Bully for Brontosaurus

by Stephen Jay Gould

  Internally, the puzzle only increased. The oviducts did not unite into a uterus, but extended separately into the cloacal tube. Moreover, as in birds, the right ovary had become rudimentary, and all egg cells formed in the left ovary. This configuration inevitably led to a most troubling hypothesis for biologists committed, as most were in these pre-Darwinian days, to the division of nature into unambiguous, static categories: no uterus, no internal space to form a placenta, a reproductive tract reptilian in form. All this suggested the unthinkable for a mammal—birth from eggs. The neighboring marsupials, with their pouches and tiny joeys, had already compromised the noble name of mammal. Would Australia also yield the ultimate embarrassment of fur from eggs?

  As anatomists studied this creature early in the nineteenth century, the mystery only deepened. The platypus looked like a perfectly good mammal in all “standard” nonreproductive traits. It sported a full coat of hair and the defining anatomical signature of mammals—one bone, the dentary, in its lower jaw and three, the hammer, anvil, and stirrup, in its middle ear. (Reptiles have several jawbones and only one ear bone. Two reptilian jawbones became the hammer and anvil of the mammalian ear.) But premammalian characters also extended beyond the reproductive system. In particular, the platypus grew an interclavicle bone in its shoulder girdle—a feature of reptiles shared by no placental mammal.

  What could this curious mélange be, beyond a divine test of faith and patience? Debate centered on modes of reproduction, for eggs had not yet been found and Caldwell’s telegram lay half a century in the future. All three possibilities boasted their vociferous and celebrated defenders—for no great biologist could avoid such a fascinating creature, and all leaders of natural history entered the fray. Meckel, the great German anatomist, and his French colleague Blainville predicted viviparity, argued that eggs would never be found, and accommodated the monotremes among ordinary mammals. E. Home, who first described the platypus in detail (1802), and the renowned English anatomist Richard Owen chose the middle pathway of ovoviviparity and argued that failure to find eggs indicated their dissolution within the female’s body. But the early French evolutionists, Lamarck and Etienne Geoffroy Saint-Hilaire, insisted that anatomy could not lie and that the platypus must be oviparous. Eggs, they argued, would eventually be found.

  Geoffroy, by the way, coined the name monotreme in an interesting publication that reveals as much about French social history as peccavi indicated for imperial Britain. This issue of the Bulletin des sciences is labeled Thermidor, an 11 de la République. With revolutionary fervor at its height, France broke all ties with the old order and started counting again from year one (1793). They also redivided the year into twelve equal months, and renamed the months to honor the seasons rather than old gods and emperors. Thus, Geoffroy christened the monotremes in a summer month (Thermidor) during the eleventh year (1803) of the Republic (see Essay 24 for more on the French revolutionary calendar).

  Just one incident in the pre-Caldwell wars will indicate the intensity of nineteenth-century debate about platypuses and the relief at Caldwell’s resolution. When the great naturalists delineated their positions and defined the battleground, mammary glands had not been found in the female platypus—an apparent argument for those, like Geoffroy, who tried to distance monotremes as far as possible from mammals. Then, in 1824, Meckel discovered mammary glands. But since platypuses never do anything by the book, these glands were peculiar enough to spur more debate rather than conciliation. The glands were enormous, extending nearly from the forelegs to the hind limbs—and they led to no common opening, for no nipples could be found. (We now know that the female excretes milk through numerous pores onto a portion of her ventral surface, where the baby platypus laps it up.) Geoffroy, committed to oviparity and unwilling to admit anything like a mammalian upbringing, counterattacked. Meckel’s glands, he argued, were not mammary organs, but homologues of the odiferous flank glands of shrews, secreting substances for attraction of mates. When Meckel then extracted a milky substance from the mammary gland, Geoffroy admitted that the secretion must be food of some sort, but not milk. The glands, he now argued, are not mammary but a special feature of monotremes, used to secrete thin strands of mucus that thicken in water to provide food for young hatched from the undiscovered eggs.

