a different domain for constraint, as a category subservient to adaptation by the two standard arguments of relative frequency: the spatial claim of limited room (nooks and crannies) and the temporal claim of secondary status (sequelae to adaptation) — see Figure 4-3.
4-1. The standard pre-evolutionary and dichotomous conception of the causes of form as working either by adaptation to immediate conditions of existence, or by manifestation of laws of form that reflect unity of type.
4-2. Darwin literally adds a third dimension of history for the explanation of form. But he greatly devalues the domain previously ascribed to unity of type, admitting constraints of laws of form only by redefining such similarities as homologies based on the inheritance of past adaptations, and therefore adaptational in their origin and primarily due to the other (and now predominant) domain of conditions of existence.
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But many 19th century biologists, and many evolutionists in our day again, feel that Darwin demoted constraint too far, and that the two domains — constraint and adaptation — must again share potential partnership, as expressed by the important relative frequency of each component. We would therefore restore the strength of the dimension that Darwin first eliminated (when he reinterpreted Unity of Type as a consequence of adaptation) and then reintroduced in weakened form (when he allowed laws of growth to fill nooks and crannies in a domain ruled by natural selection) — see Figure 4-4.
This full model of Figure 4-4 shows three dimensions of form and their interactions: adaptation, constraint, and histor
y. A current trait of an organism may arise as an immediate adaptation to surrounding environments, as a constraint not particular to the contingent history of its lineage (architectural or structural principles, correlations to current adaptations), or by inheritance of an ancestral form (often called historical or phylogenetic constraint, but quite different in principle from nonhistorical styles of constraint). This distinction suggests a recursion, because contributions from the axis of “history”
4-3. Darwin does allow minor influence for constraint apart from mere inheritance of past adaptations. See text for details.
4-4. Constraint reestablished as equal in importance to adaptation as an immediate cause of form. See text for details.
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represent traits that, at their origin in an ancestor, arose as either adaptations or constraints. Nonetheless, the immediate form of an organism can still be meaningfully parsed into three major contributions of current adaptation, current constraint, and historical inheritance — Figure 4-5. This insight has generated the various “triangular” models of evolutionary causation that have gained vogue in recent years (see Fig. 4-6).
The Structure of Evolutionary Theory Page 42