Bully for Brontosaurus

by Stephen Jay Gould

  This volume also presents enough detail (usually lacking in technical publications) to give nonscientists a feel for the actual procedures of research, warts and all (an appropriate metaphor for the subject). Glen Ingram’s article on natural history, for example, enumerates all the day-to-day dilemmas that technical papers rarely mention: slippery bodies that elude capture; simple difficulties in seeing a small, shy frog that lives in inaccessible places (Ingram learned to identify Rheobatrachus by characteristic ripples made by its jump into water); rain, fog, and dampness; and regeneration that frustrates identification (ecologists must recognize individual animals in order to monitor size and movement of populations by mark-recapture techniques; amphibians and reptiles are traditionally marked by distinctive patterns of toe clipping, a painless and unobtrusive procedure, but Rheobatrachus frustrates tradition by regenerating its clipped toes, and Ingram could not reidentify his original captures). To this, we must add the usually unacknowledged bane of all natural history: boredom. You don’t see your animals most of the time; so you wait and wait and wait (not always pleasant on the boggy banks of a stream in rainy season). Somehow, though, such plagues seem appropriate enough, given the subject. Frogs, after all, stand among the ten Mosaic originals: “I will smite all thy borders with frogs: And the river shall bring forth frogs abundantly, which shall go up and come into thine house, and into thy bedchambers, and upon thy bed…and into thine ovens, and into thy kneading troughs” (Exod. 8:2–3).

  The biblical author of Exodus was, unfortunately, not describing Rheobatrachus, a rare animal indeed. Not a single Rheobatrachus silus has been seen in its natural habitat since 1981. A series of dry summers and late rains has restricted the range of this aquatic frog—and five years of no sitings must raise fears about extinction. Fortunately, a second species, named R. vitellinus, was discovered in January 1984, living in shallow sections of fast-flowing streams, about 500 miles north of the range of R. silus. This slightly larger version (up to three inches in length) also broods in its stomach; twenty-two baby frogs inhabited a pregnant female.

  When discussed as a disembodied oddity (the problem with traditional writing in natural history), Rheobatrachus may pique our interest but not our intellect. Placed into a proper context among other objects of nature’s diversity—the “comparative approach” so characteristic of evolutionary biology—gastric brooding in Rheobatrachus embodies a message of great theoretical interest. Rheobatrachus, in one sense, stands alone. No other vertebrate swallows its own fertilized eggs, converts its stomach into a brood pouch, and gives birth through its mouth. But in another sense, Rheobatrachus represents just one solution to a common problem among frogs.

  In his review of parental care, R. W. McDiarmid argues that frogs display “the greatest array of reproductive modes found in any vertebrates” (see his article in G. M. Burghardt and M. Bekoff, 1978). Much inconclusive speculation has been devoted to reasons for the frequent and independent evolution of brooding (and other forms of parental care) in frogs—a profound departure, after all, from the usual amphibian habit of laying eggs in water and permitting the young to pass their early lives as unattended aquatic tadpoles. Several authors have suggested the following common denominator: In many habitats, and for a variety of reasons, life as a free-swimming tadpole may become sufficiently uninviting to impose strong evolutionary pressure for bypassing this stage and undergoing “direct development” from egg to completed frog. Brooding is an excellent strategy for direct development—since tadpole life may be spent in a brood pouch, and the bad old world need not be faced directly before froghood.

  In any case, brooding has evolved often in frogs, and in an astonishing variety of modes. As a minimal encumbrance and modification, some frogs simply attach eggs to their exteriors. Males of the midwife toad Alytes obstetricans wrap strings of eggs about their legs and carry them in tow.

  At the other extreme of modification, some frogs have evolved special brood pouches in unconventional places. The female Gastrotheca riobambae, an Ecuadorean frog from Andean valleys, develops a pouch on her back, with an opening near the rear and an internal extension nearly to her head. The male places fertilized eggs in her pouch, where they develop under the skin of her back for five to six weeks before emerging as late-stage tadpoles.

