Theories are excellent servants but very bad masters.

— Thomas Henry Huxley

Natural selection does not act on anything, nor does it select (for or against), force, maximize, create, modify, shape, operate, drive, favor, maintain, push, or adjust. Natural selection does nothing. Natural selection as a natural force belongs in the insubstantial category already populated by the Becker/Stahl phlogiston or Newton’s “ether.” ….

Having natural selection select is nifty because it excuses the necessity of talking about the actual causation of natural selection. Such talk was excusable for Charles Darwin, but inexcusable for evolutionists now.

— Provine 2001: 199-200, The Origins of Theoretical Population Genetics.

Darwin has often been depicted as a radical selectionist at heart who invoked other mechanisms only in retreat, and only as a result of his age’s own lamented ignorance about the mechanisms of heredity. This view is false. Although Darwin regarded selection as the most important of evolutionary mechanisms (as do we), no argument from opponents angered him more than the common attempt to caricature and trivialize his theory by stating that it relied exclusively upon natural selection. In the last edition of the Origin, he wrote (1872, 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 misinterpretation.

Charles Darwin, Origin of Species (1872, p. 395)

— Gould, Stephen J., & Lewontin, Richard C. (1979) The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme. PROCEEDINGS OF THE ROYAL SOCIETY OF LONDON, SERIES B, VOL. 205, NO. 1161, PP. 581-598.

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Ernest Mayr’s (1963, p. 586) epitome of Darwinism as preached by the Modern Synthesis: “All evolution is due to the accumulation of small genetic changes, guided by natural selection …, and that transpecific evolution … is nothing but an extrapolation and magnification of the events that take place within populations and species.” (Gould 2002: 160) [See The Evolution of the Genome ]

Throughout Mayr’s 1963 book [Animal Species and Evolution, Cambridge MA: Harvard University Press] — with a cadence that sounds, at times, almost like a morality play — phenomenon after phenomenon falls to the explanatory unity of adaptation, as the light of nature’s truth expands into previous darkness: non-genetic variation (p. 139), homeostasis (pp. 57, 61), prevention of hybridization (p. 109). Former standard bearers of the opposition fall into disarray, finally succumbing to defeat almost by definition: “It is now evident that the term ‘drift’ was ill-chosen and that all or virtually all of the cases listed in the literature as ‘evolutionary change due to genetic drift’ are to be interpreted in terms of selection” (p. 214). All particular Goliaths have been slain (although later genetic studies would revivify this particular old warrior): “The human blood-group genes have in the past been held up as an exemplary case of ‘neutral-genes,’ that is, genes of no selective significance. This assumption has now been thoroughly disproved.” (p. 161). (Gould 2002: 539)

However, Mayr’s most interesting expression of movement towards a hardened adaptationism occurs not so much in these explicit claims for near ubiquity, but even more forcefully in the subtle redefinition of all evolutionary problems as issues in adaptation. The very meaning of terms, questions, groupings and weights of phenomena, now enter evolutionary discourse under adaptationist presumptions. Not only have alternatives to adaptation been routed on an objective playing field, Mayr claims in 1963, but the conceptual space of evolutionary inquiry has also become so reconfigured that hardly any room (or even language) remains for considering, or even formulating, a potential way to consider answers outside an adaptationist framework. (Gould 2002: 539)

Major subjects, the origin of evolutionary novelty for example, now reside exclusively within an adaptationist framework by purely functional definition: “We may begin by defining evolutionary novelty as any newly acquired structure or property that permits the performance of a new function, which, in turn, will open a new adaptive zone” (p. 602). In a world of rapid and precise adaptation, morphological similarity between distantly related groups can only arise through convergence imposed by similar adaptive regimes upon fundamentally different genetic material. The older, internalist view (constraint-based and potentially nonadaptationist) — the claim that we might attribute such similarities to parallelism produced by homologous genes — is dismissed as both old-fashioned and wrong headed. (In modern hindsight, this claim provides a particularly compelling example of how hardened adaptationism can suppress interesting questions — for such homologues have now been found in abundance. Their discovery ranks as one of the most important events in modern evolutionary science — see Chapter 10, p. 1092, where we will revisit this particular Mayrian claim): “In the early days of Mendalism there was much search for homologous genes that would account for such similarities. Much that has been learned about gene physiology makes it evident that the search for homologous genes is quite futile except in very close relatives” (1963 [Animal Species and Evolution, Cambridge MA: Harvard University Press], p. 609). (Gould 2002: 539)