  Owen then counterattacked to support Meckel for three reasons: The glands are largest shortly after the inferred time of birth (though Geoffroy expected the same for mucus used in feeding). The female echidna, living in sand and unable to thicken mucus in water, possesses glands of the same form. Finally, Owen suspended the secretion in alcohol and obtained globules, like milk, not angular fragments, like mucus (an interesting commentary upon the rudimentary state of chemical analysis during the 1830s).

  Geoffroy held firm—both to oviparity (correctly) and to the special status of feeding glands (incorrectly, for they are indeed mammary). In 1822, Geoffroy formally established the Monotremata as a fifth class of vertebrates, ranking equally with fishes, reptiles (then including amphibians), birds, and mammals. We may view Geoffroy as stubborn, and we certainly now regard the monotremes as mammals, however peculiar—but he presents a cogent and perceptive argument well worth our attention. Don’t shoehorn monotremes into the class Mammalia to make everything neat and foreclose discussion, he pleads. Taxonomies are guides to action, not passive devices for ordering. Leave monotremes separate and in uncomfortable limbo—“which suggests the necessity of further examination [and] is far better than an assimilation to normality, founded on strained and mistaken relations, which invites indolence to believe and slumber” (letter to the Zoological Society of London, 1833).

  Geoffroy also kept the flame of oviparity alive, arguing that the cloaca and reproductive tract bore no other interpretation: “Such as the organ is, such must be its function; the sexual apparatus of an oviparous animal can produce nothing but an egg.” So Caldwell arrived in Australia in September 1883—and finally resolved the great debate, eighty years after its inception.

  Caldwell, though barely a graduate, proceeded in the grand imperial style (he soon disappeared from biological view and became a successful businessman in Scotland). He employed 150 aboriginals and collected nearly 1,400 echidnas—quite a hecatomb for monotreme biology. On the subject of social insights, this time quite uncomfortable, Caldwell described his colonial style of collecting:

  The blacks were paid half-a-crown for every female, but the price of flour, tea, and sugar, which I sold to them, rose with the supply of Echidna. The half-crowns were, therefore, always just sufficient to buy food enough to keep the lazy blacks hungry.

  It was, of course, often done—but rarely said so boldly and without apology. In any case, Caldwell eventually found the eggs of the platypus (usually laid two at a time and easily overlooked at their small size of less than an inch in length).

  Caldwell solved a specific mystery that had plagued zoology for nearly a century, but he only intensified the general problem. He had proved irrevocably that the platypus is a mélange, not available for unambiguous placement into any major group of vertebrates. Geoffroy had been right about the eggs; Meckel about the mammary glands.

  The platypus has always suffered from false expectations based on human foibles. (This essay discusses the two stages of this false hoping, and then tries to rescue the poor platypus in its own terms.) During the half-century between its discovery and Darwin’s Origin of Species, the platypus endured endless attempts to deny or mitigate its true mélange of characters associated with different groups of vertebrates. Nature needed clean categories established by divine wisdom. An animal could not both lay eggs and feed its young with milk from mammary glands. So Geoffroy insisted upon eggs and no milk; Meckel upon milk and live birth.

  Caldwell’s discovery coincided with the twenty-fifth anniversary of Darwin’s Origin. By this time, evolution had made the idea of intermediacy (and mélanges of characters) acceptable, if not positively intriguing. Yet, freed of one burden, the pl
atypus assumed another—this time imposed by evolution, the very idea that had just liberated this poor creature from uncongenial shoving into rigid categories. The platypus, in short, shouldered (with its interclavicle bone) the burden of primitiveness. It would be a mammal, to be sure—but an amoeba among the gods; a tawdry, pitiable little fellow weighted down with the reptilian mark of Cain.