  In another Australian frog, Assa darlingtoni, males develop pouches on their undersides, opening near their hind legs but extending forward to the front legs (see article by G. J. Ingram, M. Anstis, and C. J. Corben, 1975). Females lay their eggs among leaves. When they hatch, the male places himself in the middle of the mass and either coats himself with jelly from the spawn or, perhaps, secretes a slippery substance himself. The emerging tadpoles then perform a unique act of acrobatics among amphibians: they move in an ungainly fashion by bending their bodies, head toward tail, and then springing sideways and forward. In this inefficient manner, they migrate over the slippery body of their father and enter the brood pouch under their own steam. (I am almost tempted to say, given the Australian venue, that these creatures have been emboldened to perform in such unfroglike ways by watching too many surrounding marsupials, for the kangaroo’s undeveloped, almost larval joey also must endure a slow and tortuous crawl to the parental pouch!)

  In a kind of intermediate mode, some frogs brood their young internally but use structures already available for other purposes. I have already discussed Rhinoderma, the vocal-pouch brooder of Chile. Evolution seizes its opportunities. The male vocal pouch is roomy and available; in a context of strong pressure for brooding, some lineage will eventually overcome the behavioral obstacles and grasp this ready possibility. The eggs of R. darwini develop for twenty-three days before the tadpoles hatch. For the first twenty days, tadpoles grow within eggs exposed to the external environment. But tadpoles then begin to move, and this behavior apparently triggers a response from the male parent. He then takes the advanced eggs into his vocal pouch. They hatch there three days later and remain for fifty-two days until the end of metamorphosis, when the young emerge through their father’s mouth as perfectly formed little froglets. In the related species R. rufum, muscular activity begins after eight days within the egg, and males keep the tadpoles in their vocal sacs for much shorter periods, finally expelling them, still in the tadpole stage, into water (see article by K. Busse, 1970).

  In this context, Rheobatrachus is less an oddity than a fulfillment. Stomachs provide the only other large internal pouch with an egress of sufficient size. Some lineage of frogs was bound to exploit this possibility. But stomachs present a special problem not faced by vocal sacs or novel pouches of special construction—and we now encounter the key dilemma that will bring us back to mimicry in butterflies and the evolutionary problem of incipient stages. Stomachs are already doing something else—and that something is profoundly inimical to the care and protection of fragile young. Stomachs secrete acid and digest food—and eggs and tadpoles are, as they say down under, mighty good tucker.

  In short, to turn a stomach into a brood pouch, something must turn off the secretion of hydrochloric acid and suppress the passage of eggs into the intestine. At a minimum, the brooding mother cannot eat during the weeks that she carries young in her stomach. This inhibition may arise automatically and present no special problem. Stomachs contain “stretch receptors” that tell an organism when to stop eating by imposing a feeling of satiety as the mechanical consequence of a full stomach. A batch of swallowed eggs will surely set off this reaction and suppress further eating.

  But this fact scarcely solves our problem—for why doesn’t the mother simply secrete her usual acid, digest the eggs, and relieve her feeling of satiety? What turns off the secretion of hydrochloric acid and the passage of eggs into the intestine?

  Tyler and his colleagues immediately realized, when they discovered gastric brooding in Rheobatrachus, that suppression of stomach function formed the crux of their problem. “Clearly,” they wrote, “the intact amphibian stomach is likely to be an alien envi
ronment for brooding.” They began by studying the changes induced by brooding in the architecture of the stomach. They found that the secretory mucosa (the lining that produces acid) regresses while the musculature strengthens, thus converting the stomach into a strong and chemically inert pouch. Moreover, these changes are not “preparatory”—that is, they do not occur before a female swallows her eggs. Probably, then, something in the eggs or tadpoles themselves acts to suppress their own destruction and make a congenial place of their new home. The Australian researchers then set out to find the substance that suppresses acid secretion in the stomach—and they have apparently succeeded.

