All major theories of speciation maintain that splitting takes place rapidly in very small populations. The theory of geographic, or allopatric, speciation is preferred by most evolutionists for most situations (allopatric means “in another place”).* A new species can arise when a small segment of the ancestral population is isolated at the periphery of the ancestral range. Large, stable central populations exert a strong homogenizing influence. New and favorable mutations are diluted by the sheer bulk of the population through which they must spread. They may build slowly in frequency, but changing environments usually cancel their selective value long before they reach fixation. Thus, phyletic transformation in large populations should be very rare—as the fossil record proclaims.
But small, peripherally isolated groups are cut off from their parental stock. They live as tiny populations in geographic corners of the ancestral range. Selective pressures are usually intense because peripheries mark the edge of ecological tolerance for ancestral forms. Favorable variations spread quickly. Small, peripheral isolates are a laboratory of evolutionary change.
What should the fossil record include if most evolution occurs by speciation in peripheral isolates? Species should be static through their range because our fossils are the remains of large central populations. In any local area inhabited by ancestors, a descendent species should appear suddenly by migration from the peripheral region in which it evolved. In the peripheral region itself, we might find direct evidence of speciation, but such good fortune would be rare indeed because the event occurs so rapidly in such a small population. Thus, the fossil record is a faithful rendering of what evolutionary theory predicts, not a pitiful vestige of a once bountiful tale.
Eldredge and I refer to this scheme as the model of punctuated equilibria. Lineages change little during most of their history, but events of rapid speciation occasionally punctuate this tranquillity. Evolution is the differential survival and deployment of these punctuations. (In describing the speciation of peripheral isolates as very rapid, I speak as a geologist. The process may take hundreds, even thousands of years; you might see nothing if you stared at speciating bees on a tree for your entire lifetime. But a thousand years is a tiny fraction of one percent of the average duration for most fossil invertebrate species—5 to 10 million years. Geologists can rarely resolve so short an interval at all; we tend to treat it as a moment.)
If gradualism is more a product of Western thought than a fact of nature, then we should consider alternate philosophies of change to enlarge our realm of constraining prejudices. In the Soviet Union, for example, scientists are trained with a very different philosophy of change—the so-called dialectical laws, reformulated by Engels from Hegel’s philosophy. The dialectical laws are explicitly punctuational. They speak, for example, of the “transformation of quantity into quality.” This may sound like mumbo jumbo, but it suggests that change occurs in large leaps following a slow accumulation of stresses that a system resists until it reaches the breaking point. Heat water and it eventually boils. Oppress the workers more and more and bring on the revolution. Eldredge and I were fascinated to learn that many Russian paleontologists support a model similar to our punctuated equilibria.
I emphatically do not assert the general “truth” of this philosophy of punctuational change. Any attempt to support the exclusive validity of such a grandiose notion would border on the nonsensical. Gradualism sometimes works well. (I often fly over the folded Appalachians and marvel at the striking parallel ridges left standing by gradual erosion of the softer rocks surrounding them.) I make a simple plea for pluralism in guiding philosophies, and for the recognition that such philosophies, however hidden and unarticulated, constrain all our thought. The dialectical laws express an ideology quite openly; our Western preference for gradualism does the same thing more subtly.
Nonetheless, I will confess to a personal belief that a punctuational view may prove to map tempos of biological and geologic change more accurately and more often than any of its competitors—if only because complex systems in steady state are both common and highly resistant to change. As my colleague British geologist Derek V. Ager writes in supporting a punctuational view of geologic change: “The history of any one part of the earth, like the life of a soldier, consists of long periods of boredom and short periods of terror.”
18 | Return of the Hopeful Monster
BIG BROTHER, THE tyrant of George Orwell’s 1984, directed his daily Two Minutes Hate against Emmanuel Goldstein, enemy of the people. When I studied evolutionary biology in graduate school during the mid-1960s, official rebuke and derision focused upon Richard Goldschmidt, a famous geneticist who, we were told, had gone astray. Although 1984 creeps up on us, I trust that the world will not be in Big Brother’s grip by then. I do, however, predict that during this decade Goldschmidt will be largely vindicated in the world of evolutionary biology.
Goldschmidt, a Jewish refugee from Hitler’s decimation of German science, spent the remainder of his career at Berkeley, where he died in 1958. His views on evolution ran afoul of the great neo-Darwinian synthesis forged during the 1930s and 1940s and continuing today as a reigning, if insecure, orthodoxy. Contemporary neo-Darwinism is often called the “synthetic theory of evolution” because it united the theories of population genetics with the classical observations of morphology, systematics, embryology, biogeography, and paleontology.
The core of this synthetic theory restates the two most characteristic assertions of Darwin himself: first, that evolution is a two-stage process (random variation as raw material, natural selection as a directing force); secondly, that evolutionary change is generally slow, steady, gradual, and continuous.