(….) All potential anomalies yield to a more complex selectionist scenario, often presented as a “just-so-story.” Why did the crown height of molars increase slowly, if hypsodontry became so advantageous once horses shifted to vegetational regimes of newly-evolved grasses with high silica content? Mayr devises a story — sensible, though empirically wrong in this case — and regards such a hypothetical claim for plausibility as an adequate reason to affirm a selectionist cause. (The average increase may have been as small as the figure cited by Mayr, but horses did not change in anagenetic continuity at constant rates. Horses probably evolved predominantly by punctuated equilibrium — see Prothero and Shubin, 1989). The average of a millimeter per million years represents a meaningless amalgam of geological moments of rapid change during speciation mixed with long periods of stasis: “An increase in tooth length (hysodontry) was a selective advantage to primitive horses shifting from browsing to grazing in an increasingly arid environment. However, such a change in feeding habits required a larger jaw and stronger jaw muscle, hence a bigger and heavier skull supported by heavier neck muscles, as well as shifts in the intestinal tract. Too rapid an increase in tooth length was consequently opposed by selection, and indeed the increase averaged only about 1 millimeter per million years” (1963, p. 238) (Gould 2002: 540)

(….) [T]he synthesis can no longer assert full sufficiency to explain evolution at all scales…. I advance this opinion only with respect to a particular, but … quite authoritative, definition of the synthesis…. The definition begins Mayr’s chapter on “species and transspecific evolution” from his 1963 classic… Mayr wrote …: “The proponents of the synthetic theory maintain that all evolution is due to the accumulation of small genetic changes, guided by natural selection, and that transspecific evolution is nothing but an extrapolation and magnification of the events that take place within populations and species.” (Gould 2002: 1003)

(….) The discovery [evo-devo] that has so discombobulated the confident expectations of orthodox theory can be stated briefly and baldly: the extensive “deep homology” now documented in both the genetic structure and developmental architecture of phyla separated at least since the Cambrian explosion (ca. 530 million years ago) should not, and cannot, exist under conventional concepts of natural selection as the dominant cause of evolutionary change. (Gould 2002: 1065)

(….) Darwinian biology attributes the origin of shared homologous characters to ordinary adaptation by natural selection in a common ancestor. Moreover, homologous characters not only continue to express their adaptive origin, but also remain fully subject to further adapative change — even to the point of losing their ready identity as homologies — if they become inadaptive in the environment of any descendent lineage. Homological similarity in related taxa living in different environments therefore indicates a lack of selective pressure for alteration, not a limitation upon the power of selection to generate such changes. (At the Chicago Macroevolution meeting in 1980, for example, Maynard Smith acknowledged the allometric basis of many homologies, but stated that the attribution of such similarity to “developmental constraint” would represent what he proposed to christen as the “Gould-Lewontin fallacy” — for natural selection can unlock any inherited developmental correlation if adaptation to immediate environment favors such an alteration.) (Gould 2002: 1065-1066)

(….) Second, homological holds must be limited in taxonomic and structural extent to close relatives of similar Bauplan and functional design. The basic architectural building blocks of life — the DNA code, or the biomolecular structure of fundamental organic compounds for example — may be widely shared by homology among phyla. But the particular blueprints of actual designs and the pathways of their construction … must be limited to clades of closer relationship. (Gould 2002: 1066)

(….) Any wider hold of homology [which has already occurred] would have to inspire suspicions that the central tenet of orthodox Darwinism can no longer be sustained: the control of rates and directions of evolutionary change by the functional force of natural selection. In a particularly revealing quote within the greatest summary document of the Modern Synthesis, for example, Mayr … formulated the issue in a forthright manner. After all, he argued, more than 500 million years of independent evolution must erase any extensive genetic homology among phyla if natural selection holds such power to generate favorable change [novelty]. Adaptive evolution, over these long intervals, must have crafted and recrafted every genetic locus, indeed every nucleotide position, time and time again to meet the constantly changing selective requirements of continually varying environments. At this degree of cladistic separation, any independently evolved phenotypic similarity in basic adaptive architecture must represent the selective power of separate shaping by convergence, and cannot record conserved influence of retained genetic sequences, or common generation by parallelism: “In the early days of Mendelism there was much search for homologous genes that would account for such similarities. Much that has been learned about gene physiology makes it evident that the search for homologous genes is quite futile except in very close relatives.” (Gould 2002: 1066)

But we now know that extensive genetic homology for fundamental features of development does hold across the most disparate animal phyla. For an orthodox Darwinian functionalist, only one fallback position remains viable in this new and undeniable light… One can admit the high frequency and great importance of such genetic constraints (and also designate their discovery as stunningly unexpected), while continuing to claim that natural selection holds exclusive sway over evolutionary change because deep homology only imposes limits upon styles and ranges of developmental pathways, but cannot power any particular phyletic alteration. Natural selection can still reign supreme as the pool cue of actual evolutionary motion. (Gould 2002: 1066-1067)