  Caldwell dispatched his epitome a century ago, but the platypus has never escaped. I have spent the last week as a nearly full-time reader of platypusology. With a few welcome exceptions (mostly among Australian biologists who know the creature intimately), nearly every article identifies something central about the platypus as undeveloped or inefficient relative to placental mammals—as if the undoubted presence of premammalian characters condemns each feature of the platypus to an unfinished, blundering state.

  Before I refute the myth of primitiveness for the platypus in particular, I should discuss the general fallacy that equates early with inefficient and still underlies so much of our failure to understand evolution properly. The theme has circulated through these essays for years—ladders and bushes. But I try to provide a new twist here—the basic distinction between early branching and undeveloped, or inefficient, sturcture.

  If evolution were a ladder toward progress, with reptiles on a rung below mammals, then I suppose that eggs and an interclavicle would identify platypuses as intrinsically wanting. But the Old Testament author of Proverbs, though speaking of wisdom rather than evolution, provided the proper metaphor, etz chayim: She is a tree of life to them who take hold upon her. Evolution proceeds by branching, and not (usually) by wholesale transformation and replacement. Although a lineage of reptiles did evolve into mammals, reptiles remain with us in all their glorious abundance of snakes, lizards, turtles, and crocodiles. Reptiles are doing just fine in their own way.

  The presence of premammalian characters in platypuses does not brand them as inferior or inefficient. But these characters do convey a different and interesting message. They do signify an early branching of monotreme ancestors from the lineage leading to placental mammals. This lineage did not lose its reptilian characters all at once, but in the halting and piecemeal fashion so characteristic of evolutionary trends. A branch that split from this central lineage after the defining features of mammals had evolved (hair and an earful of previous jawbones, for example) might retain other premammalian characters (birth from eggs and an interclavicle) as a sign of early derivation, not a mark of backwardness.

  The premammalian characters of the platypuses only identify the antiquity of their lineage as a separate branch of the mammalian tree. If anything, this very antiquity might give the platypus more scope (that is, more time) to become what it really is, in opposition to the myth of primitivity: a superbly engineered creature for a particular, and unusual, mode of life. The platypus is an elegant solution for mammalian life in streams—not a primitive relic of a bygone world. Old does not mean hidebound in a Darwinian world.

  Once we shuck the false expectation of primitiveness, we can view the platypus more fruitfully as a bundle of adaptations. Within this appropriate theme of good design, we must make one further distinction between shared adaptations of all mammals and particular inventions of platypuses. The first category includes a coat of fur well adapted for protecting platypuses in the (often) cold water of their streams (the waterproof hair even traps a layer of air next to the skin, thus providing additional insulation). As further protection in cold water and on the same theme of inherited features, platypuses can regulate their body temperatures as well as most “higher” mammals, although the assumption of primitivity stalled the discovery of this capacity until 1973—before that, most biologists had argued that platypus temperatures plummeted in cold waters, requiring frequent returns to the burrow for warming up. (My information on the ecology of modern platypuses comes primarily from Tom Grant’s excellent book, The Platypus, New South Wales University Press, 1984, and from conversations with Frank Carrick in Brisbane. Grant and Carrick are Australia’s leading professional students of platypuses, and I thank them for their time and care.)

  These features, shared by passive inheritance with other mammals, certainly benefit the platypus, but they provide no argument for my theme of direct adaptation—the replacement of restraining primitivity by a view of the platypus as actively evolving in its own interest. Many other features, however, including nearly everything that makes the platypus so distinctive, fall within the second category of special invention.

  Platypuses are relatively small mammals (the largest known weighed just over five pounds and barely exceeded two feet from tip to tail). They construct burrows in the banks of creeks and rivers: long (up to sixty feet) for nesting; shorter for daily use. They spend most of their life in the water, searching for food (primarily insect larvae and other small invertebrates) by probing into bottom sediments with their bills.