Geneticists can study the gradual increase of favored genes within populations of fruit flies in laboratory bottles. Naturalists can record the steady replacement of light moths by dark moths as industrial soot blackens the trees of Britain. Orthodox neo-Darwinians extrapolate these even and continuous changes to the most profound structural transitions in the history of life: by a long series of insensibly graded intermediate steps, birds are linked to reptiles, fish with jaws to their jawless ancestors. Macroevolution (major structural transition) is nothing more than microevolution (flies in bottles) extended. If black moths can displace white moths in a century, then reptiles can become birds in a few million years by the smooth and sequential summation of countless changes. The shift of gene frequencies in local populations is an adequate model for all evolutionary processes—or so the current orthodoxy states.
The most sophisticated of modern American textbooks for introductory biology expresses its allegiance to the conventional view in this way:
[Can] more extensive evolutionary change, macroevolution, be explained as an outcome of these micro-evolutionary shifts? Did birds really arise from reptiles by an accumulation of gene substitutions of the kind illustrated by the raspberry eye-color gene?
The answer is that it is entirely plausible, and no one has come up with a better explanation…. The fossil record suggests that macroevolution is indeed gradual, paced at a rate that leads to the conclusion that it is based upon hundreds or thousands of gene substitutions no different in kind from the ones examined in our case histories.
Many evolutionists view strict continuity between micro-and macroevolution as an essential ingredient of Darwinism and a necessary corollary of natural selection. Yet, as I argue in essay 17, Thomas Henry Huxley divided the two issues of natural selection and gradualism and warned Darwin that his strict and unwarranted adherence to gradualism might undermine his entire system. The fossil record with its abrupt transitions offers no support for gradual change, and the principle of natural selection does not require it—selection can operate rapidly. Yet the unnecessary link that Darwin forged became a central tenet of the synthetic theory.
Goldschmidt raised no objection to the standard accounts of microevolution; he devoted the first half of his major work, The Material Basis of Evolution (Yale Universit
y Press, 1940), to gradual and continuous change within species. He broke sharply with the synthetic theory, however, in arguing that new species arise abruptly by discontinuous variation, or macromutation. He admitted that the vast majority of macromutations could only be viewed as disastrous—these he called “monsters.” But, Goldschmidt continued, every once in a while a macromutation might, by sheer good fortune, adapt an organism to a new mode of life, a “hopeful monster” in his terminology. Macroevolution proceeds by the rare success of these hopeful monsters, not by an accumulation of small changes within populations.
I want to argue that defenders of the synthetic theory made a caricature of Goldschmidt’s ideas in establishing their whipping boy. I shall not defend everything Goldschmidt said; indeed, I disagree fundamentally with his claim that abrupt macroevolution discredits Darwinism. For Goldschmidt also failed to heed Huxley’s warning that the essence of Darwinism—the control of evolution by natural selection—does not require a belief in gradual change.
As a Darwinian, I wish to defend Goldschmidt’s postulate that macroevolution is not simply microevolution extrapolated, and that major structural transitions can occur rapidly without a smooth series of intermediate stages. I shall proceed by discussing three questions: (1) can a reasonable story of continuous change be constructed for all macroevolutionary events? (my answer shall be no); (2) are theories of abrupt change inherently anti-Darwinian? (I shall argue that some are and some aren’t); (3) do Goldschmidt’s hopeful monsters represent the archetype of apostasy from Darwinism, as his critics have long maintained? (my answer, again, shall be no).
All paleontologists know that the fossil record contains precious little in the way of intermediate forms; transitions between major groups are characteristically abrupt. Gradualists usually extract themselves from this dilemma by invoking the extreme imperfection of the fossil record—if only one step in a thousand survives as a fossil, geology will not record continuous change. Although I reject this argument (for reasons discussed in essay 17), let us grant the traditional escape and ask a different question. Even though we have no direct evidence for smooth transitions, can we invent a reasonable sequence of intermediate forms—that is, viable, functioning organisms—between ancestors and descendants in major structural transitions? Of what possible use are the imperfect incipient stages of useful structures? What good is half a jaw or half a wing? The concept of preadaptation provides the conventional answer by permitting us to argue that incipient stages performed different functions. The half jaw worked perfectly well as a series of gill-supporting bones; the half wing may have trapped prey or controlled body temperature. I regard preadaptation as an important, even an indispensable, concept. But a plausible story is not necessarily true. I do not doubt that preadaptation can save gradualism in some cases, but does it permit us to invent a tale of continuity in most or all cases? I submit, although it may only reflect my lack of imagination, that the answer is no, and I invoke two recently supported cases of discontinuous change in my defense.
On the isolated island of Mauritius, former home of the dodo, two genera of boid snakes (a large group that includes pythons and boa constrictors) share a feature present in no other terrestrial vertebrate: the maxillary bone of the upper jaw is split into front and rear halves, connected by a movable joint. In 1970, my friend Tom Frazzetta published a paper entitled “From Hopeful Monsters to Bolyerine Snakes?” He considered every preadaptive possibility he could imagine and rejected them in favor of discontinuous transition. How can a jawbone be half broken?