But a formalist defender of positive constraint will reply that such unanticipated deep homology also channels change in positive ways — and that the key to this central argument resides in an old distinction that, unfortunately, cannot be matched for both conceptual and terminological confusion, and for consequent failure of most evolutionists to engage in the issue seriously: namely, the differences in causal meaning (not just in geometric pattern) between parallelism and convergence. (Gould 2002: 1067)

(….) But — and now we come to the nub of the issue, and to the central role of positive developmental constraint as a major challenge to selectionist orthodoxy — the attribution of similar evolutionary changes in independent lineages to internal constraint of homologous genes and developmental pathways, and not only to an external impetus of common selective pressures, must be limited to very close relatives still capable of maintaining substantial genetic identity as a consequence of recent common ancestry. Mayr’s characterization of selectionist orthodoxy comes again to mind: distantly related lineages cannot be subject to such internal limitation or channeling because the pervasive scrutiny and ruthless efficiency of natural selection, operating on every feature over countless generations in geological immensity, must have fractured any homological hold by underlying genes and developmental pathways over the freedom of phenotypes to follow wherever selection leads. (Gould 2002: 1067)

Darwin’s famous words, so often quoted, haunt the background of this discussion (1859, p. 84): “It may be said that natural selection is daily and hourly scrutinizing, throughout the world, every variation, even the slightest; rejecting that which is bad, preserving and adding up all that is good; silently and insensibly working, whenever and wherever opportunity offers, at the improvement of each organic being in relation to its organic and inorganic conditions of life.” (Gould 2002: 1068)

Therefore, an uncannily detailed phenotypic similarity evolved between distantly related groups must arise by convergence from substrates of non-homologous genotypes thus affirming our usual view of selection’s overarching power, especially if common function for the two similar forms can validate the hypothesis of generation within a comparable adaptational matrix. (Note the logical danger of circularity that intrudes upon the argument at this point, for this extent of detailed similarity the very datum that, in an unbiased approach, would lead one to entertain parallelism based upon common internal constraint as a viable alternative to convergence based on similar adaptive needs now becomes an a priori affirmation of selection’s power, the hypothesis supposedly under test.) (Gould 2002: 1068)

For this reason, such detailed functional and structural similarities, evolved independently in distantly related lineages, have become “poster boy” examples of convergence itself the “poster boy” phenomenon and general concept for showcasing selection’s dominant sway precisely because similarities evolved in this mode cannot, by Mayr’s argument, be ascribed to parallelism based on positive constraint imposed by homologous genetic and developmental pathways. With internal channeling thus theoretically barred as a potential source of impressive similarity, convergence becomes the favored explanation by default. The argument, surely “tight” in logic and principle, seems incontrovertible. (Gould 2002: 1068)

(….) [O]ne of the major discoveries of evo-devo has revealed a deep genetic homology underlying and promoting the separate evolution of lens eyes in cephalopods and vertebrates…. [B]oth phyla share key underlying genes and developmental pathways as homologies, and the example [of ‘convergence’] has lost its former status as the principle textbook case of natural selection’s power to craft stunning similarities from utterly disparate raw materials. (Gould 2002: 1069)

With this “one liner” of maximal force evo-devo has reinterpreted several textbook examples of convergence as consequences of substantial parallelism we can encapsulate the depth of theoretical disturbance introduced by this subject into the heart of Darwinian theory. Our former best exaples of full efficacy for the functional force of natural selection only exist because internal constraints of homologous genes and developmental pathways have kept fruitful channels of change open and parallel, even in the most disparate and most genealogically distant bilaterian phyla. The homological hold of historical constraint channels change at all levels, even for the broadest patterning of morphospace, and not only for details of parallel evolution in very closely related groups. (Gould 2002: 1069)

(….) [P]arallelism marks the formal influence of internal constraint, while convergence reflects the functional operation of natural selection upon two substrates different enough to exclude internal factors as influences upon the resulting similarity. This recognition of internal channeling as the root cause of parallelism — the principle basis for ascribing evolutionary change, and not only limitation, to historical constraint — lies at the heart of evo-devo’s theoretical novelty and importance to the Darwinian worldview. (Gould 2002: 1075)

(….) I began this “symphony” of evo-devo with a quotation from one of the great architects of the Modern Synthesis — Mayr’s statement, based on adaptationist premises then both reasonable and conventional, that any search for genetic homology between distantly-related animal phyla would be doomed a priori and in theory by selection’s controlling power, a mechanism that would surely recycle every nucleotide position (often several times) during so long a period of independent evolution between two lines. The new data of evo-devo have falsified this claim and revised our basic theory to admit a great, and often controlling, power for historical constraints based on conserved developmental patterns coed by the very genetic homologies that Mayr had deemed impossible. (Gould 2002: 1175)

(….) The argument that structural and morphological archetypes underlie, and actively generate, a basic and common architecture in taxonomically distant groups defines — both as a fact of our profession’s actual history and as a dictate of the logic of our explanatory theories — the strongest kind of claim for developmental constraint as a major factor in patterns of evolutionary change and the occupation of morphospace. I suspect that the depth of this challenge has always been recognized, but the empirical case for such constraining archetypes has remained weak, since the heyday of Geoffroy and Own some 150 years ago, that the issue simply didn’t generate much serious concern — and rightly so.

