The Flamingo’s Smile (4 page)

African catfishes of the family Mochokidae include several species that characteristically swim upside down (see G. Sterba, in bibliography). Behavior has already changed radically, and we even have good hints about the triggers in some cases. (
Synodontis nigriventris
, for example, eats algae by grazing the undersides of leaves on water-dwelling plants.) But form has altered scarcely, if at all. A few species have reversed the usual pattern of cryptic coloration for fish swimming near the surface. The light bellies of most fish render them invisible to predators looking up through the water into sunlight above. But
S. nigriventris
, as its name (black belly) implies, is dark on its anatomical underside, and light on its structural top. Since this fish swims upside down, the light side lies below, as usual. Yet, beyond this switch in color, most upside-down mochokids look just like their upright relatives. Size, shape, and position of fins have not changed. The trigger (presumably recent) is behavioral. We shall wait to see what changes in form might still ensue.

As a final point, readers might acknowledge my argument, but dismiss the examples as trivial or peripheral. We all love flamingos, and
Cassiopea
might prick our interest (our bodies too, if we get in the way). Mochokids are amusing in aquaria. But can we view life upside down as any more than a funny little corner of natural history? All my examples are the dead-end adaptations of a few species; can turning upside down lead to anything fundamental and expansive?

As an important illustration from history (though almost surely an incorrect idea), life upside down once compelled attention as a leading speculation for the origin of vertebrates—the “worm that turned” theory, so to speak. Annelids and arthropods, the most complex of segmented invertebrates, develop ventral (bottom) nerve cords; the esophagus pierces the nerve cords and connects an even more ventral mouth to a central alimentary (gut) canal lying above the nerve cords. In vertebrates, the major nerve cord runs fore and aft in a dorsal (top) position, and the alimentary canal, including mouth and esophagus, lies entirely below.

These two designs seem quite incompatible and unrelated. But, and ironically in the context of my contrast between structural and functional views, the greatest of all structuralists, Geoffroy Saint-Hilaire himself, noted that an annelid turned on its back would look more than a bit like a vertebrate—for the ventral nerve cord would then become dorsal and lie above the alimentary canal. In solving one problem, others emerge: the mouth now opens atop the inverted worm. Geoffroy suggested, as an
ad hoc
solution straining credulity, that the old mouth and nerve-piercing esophagus simply disappeared, and that an entirely new opening (the vertebrate mouth) developed below the dorsal nerve cord, connecting directly with the gut canal, and no longer piercing the nervous system. (So many other differences plague the comparison—lack of any annelid structure resembling the notocord or gill slits of vertebrates, fundamental disparities in embryological development between the two groups, for example—that the worm theory never commanded general assent, though it remained a leading contender for nearly a century.)

Geoffroy never intended his comparison of vertebrate to inverted worm as an evolutionary speculation, but only as a structural comparison to buttress his remarkable theory that all animals shared a common architectural plan. (He also argued that the segments of an insect’s external skeleton matched our internal vertebrae—and that insects literally lived within their own vertebrae. This comparison compelled the additional and astonishing conclusion, forthrightly maintained by Geoffroy, that insect legs are vertebrate ribs.)

Geoffroy also did not advance his comparison as a functional hypothesis about adaptation—he did not argue (as Lamarck might have done) that a worm’s innovative behavior (in turning over) triggered an adaptive pressure for redesign. Quite the contrary. As a structuralist, he contended that belly and back are meaningless terms of human invention to describe a superficial orientation utterly without significance to what really matters—abstract structural laws of form and permitted pathways of change.

Today, we reject Geoffroy’s speculation along with his approach to form and function. Life upside down affirms Lamarck’s claim that substantial change in morphology usually arises as a consequence of behavioral triggers. The famous fourteenth-century motto of that upstart institution, New College, Oxford, seems to embody an essential truth about history as well as conduct: manners makyth man.

THE CONVENTIONAL PROSE
of twentieth-century science is lean and spare. But our Victorian predecessors delighted in leisurely detail, in keeping perhaps with the gingerbread on their houses and the shelves of bric-a-brac inside. Consider, for example, this extended (but most entertaining) description of sex and death in praying mantises, published by L.O. Howard in 1886:

I cite this passage not merely for its style, but primarily for its substance—since it represents the first account I know of an all-time favorite among nature’s curious facts. We have all heard that some animals can live after losing large portions of themselves, but we think of them as just scraping by in such a limited state, not as improving their skills. Our cliché about “running around like a chicken with its head cut off” underscores this reasonable assumption that reduced anatomy entails diminished competence. Yet male mantises, beheaded by a rapacious mate, not only continue their act of courtship and copulation but actually perform more persistently and successfully.