  P. O’Brien and D. Shearman, in a series of ingenious experiments, concentrated water that had been in contact with developing Rheobatrachus embryos to test for a chemical substance that might suppress stomach function in the mothers. They dissected out the gastric mucosa (secreting surface) of the toad Bufo marinus (Rheobatrachus itself is too rare to sacrifice so many adult females for such an experiment) and kept it alive in vitro. They showed that this isolated mucosa can function normally to secrete stomach acids and that well-known chemical inhibitors will suppress the secretion. They then demonstrated that water in contact with Rheobatrachus tadpoles suppresses the mucosa, while water in contact with tadpoles of other species has no effect. Finally, they succeeded in isolating a chemical suppressor from the water—prostaglandin E2. (The prostaglandins are hormonelike substances, named for their first discovery as secretions of the human prostate gland—though they form throughout the body and serve many functions.)

  Thus, we may finally return to mimicry and the problem of incipient stages. I trust that some readers have been bothered by an apparent dilemma of illogic and reversed causality. The eggs of Rheobatrachus must contain the prostaglandin that suppresses secretion of gastric acid and allows the stomach to serve as an inert brood pouch. It’s nice to know that eggs contain a substance for their own protection in a hostile environment. But in a world of history—not of created perfection—how can such a system arise? The ancestors of Rheobatrachus must have been conventional frogs, laying eggs for external development. At some point, a female Rheobatrachus must have swallowed its fertilized eggs (presumably taking them for food, not with the foresight of evolutionary innovation)—and the fortuitous presence of prostaglandin suppressed digestion and permitted the eggs to develop in their mother’s stomach.

  The key word is fortuitous. One cannot seriously believe that ancestral eggs actively evolved prostaglandin because they knew that, millions of years in the future, a mother would swallow them and they would then need some inhibitor of gastric secretion. The eggs must have contained prostaglandin for another reason or for no particular reason at all (perhaps just as a metabolic by-product of development). Prostaglandin provided a lucky break with respect to the later evolution of gastric brooding—a historical precondition fortuitously available at the right moment, a sine qua non evolved for other reasons and pressed into service to initiate a new evolutionary direction.

  Darwin proposed the same explanation for the initiation of mimicry—as a general solution to the old problem of incipient stages. Mimicry works splendidly as a completed system, but what gets the process started along one potential pathway among many? Darwin argued that a mimicking butterfly must begin with a slight and fortuitous resemblance to its model. Without this leg up for initiation, the process of improvement to mimetic perfection cannot begin. But once an accidental, initial resemblance provides some slight edge, natural selection can improve the fit from imperfect beginnings.

  Thus, Darwin noted with pleasure Bates’s demonstration that mimicry always arose among butterflies more prone to vary than others that never evolve mimetic forms. This tendency to vary must be the precondition that establishes fortuitous initial resemblance to models in some cases. “It is necessary to suppose,” Darwin wrote, that ancestral mimics “accidently resembled a member of another and protected group in a sufficient degree to afford some slight protection, this having given the basis for the subsequent acquisition of the most perfect resemblance.” Ancestral mimics happened to resemble a model in some slight manner—and the evolutionary process could begin. The eggs of Rheobatrachus happened to contain a prostaglandin that inhibited gastric secretion—and their mother’s stomach became a temporary home, not an engine of destruction.

  New evolutionary directions must have such quirky beginnings based on the fortuitous presence of structures and possibilities evolved for other reasons. After all, in nature, as in human invention, one cannot prepare actively for the utterly unexpected. Gastric brooding must be an either-or, a quantum jump in evolutionary potential. As Tyler argues, what intermediary stage can one imagine? Many fishes (but no frogs) brood young in their mouths—while only males possess throat pouches, but only female Rheobatrachus broods in its stomach. Eggs can’t develop halfway down the esophagus.

