The Structure of Evolutionary Theory

by Stephen Jay Gould

  For a final factor among limiting constraints (in this abbreviated list), brakes on development act strongly at both levels (line IVB4). Ever since the inception of modern embryology, von Baer's (1828) laws have defined the hold placed by ontogenetic intricacy upon potentials for change in complex Metazoa. At the species level, the hold of homology (as expressed in all the factors, genetic and otherwise, that limit the amount of change per speciation event) functions as a developmental constraint in the same basic manner — that is, by limiting the difference that can separate a parent and its immediate offspring.

  All these sources of limitation also contribute to the more important posi­tive aspects of constraint, as channeling or enhancing preferred directions for change. In the category of positive channeling by structure (line IVB5), onto­genetic pathways already established in the lives of organisms provide by extension, or by relative shuffling of rates among components (see Gould, 1977b), the classic mode of constrained and substantial change in organismic evolution — thus explaining the importance of heterochrony as a morphogenetic phenomenon (Jones and Gould, 1999; McNamara and McKinney, 1991). At the upper level of speciational trends within clades, structural rules and differential ease of modifiability among parts and correlations of Bauplan play the same role of directing and accelerating change along cer­tain preferred pathways. Liem (1973), for example, showed how a set of small and accessible changes in a jaw muscle, the fourth levator externi, could greatly alter the adaptive feeding devices of cichlid fishes (but not of other re­lated groups), thus helping to explain the rapidly evolved species flocks of this clade in several African lakes.

  In a second category of positive channeling by directed variability from lev­els below, the organismic level experiences no important effect because such drives will generally be suppressed by organismic selection. But the driving [Page 741] force of directional speciation can greatly enhance and channel cladal trends by working synergistically with such species-level modes of change as species selection.

  Perhaps the most important positive constraint, acting similarly at both levels, lies in the large size of “exaptive pools” (see full discussion in Chapter 11), or nonrandom variation made available through evolutionary processes acting on other features or at other levels, but later exploitable by organisms or species for their own exaptive benefits. The redundancy supplied by ge­netic duplication for organismal flexibility serves as the classic illustration of this phenomenon at the traditional level of natural selection. The exaptive pool of the species level may become even larger because species do not sup­press lower levels of change, while these genic and organismal directionalities frequently act in synergism with advantages at the species level (see Gould and Lloyd, 1999, for a detailed development of this argument).

  Summary comments on the strengths of species selection and its

  interaction with other macroevolutionary causes of change

  Species selection, the Darwinian analog at this higher level, but by no means the only irreducible force of macroevolutionary change, differs from conven­tional natural selection at the organismic level both in character and in gen­eral strength. The major aspect of character — as I have emphasized through­out this chapter in stressing the non-fractality of hierarchical levels — lies in the potency of species selection for governing “what species do.” Species se­lection does not, and cannot, build the complex adaptive phenotypes of or­ganisms, but this common statement only recognizes the general nature of hi­erarchical organization and does not represent a fair criticism of the efficacy of species selection, despite the claims of Dawkins (1982) and others (see p. 711 for a discussion of this point).

  The primary force of species selection lies in its power to promote trends within clades, and to regulate the waxing and waning of differential spe­cies diversity within and among clades through time. The influence of species selection upon trends will also be enhanced because this process not only builds trends in species-level characters directly, but also establishes corre­lated trends in any character of the organismal phenotype that either helps to determine the species-level property, or merely hitchhikes upon the trend by linkages of homology within the phylogenetic structure of evolutionary trees — a very common phenomenon, as Raup and Gould, 1974, showed in theory and practice. This insight about trends, which I shall explore more thoroughly in the next chapter (pp. 886–893), may provide a key for explain­ing one of the most puzzling phenomena in paleontology — persistent and pervasive cladal trends (such as decreasing stipe number in graptolites, or in­creasing symmetry of crinoidal cups) that have defied all attempts at explana­tion in traditional terms of biomechanical advantages to organisms.

  As for general strength, species selection (in primary comparison with the traditional level of Darwinian natural selection on organisms) includes certain [Page 742] features that diminish its influence, and others that enhance its power. Among factors that weaken the potential of species selection, we may men­tion:

  (1) The generally low population size of species in clades, and the generally long life of species-individuals, both factors limiting the amount of variation usually available for a process of selection.

  (2) Unlike the organism, the species-individual does not actively suppress selection at lower levels within itself. Since the individuals of lower levels, by their shorter cycle times, present much more variation for selection (per given unit of time), this unsuppressed lower-level selection may overwhelm the op­eration of species selection.

  (3) Species selection, as the analog of asexual reproduction at the organismal level, becomes subject to the same important limit that favorable traits arising in one individual cannot be transferred laterally (for mixing and matching) to other individuals, but only vertically to direct descendants.

  (4) Species selection is limited by particular structural constraints, encountered only at this higher level, most notably the apparently unbreakable correlation between origination and extinction rates, thus tying together by negative interaction the very two phenomena that, if positively associated — that is, high speciation with low extinction — could so powerfully accelerate any trend produced by species selection.