  The special adaptations of platypuses have fitted them in a subtle and intricate way for aquatic life. The streamlined body moves easily through water. The large, webbed forefeet propel the animal forward by alternate kicks, while the tail and partially webbed rear feet act as rudders and steering devices (in digging a burrow, the platypus anchors with its rear feet and excavates with its forelimbs). The bill works as a feeding structure par excellence, as I shall describe in a moment. Other features undoubtedly serve in the great Darwinian game of courtship, reproduction, and rearing—but we know rather little about this vital aspect of platypus life. As an example, males bear a sharp, hollow spur on their ankles, attached by a duct to a poison gland in their thighs. These spurs, presumably used in combat with competing males, grow large during the breeding season. In captivity, males have killed others with poison from their spurs, and many platypuses, both male and female, sport distinctive punctures when captured in the wild.

  Yet even this long and impressive list of special devices has been commonly misrepresented as yet another aspect (or spin-off) of pervasive primitiveness. Burrell, in his classic volume (1927), actually argued that platypuses develop such complex adaptations because simple creatures can’t rely upon the flexibility of intelligence and must develop special structures for each required action. Burrell wrote:

  Man…has escaped the need for specialization because his evolution has been projected outside himself into an evolution of tools and weapons. Other animals in need of tools and weapons must evolve them from their own bodily parts; we therefore frequently find a specialized adaptation to environmental needs grafted on to primitive simplicity of structure.

  You can’t win in such a world. You are either primitive prima facie or specialized as a result of lurking and implicit simplicity! From such a Catch-22, platypuses can only be rescued by new concepts, not additional observations.

  As a supreme irony, and ultimate defense of adaptation versus ineptitude, the structure that built the myth of primitivity—the misnamed duckbill itself—represents the platypus’s finest special invention. The platypus bill is not a homologue of any feature in birds. It is a novel structure, uniquely evolved by monotremes (the echidna carries a different version as its long and pointed snout). The bill is not simply a hard, inert horny structure. Soft skin covers the firm substrate, and this skin houses a remarkable array of sensory organs. In fact, and strange to tell, the platypus, when under water, shuts down all its other sensory systems and relies entirely upon its bill to locate obstacles and food. Flaps of skin cover tiny eyes and nonpinnate ears when a platypus dives, while a pair of valves closes off the nostrils under water.

  E. Home, in the first monograph of platypus anatomy (1802), made an astute observation that correctly identified the bill as a complex and vital sensory organ. He dissected the cranial nerves and found almost rudimentary olfactory and optic members but a remarkably developed trigeminal, carrying information from the face to the brain. With great insight, Home compared the platypus bill to a human hand in function and subtlety. (Home never saw a live plat
ypus and worked only by inference from anatomy.) He wrote:

  The olfactory nerves are small and so are the optic nerves; but the fifth pair which supplies the muscles of the face are uncommonly large. We should be led from this circumstance to believe, that the sensibility of the different parts of the bill is very great, and therefore it answers to the purpose of a hand, and is capable of nice discrimination in its feeling.

  Then, in the same year that Caldwell discovered eggs, the English biologist E. B. Poulton found the primary sensory organs of the bill. He located numerous columns of epithelial cells, each underlain by a complex of neural transmitters. He called them “push rods,” arguing by analogy with electrical bells that a sensory stimulus (a current of water or an object in bottom sediments) would depress the column and ignite the neural spark.

  A set of elegant experiments in modern neurophysiology by R. C. Bohringer and M. J. Rowe (1977 and 1981) can only increase our appreciation for the fine-tuned adaptation of the platypus bill. They found Poulton’s rods over the bill’s entire surface, but four to six times more densely packed at the anterior border of the upper bill, where platypuses must first encounter obstacles and food items. They noted different kinds of nerve receptors under the rods, suggesting that platypuses can distinguish varying kinds of signals (perhaps static versus moving components or live versus dead food). Although individual rods may not provide sufficient information for tracing the direction of a stimulus, each rod maps to a definite location on the brain, strongly implying that the sequence of activation among an array of rods permits the platypus to identify the size and location of objects.