Many rodents have cheek pouches for storing food. These internal pouches connect to the pharynx and may have evolved gradually under selective pressure for holding more and more food in the mouth. But the Geomyidae (pocket gophers) and Heteromyidae (kangaroo rats and pocket mice) have invaginated their cheeks to form external fur-lined pouches with no connection to the mouth or pharynx. What good is an incipient groove or furrow on the outside? Did such hypothetical ancestors run about three-legged while holding a few scraps of food in an imperfect crease with their fourth leg? Charles A. Long has recently considered a suite of preadaptive possibilities (external grooves in burrowing animals to transport soil, for example) and rejected them all in favor of discontinuous transition. These tales, in the “just-so story” tradition of evolutionary natural history, do not prove anything. But the weight of these, and many similar cases, wore down my faith in gradualism long ago. More inventive minds may yet save it, but concepts salvaged only by facile speculation do not appeal much to me.
If we must accept many cases of discontinuous transition in macroevolution, does Darwinism collapse to survive only as a theory of minor adaptive change within species? The essence of Darwinism lies in a single phrase: natural selection is the major creative force of evolutionary change. No one denies that natural selection will play a negative role in eliminating the unfit. Darwinian theories require that it create the fit as well. Selection must do this by building adaptations in a series of steps, preserving at each stage the advantageous part in a random spectrum of genetic variability. Selection must superintend the process of creation, not just toss out the misfits after some other force suddenly produces a new species, fully formed in pristine perfection.
We can well imagine such a non-Darwinian theory of discontinuous change—profound and abrupt genetic alteration luckily (now and then) making a new species all at once. Hugo de Vries, the famous Dutch botanist, supported such a theory early in this century. But these notions seem to present insuperable difficulties. With whom shall Athena born from Zeus’s brow mate? All her relatives are members of another species. What is the chance, of producing Athena in the first place, rather than a deformed monster? Major disruptions of entire genetic systems do not produce favored—or even viable—creatures.
But all theories of discontinuous change are not anti-Darwinian, as Huxley pointed out nearly 120 years ago. Suppose that a discontinuous change in adult form arises from a small genetic alteration. Problems of discordance with other members of the species do not arise, and the large, favorable variant can spread through a population in Darwinian fashion. Suppose also that this large change does not produce a perfected form all at once, but rather serves as a “key” adaptation to shift its possessor toward a new mode of life. Continued success in this new mode may require a large set of collateral alterations, morphological and behavioral; these may arise by a more traditional, gradual route once the key adaptation forces a profound shift in selective pressures.
Defenders of the modern synthesis have cast Goldschmidt as Goldstein by linking his catchy phrase—hopeful monster—to non-Darwinian notions of immediate perfection by profound genetic change. But this is not entirely what Goldschmidt maintained. In fact, one of his mechanisms for discontinuity in adult forms relied upon a notion of small underlying genetic change. Goldschmidt was a student of embryonic development. He spent most of his early career studying geographic variation in the gypsy moth, Lymantria dispar. He found that large differences in the color patterns of caterpillars resulted from small changes in the timing of development: the effects of a slight delay or enhancement of pigmentation early in growth increased through ontogeny and led to profound differences among fully grown caterpillars.
Goldschmidt identified the genes responsible for these small changes in timing, and demonstrated that large final differences reflected the action of one or a few “rate genes” acting early in growth. He codified the notion of a rate gene in 1918 and wrote twenty years later:
The mutant gene produces its effect…by changing the rates of partial processes of development. These might be rates of growth or differentiation, rates of production of stuffs necessary for differentiation, rates of reactions leading to definite physical or chemical situations at definite times of development, rates of those processes which are responsible for segregating the embryonic potencies at definite times.
In his infamous book of 1940, Goldschmidt specifically invokes rate gene
s as a potential maker of hopeful monsters: “This basis is furnished by the existence of mutants producing monstrosities of the required type and the knowledge of embryonic determination, which permits a small rate change in early embryonic processes to produce a large effect embodying considerable parts of the organism.”
In my own, strongly biased opinion, the problem of reconciling evident discontinuity in macroevolution with Darwinism is largely solved by the observation that small changes early in embryology accumulate through growth to yield profound differences among adults. Prolong the high prenatal rate of brain growth into early childhood and a monkey’s brain moves toward human size. Delay the onset of metamorphosis and the axolotl of Lake Xochimilco reproduces as a tadpole with gills and never transforms into a salamander. (See my book Ontogeny and Phylogeny [Harvard University Press, 1977] for a compendium of examples, and pardon me for the unabashed plug.) As Long argues for the external cheek pouch: “A genetically controlled developmental inversion of the cheek pouch may have occurred, recurred, and persisted in some populations. Such a morphological change would have been drastic in effect, turning the pockets ‘wrong side out’ (furry side in), but nevertheless it would be a rather simple embryonic change.”
Indeed, if we do not invoke discontinuous change by small alteration in rates of development, I do not see how most major evolutionary transitions can be accomplished at all. Few systems are more resistant to basic change than the strongly differentiated, highly specified, complex adults of “higher” animal groups. How could we ever convert an adult rhinoceros or a mosquito into something fundamentally different. Yet transitions between major groups have occurred in the history of life.