  But several features that grant potential strength to species selection will counteract these negative forces and limits:

  (1) Species selection may be theoretically weak relative to the power of transformation by continuous selection of lower-level individuals (organisms in this case) within species. But, in fact, such transformation by anagenesis rarely occurs in nature, as the great majority of species exhibit stasis during their geological lifetimes. With general anagenesis usually weak or inopera­tive, and with effective organismal selection concentrated at the origin of new species and their differentia (and thus also limited to the cycle time of species themselves), species selection can become a predominant process.

  (2) The population size of species in clades may be low, but each event of speciation must produce difference from parental traits (at least enough to yield reproductive isolation) — whereas events of organismal birth need not add any new variation to the population. The amount of change per speciational event may be large, even providing a potential macroevolutionary ana­log to macromutation. (At such a point, however, we must also allow some possible weakening of selection's power as well, for macromutation, by pro­ducing a completed form of change in one step, deprives selection of its cre­ative role in building adaptation gradually — see Chapter 2.)

  (3) At the species level, not only does each birth of a new individual include novel variation that may be substantial, but the variation also arises in an adaptive context (whereas mutation, the source of variation at the organismic level, will usually be detrimental to the organism). Of course, the adaptive component in the production of a new species-individual need only exist at the level of its own causal origin — often the organismal level, rather than the [Page 743] species level itself. But the new variation will often be adaptive
at the species level for two reasons: first, because species-level rather than organismic pro­cesses often underlie the genesis of the variation; and second, because var­iation caused at the organismic level will often be synergistic with species advantages, whereas mutational variation rarely enjoys synergism with the benefits of organisms.

  (4) The common synergism of organismal with species advantages pro­duces a powerful acceleration of macroevolution (Gould and Lloyd, 1999). Drives of directional speciation (often based on organismal adaptation) fre­quently foster species selection along the same pathway by accelerating the speciation rate or, perhaps more commonly, by enhancing the longevity of species arising in the direction of the drive. On the other hand, when or­ganismal selection runs counter to the interests of species, negative species se­lection may provide the only effective higher-level force that can act as a gov­ernor to slow or stymie the trend — probably a common feature in phylogeny, and previously given (in textbooks of my student days, but now rarely used) the unfelicitous and unfortunate name of “overspecialization.”

  As a final point and guide to understanding the essential role of the species-individual in macroevolution, we must remind ourselves of the highly un­usual character of the individual conventionally (and usually unthinkingly) taken as a paradigm for all evolutionary causality — the organism. If we view evolutionary change as tripartite in causal nature — with drive, selection, and drift as the three major modes — then we may say that the organism allows se­lection to reign nearly supreme by “clearing out” the surrounding space of the other two processes. Drives do not seem important at the organismal level, because drives emerge from below, and organisms, as repeatedly em­phasized in this chapter, work so effectively as suppressors of lower-level se­lection. At the same time, drift produces limited impact at the organismal level because population sizes tend to be too large in most circumstances, and because the high degree of functional integration within organisms grants a selective significance to nearly every part, thus lowering the relative frequency of substantial neutrality in potential sites for drift. Therefore, selection based on organismal properties reigns at this canonical level — thus engendering the two great parochial prejudices of the strict Darwinian world view: the adaptationist program as a guide to nearly all evolutionary phenomena, and the virtual restriction of causality to natural selection working at the single level of organisms (two of the three legs of Darwin's tripod in the terms of this book).

  But when we turn to the species level, we find an interesting partnership among the three causal forces of drive, selection and drift. Selection at the species level does not “clear out” these surrounding forces. Drives from be­low exert great influence in the phenomenon of directional speciation. Drift maintains similar impact in both its major manifestations: as species drift for the transformation of collectivities (clades); and as founder drift in differen­tial proliferation or reduction of subclades by accidents of propitious or limit­ing colonization. This absence of “clearing out” denotes no failure or weakness [Page 744] of selection at the species level, but should rather be viewed as a different “strategy” for the distinct and effective world of macroevolution. Higher-level selection does not bestride this larger world like the colossus of its ana­log at the organismal level. But higher-level selection gains a different kind of strength and interest in its fascinating and fruitful synergism (and opposition) with drives from below and with drift in the collegiality of its own domain.

  [Page 745]

  CHAPTER NINE

  Punctuated Equilibrium

  and the Validation of

  Macroevolutionary Theory

  What Every Paleontologist Knows

  AN INTRODUCTORY EXAMPLE

  If Hugh Falconer (1808-1865) had not died before writing his major and synthetic works, he might be remembered today as perhaps the greatest verte­brate paleontologist of the late 19th century. Falconer went to India in 1830 as a surgeon for the East India Company, but spent most of his time as a natu­ralist in two very different realms. In 1832, he became superintendent of the botanical garden at Saharanpur, at the base of the Siwaliks, a “foothill” range of the Himalayas. There he played a major role in fostering the cultivation of Indian tea, but he also collected and described one of the most famous and important of all fossil faunas, the Tertiary mammalian remains of the Siwalik Hills. Broken health forced a return to England in 1842, where he worked for several years on the collection of Indian fossils at the British Museum. He then returned to India, this time as professor of botany at Calcutta Medical College, but declining health forced his permanent repatriation to England in 1855. During the last decade of his life, Falconer studied the late Tertiary and Quaternary mammals of Europe and North America, particularly the history of fossil elephants.