I want, as usual, to discuss the larger message behind this paramount oddity, but adequate treatment requires a long digression right back to Darwin himself. So bear with me, and we’ll eventually get back to mantises and much more of what the biological literature calls “sexual cannibalism.”

The
Descent of Man
is, without doubt, Darwin’s most misunderstood book. Many people suppose that it represents Darwin’s attempt to fit the facts of human evolution into his evolutionary perspective. But no direct facts existed when he published in 1871, for besides Neanderthal (a race of our own species, not an ancestor or any form of “missing link”) no human fossils were discovered until the 1890s. Rather, the
Descent of Man
is an extended essay on the close biological relationship of humans with great apes and the possible modes of our physical and mental evolution from this common ancestry. But Darwin abhorred speculation; he never wrote a purely theoretical treatise. Even the
Origin of Species
is a compendium of facts pointing to a powerful conclusion. He would not have written a naked account of how it might have been, no matter how much he yearned to extend his evolutionary perspective to what he once called “the citadel itself”—the human mind.

The key to the
Descent of Man
is its situation as a relatively short preface to a large, two-volume work,
The Descent of Man and Selection in Relation to Sex
. Darwin could weave wonderful and extensive tapestries about central themes—so much so that his readers often lose the core in its extensive mantling. But all his books are solutions to specific puzzles; the rest, for all its brilliance, is superstructure. The coral reef book is about historical inference from contemporary results, the orchid book about imperfect adaptation based on parts available, the worm book about large effects accumulated by successive small changes (see essay 9 in
Hen’s Teeth and Horse’s Toes
). But because he loved detail, Darwin tells you more than you want to know about how insects fertilize orchids or how worms pull objects into their burrows—and you easily lose the kernel, the paradox, the gem of a problem that started the whole edifice.

The
Descent of Man
is a preface to such a problem. By 1871, twelve years after the
Origin of Species
, Darwin no longer needed to convince people of good will and mental flexibility that evolution had occurred; that battle had been won. But how does evolution work, what kind of world do we inhabit, and how can we know? Darwin’s radical message lay in his claim that the beauties and harmony of nature are all byproducts of one primary process called natural selection: organisms struggle to achieve greater personal reproductive success—in modern parlance, to pass more of their genes into future generations (since they cannot preserve their bodies)—and that is all. No overarching laws about the good of species or ecosystems, no wise and watchful regulator in the skies—just organisms struggling.

But how can we know that the world is regulated by selection and not by some other evolutionary principle? Darwin’s answer is brilliant, paradoxical, and usually misunderstood. Do not, he cautions, rest your case on what might seem to be the most elegant expression of selection—the beautiful, optimally designed adaptations of organisms to their environments: the aerodynamic perfection of a bird’s wing or the streamlined beauty of a marlin. For good design is the expectation of most evolutionary theories (and of creationism as well, for that matter). There is nothing distinctively Darwinian about perfection. Instead, look for the oddities and imperfections that only occur if selection based on the reproductive success of individuals—and not on some other evolutionary mechanism—shapes the path of evolution.

The largest class of such oddities includes those structures and habits that plainly compromise the good design of organisms (and the ultimate success of species) but just as clearly increase the reproductive prowess of individuals bearing them. (My favorite examples are the tail feathers of peacocks and the huge, encumbering antlers of Irish elks, both adaptations in the struggle among males for access to, or acceptance by, females, but certainly not contributions to good design in the biomechanical sense.) Our world overflows with peculiar, otherwise senseless shapes and behaviors that function only to promote victory in the great game of mating and reproduction. No other world but Darwin’s would fill nature with such curiosities that weaken species and hinder good design but bring success where it really matters in Darwin’s universe alone—passing more genes to future generations.

Darwin realized that natural selection in its usual sense—increasing adaptation to changing local environments—would not explain this large class of features evolved to secure purely reproductive benefits for individuals. So he christened a parallel process, sexual selection, to explain this crucial evidence. He argued that sexual selection might work by combat among males or choice by females: the first to produce overblown weapons and instruments of display; the second to encourage those adornments and elaborate posturings that impel notice and acceptance (the nightingale does not sing for our delectation).

Humans enter the story at this point. Why did Darwin choose his long and detailed treatise on sexual selection as a home for his much shorter preface on the
Descent of Man?
The answer again lies in Darwin’s fascination with specific puzzles and the contribution made by their solution to his larger goal. The
Descent of Man
has its anchor in a particular problem of human racial variation; it is not a waffling treatise on generalities. We can, Darwin argues, understand some racial differences, skin colors for example, as conventional adaptations to local environments (dark skin evolved several times independently and always in tropical climates). But surely we cannot argue that all the small, subtle differences among peoples—minor but consistent variations in the shape and form of noses and ears or the texture of hair—have their origin in what local environments ordain. It would be a vulgar caricature of natural selection to argue, by clever invention, that each insignificant nuance of design is really an optimal configuration for local circumstances (although many overzealous votaries continue to promote this view. A prominent evolutionist once seriously proposed to me that Slavic languages are full of consonants because mouths are best kept closed in cold weather, while Hawaiian has little but vowels because the salutary air of oceanic islands should be savored and imbibed). How then, if not by ordinary natural selection, did these small and subtle, but pervasive, racial differences originate?