  We glimpse in the story of Rheobatrachus a model for the introduction of creativity and new directions in evolution (not just a tale of growing bigger or smaller, fiercer or milder, by the everyday action of natural selection). Such new directions, as Darwin argued in resolving the problem of incipient stages, must be initiated by fortuitous prerequisites, thus imparting a quirky and unpredictable character to the history of life. These new directions may involve minimal changes at first—since the fortuitous prerequisites are already present, though not so utilized, in ancestors. A female Rheobatrachus swallowed its fertilized eggs, and a striking new behavior and mode of brooding arose at once by virtue of a chemical fortuitously present in eggs, and by the automatic action of stretch receptors in the stomach. Such minimal changes are pregnant with possibilities. Most probably lead nowhere beyond a few oddballs—as with Rheobatrachus, probably already well on its way to extinction.

  But a few quirky new directions may become seeds of major innovations and floods of diversity in life’s history. The first protoamphibian that crawled out of its pond has long been a favorite source of evolutionary cartoon humor. The captions are endless—from “see ya later as alligator” to “because the weather’s better out here.” But my favorite reads “here goes nothing.” It doesn’t happen often, but when nothing becomes something, the inherent power of evolution, normally an exquisitely conservative force, can break forth. Or, as Reginald Bunthorne proclaims in Gilbert and Sullivan’s Patience (which evolution must have above all else): “Nature for restraint too mighty far, has burst the bonds of art—and here we are.”

  Postscript

  It is my sad duty to report a change of state, between writing and republishing this essay, that has made its title eerily prophetic. Rheobatrachus silus, the stomach-brooding frog and star of this essay, has apparently become extinct. This species was discovered in 1973, living in fair abundance in a restricted region of southeast Queensland, Australia. In early 1990, the National Research Council (of the United States) convened a conference to discuss “unexplained losses of amphibian populations around the world” (as reported in Science News, March 3, 1990). Michael J. Tyler, member of the team that discovered stomach brooding in Rheobatrachus, reported that 100 specimens could easily be observed per night when the population maintained fair abundance during the mid-1970s. Naturalists have not found a single individual since 1981, and must now conclude that the species is extinct (for several years they hoped that they were merely observing a sharp and perhaps cyclical reduction in numbers). Even more sadly, this loss forms part of a disturbing and unexplained pattern in amphibian populations throughout the world. In Australia alone, 20 of 194 frog species have suffered serious local drops in population size during the past decade, and at least one other species has become extinct.

  7 | Intellectual Biography

  21 | In a Jumbled Drawer

  AS MY SON GROWS, I have monitored the changing fashions in kiddie culture for words expressing deep admiration—what I called “cool” in my day, and my father designated “swell.” The half-life seems to be about six m
onths, as “excellent” (with curious lingering emphasis on the first syllable) gave way to “bad” (extended, like a sheep bleat, long enough to turn into its opposite), to “wicked,” to “rad” (short for radical). The latest incumbent—“awesome”—possesses more staying power, and has been reigning for at least two years. My only objection, from the fuddy-duddy’s corner, lies in kiddie criteria for discernment. Ethan’s buddies require such a tiny extension beyond the ordinary to proclaim something “awesome”—just a little bit bigger, brighter, and, especially, louder will do. This or that is proclaimed awesome every second sentence—and we have a lost a wonderful English word.

  Now let me tell you about awesome—the real thing, when adults still held possession of the concept. I collected fossils all my youthful life, or at least on those rare occasions of departure from the asphalt of New York City. I had amassed, by the end of college, five cartonsful, all ordered and labeled—and I was pretty proud of both quantity and quality. Then I got my present job as curator of fossil invertebrates at Harvard’s Museum of Comparative Zoology. I came to Cambridge with my five cartons and discovered that my new stewardship extended to 15,000 drawers of fossils, including some of the world’s finest and oldest specimens, brought from Europe by Louis Agassiz more than a century ago. I put the cartons in a back corner of my office twenty years ago this month. I have never opened them. Me with my five cartons facing those 15,000 drawers—that is awe.