  Colleagues revered Falconer for his prodigious memory, his gargantuan capacity for work, and his inexhaustible attention to the minutest details. Dar­win, as discussed in Chapter 1 (pp. 1–6), held immense respect for Falconer, and invested much hope and trepidation in the prospect that such a master of detail might be persuaded about the probable truth of evolution.

  Among all his observations and general conclusions, Falconer took greatest interest in the stability he observed in species of fossil vertebrates, often through long geological periods, and across such maximal changes of envi­ronment as the recent glacial ages. Falconer, of course, began with the usual assumption that such stability implied creation and permanence of species. Darwin included him among the great paleontologists who supported such a view. Noting the strength of this opposition to evolution, Darwin wrote [Page 746] (1859, p. 310): “We see this in the plainest manner by the fact that all the most eminent paleontologists, namely Cuvier, Agassiz, Barrande, Falconer, E. Forbes, etc. ... have unanimously, often vehemently, maintained the immuta­bility of species.”

  Darwin sent Falconer a copy of the first edition of the Origin of Species, preceded by the following note (letter of November 11, 1859): “Lord, how savage you will be, if you read it, and how you will long to crucify me alive! I fear it will produce no other effect on you; but if it should stagger you in ever so slight a degree, in this case, I am fully convinced that you will become, year after year, less fixed in your belief in the immutability of species. With this au­dacious and presumptuous conviction, I remain, my dear Falconer, Yours most truly, Charles Darwin.” (Several years before, Darwin had chosen Fal­coner as one of the very few scientists to whom he confided his beliefs about evolution. Falconer had not, to say the least, reacted positively. In a letter to Hooker on October 13, 1858, Darwin had written of Falconer's jocular, but entirely serious, response: ”... dear old Falconer, who some few years ago once told me that I should do more harm than any ten other naturalists would do good, [and] that I had half-spoiled you already!”)

  Falconer wrote to Darwin on June 23, 1861, expressing his great respect (and that of so many others) for the Origin, though not his agreement: “My dear Darwin, I have been rambling through the north of Italy, and Germany lately. Everywhere have I heard your views and your admirable essay can­vassed — the views of course often dissented from, according to the special bias of the speaker — but the work, its honesty of purpose, grandeur of con­ception, felicity of illustration, and courageous exposition, always referred to in terms of the highest admiration. And among your warmest friends no one rejoiced more heartily in the just appreciation of Charles Darwin than did, Yours very truly, H. Falconer.” Darwin, greatly relieved, replied the next day: “I shall keep your note amongst a very few precious letters. Your kindness has quite touched me.”

  Hugh Falconer did reassess his worldview, and did accept the principle of evolution (though not causality by natural selection) — but only within the context of the one overarching phenomenon that so strongly governed the nature of the fossil record according to his extensive and meticulous observa­tions: the longterm stability of fossil species, even through major environ­mental changes. Fal
coner published his reassessment in an 1863 monograph entitled: “On the American fossil elephant of the regions bordering the Gulf of Mexico (E. columbi, Falc.); with general observations on the living and ex­tinct species.” But he first sent a copy of the manuscript to Darwin (on Sep­tember 24,1862), in eager anticipation of Darwin's reaction to his new views. In the first paragraph of his letter, Falconer reemphasized the stability of spe­cies through great climatic changes, arguing that any evolutionary account must deal with this primary fact of paleontology:

  Do not be frightened at the enclosure. I wish to set myself right by you before I go to press. I am bringing out a heavy memoir on elephants — an omnium gatherum affair, with observations on the fossil and recent species. [Page 747] One section is devoted to the persistence in time of the specific char­acters of the mammoth. I trace him from before the Glacial period, through it and after it, unchangeable and unchanged as far as the organs of digestion (teeth) and locomotion are concerned. Now, the Glacial pe­riod was no joke: it would have made ducks and drakes of your dear pi­geons and doves.

  Darwin, of course, was delighted. He wrote to Lyell on October 1,1862: “I found here a short and very kind note of Falconer, with some pages of his 'El­ephant Memoir,' which will be published, in which he treats admirably on long persistence of type. I thought he was going to make a good and crush­ing attack on me, but, to my great satisfaction, he ends by pointing out a loophole, and adds, ... The most rational view seems to be that they [Mam­moths] are the modified descendants of earlier progenitors, etc' This is cap­ital. There will not be soon one good paleontologist who believes in immuta­bility.”