The concept of interphylum archetypes, deemed too bizarre to warrant active refutation, experienced the curt and derisive dismissal reserved for crackpot ideas in science. (Goldschmidt’s saltational apostasy, on the other hand, inspired voluminous and impassioned denial because his ideas did seem sufficiently and dangerously plausible to the Modern Synthesis — see pp. 451-466). Indeed, the notion of interphylum archetypes struck most biologists as so inconceivable in theory that empirical counterclaims hardly seemed necessary. After all, the notion required extensive genetic homology among phyla, and the power of natural selection, working on different paths for minimum of 530 million years since the origin of distinct phyla in the Cambrian explosion, seemed to guarantee such thorough change at effectively every nucleotide position that the requisite common foundation could not possibly have been maintained (see Mayr, 1963, p. 609, as previously discussed on pp. 539 and 1066).

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No case has received more attention, generated more surprise, rested upon firmer data, or so altered previous “certainties,” than the discovery of an important and clearly homologous developmental pathway underlying the ubiquitous and venerable paradigm of convergence in our textbooks: the independent evolution of image-forming lens eyes in several phyla, with the stunning anatomical similarities of single-lens eyes in cephalopods and vertebrates as the most salient illustration. As Tomarev et al. (1997, p. 2421) write: “The complex eyes of cephalopod mollusks and vertebrates have been considered a classical example of convergent evolution.” (….)

PARALLELISM IN THE LARGE: PAX-6 AND THE HOMOLOGY OF DEVELOPMENTAL PATHWAYS IN HOMOPLASTIC EYES OF SEVERAL PHYLA

DATA AND DISCOVERY. Salvini-Plawen and Mayer (1977), in a classical article nearly always cited in this context, argued that photoreceptors of some form have evolved independently some 40 to 60 times among animals, with six phyla developing complex image-forming eyes, ranging from cubomedusoids among the Cnidaria, through annelids, onychophores, arthropods and mollusks to vertebrates along the conventional chain of life. In the early 1990s, using Drosophila probes, researchers cloned a family of mammalian Pax genes, most notably Pax-6, which includes both a paired box and homeobox (Walther and Gruss, 1991). (….) The similar function of these Pax-6 homologs in different phyla was then dramatically affirmed by expressing the mouse gene in Drosophila (Halder et al., 1995), and finding that the mammalian version could still induce the formation of normal fly eyes. (….) [T]he Pax-6 story has now furnished an important homological basis in underlying developmental pathways for generating complex eyes in cephalopods and vertebrates. Thus, a channel of inherited internal constraint has strongly facilitated the resulting, nearly identical solution in two phyla, and evolutionists can no longer argue that such similar eyes originated along entirely separate routes, directed only by natural selection, and without benefit of any common channel of shared developmental architecture. But just as the advocates of pure convergence erred in claiming exclusive rights of explanation, the discovery of Pax-6 homologies does not permit a complete flip to exclusive explanation by constraint. (Gould 2002: 1123-1128)

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[Gold reminds us we must not forget] … the striking reformation of evolutionary theory implied by the well-documented genetic and developmental homologies alone. De Robertis expresses this key argument in the final line of his 1997 article on the ancestry of segmentation: “The realization that all Bilateria are derived from a complex ancestor represents a major change in evolutionary thinking, suggesting that the constraints imposed by the previous history of species played a greater role in the outcome of animal evolution than anyone would have predicted until recently.” (Gould 2002: 1152) [De Robertis, E.M. 1997. The ancestory of segmentation. Nature 387: 25-26. See also, De Robertis, E.M., G. Oliver, and C.V.E. Wright. 1990. Homeobox genes and the vertebrate body plan. Scientific American, July, pp. 46-52; De Robertis, E.M., and Y. Sasai. 1996. A common plan for dorsoventral patterning in Bilateria. Nature 380: 37-40.]

(….) Hughes (2000, p. 65) has expressed this cardinal discovery of evo-devo in phyletic and paleontological terms: “It is hard to escape the suspicion that what we witness in the Cambrian is mainly tinkering with developmental systems already firmly established by the time these Cambrian beasts showed up.” (Gould 2002: 1155) [Hughes, N.C. 2000. The rocky road to Mendal’s play. Evol. and Develop. 2: 63-66.]