Darwin proposes—and I suspect he was largely right—that different standards of beauty arise for capricious reasons among the various and formerly isolated groups of humans that people the far corners of our earth. These differences—a twist of the nose here, slimmer legs there, a curl in the hair somewhere else—are then accumulated and intensified by sexual selection, since those individuals accidentally endowed with favored features are more sought and therefore more successful in reproduction.

Look at the organization of the
Descent of Man
and you will see that this argument, not the generalities, provides its focus. The book begins with an overview of some 250 pages, all leading to a final chapter on human races and a presentation of the central paradox on the last page.

Darwin now has his handle for the real meat of his book, and he spends more than twice as much space, the next 500 pages, on a detailed account of sexual selection in group after group of organisms. Finally, in three closing chapters, he returns to human racial variation and completes his solution of the paradox by ascribing our differences primarily to sexual selection.

Sexual selection has sometimes been cast as a contrast or conflict with natural selection, but such an interpretation misunderstands Darwin’s vision. Sexual selection is our most elegant confirmation of his central tenet that the struggle of individuals for reproductive success drives evolution—a notion that natural selection cannot adequately confirm because its products are also the predictions of other evolutionary theories (and also, for optimal design, of creationism itself). The proof that our world is Darwinian lies in the large set of adaptations arising
only
because they enhance reproductive success but otherwise both hinder organisms and harm species. Darwinian selection for reproductive success must be extraordinarily powerful if it can so often overwhelm other levels and modes of advantage.

We may now return to the blood meal of the mating mantis. W.H. Auden once wrote, with great understanding of our lives, that love and death are the only subjects worth the attention of literature. They are indeed the foci of Darwin’s world, a universe of struggle for survival and continuity. But should they be conjoined? At first sight, nothing seems more absurd, less in keeping with any notion of order or advantage, than the sacrifice of life for a copulation. Should a male, in Darwin’s world, not survive to mate again? Not necessarily, if he is destined for a short life and unlikely to mate again in any case, and if his “precious bodily fluids” (to cite the immortal line from
Dr. Strangelove
) will make a big difference in nourishing the eggs fertilized by his sperm within his erstwhile partner and current executioner.

After all, his body is so much Darwinian baggage. It cannot be passed to the next generation; his patrimony lies, quite literally, in the DNA of his sperm. Thus, sexual cannibalism should be a premier example of why we live in a Darwinian world—a classic curiosity, an apparent absurdity, made sensible by the proposition that evolution is fundamentally about struggle among organisms for genetic continuity. But how good is the evidence? (And now I must warn you—since this essay may be the most convoluted I have ever written—that this eminently reasonable argument for Darwinism has, in my assessment, very little going for it at present. Yet an alternative interpretation, for a different reason, affirms something even more fundamental about Darwinism and about the nature of history itself. Frankly, while I’m at the confessional, I began research for this essay on the assumption that such a lovely and reasonable argument for sexual selection would hold, and found myself quite surprised at the paucity of evidence. I also steadfastly refuse to avoid a subject because it is difficult. The world is not uncomplicated, and a restriction of general writing to the clear and uncontroversial gives a false view of how science operates and how our world works.)

A recent issue of the
American Naturalist
, one of America’s three leading journals of evolutionary biology, featured an article by R.E. Buskirk, C. Frohlich, and K.G. Ross, “The Natural Selection of Sexual Cannibalism” (see bibliography). They develop a mathematical model to show that willing sacrifice of life to an impregnated partner will be to a male’s Darwinian advantage if he can expect little subsequent success in mating and if the food value of his body will make a substantial difference to the successful development and rearing of his offspring. The model makes good sense, but nature will match it only if we can show that such males actively promote their own consumption. If they are trying like hell to escape after mating, and occasionally get caught and eaten by a rapacious female, then we cannot argue that sexual selection has directly promoted this strategy of ultimate sacrifice for genetic continuity.

Buskirk, Frohlich, and Ross are frank in stating that sexual cannibalism is not only rare in general but also much less common than other styles of consuming close relatives (as in sibling by sibling, or mothers by offspring; see essay 10 in
Ever Since Darwin
and essay 6 in
The Panda’s Thumb
). Documented examples exist only for arthropods (insects and their kin), and only thirty species or so have been implicated (though the phenomenon may be quite common in spiders). They cite three examples as best cases.