Nature's Nether Regions Read online

  If I went on flipping through my field guides, I would come up with dozens of other examples of how the best way to identify otherwise similar species of pheasants, toads, fireflies, chameleons, and so on is by the males’ feathered crests, croaking pitch, blinking pattern, skin coloration, etc. Apparently, these male signals (“secondary” sexual characters, as Darwin called them) used to woo females are among the things in nature that evolve the fastest and in widely different directions, yielding the greatest differences between species. Rather than adapting to the environment, these colorful feathers, harmonious voices, and all the other ways in which males attract attention to themselves are constantly adapting to female fancy.

  Now I drag another dusty book off my shelf: the third volume of Die Käfer Mitteleuropas (The Beetles of Central Europe) by Heinz Freude, Karl Wilhelm Harde, and Gustav Adolf Lohse. Opening it to a random page in Chapter 7, I come upon a series of line drawings that illustrates how to identify the thirty or so species of tiny Hydraena water beetles that live in the streams and swamps of Germany and surrounding countries. It doesn’t show the beetles themselves, which all look extremely similar. Instead, it shows a plate that looks like it was taken from a catalog of mail-order kitchen appliances: rows and rows of outlandishly shaped water beetle penises, the only way to correctly determine which species a hydraenid belongs to.

  The fact that water beetle penis diversity fits in a more general pattern of species differing in their kinds of male adornment should make us wonder whether their genitals might also, like flycatcher plumage and grasshopper song, evolve by Darwinian sexual selection.

  This chapter will be devoted to Eberhard’s theory that female preferences are indeed what drive the evolution of male genitalia. But first let us ask ourselves why Darwin, after spending so many pages discussing the elaborate feather displays of birds and the immensely varied constellations of horns, antlers, and prongs on the heads and thoraxes of male animals both vertebrate and invertebrate, didn’t take the next step and also embrace the priapic parade of animal penises.

  Perhaps he was sidetracked by the obvious functionality of the genital organs (in contrast to, say, virtuoso song and pink tufts of down). Remember, the fact that a male simply needs a penis (to serve his reproductive needs) is why Darwin categorized genitals as primary rather than secondary sexual characters and, hence, the result of natural rather than sexual selection. But this does not really make sense. A bird also needs a head, but that does not detract from the fact that any colorful attributes to its head may be selected by females—it’s the “part” versus “property” distinction of Ghiselin’s that we saw in Chapter 1. Similarly, the penis itself may be a functional necessity, but all its ornamental attributes (spines, flanges, ribs, knobs, anything beyond the modest functional needs of a syringe) may be selected sexually.

  Perhaps, too, Darwin simply wasn’t aware of the magnitude of penis diversity. In his 1985 book, Eberhard thought that this indeed was the explanation for Darwin’s silence on the subject: “So strong was Darwin’s apparent belief in the powers of sexual selection that if the complexity and variety of genitalic structures had been common knowledge among zoologists of his day, or even, perhaps, if he had studied beetles rather than barnacles, I suspect he would have included genitalia in his listing,” he wrote.

  But then Darwin did study beetles—as a student in Cambridge, he was such a passionate beetle collector that one of his classmates even drew a caricature of Darwin riding an oversized dung beetle while at the same time trying to catch it with a minuscule net. And in his autobiography Darwin spends several pages glorifying those beetle-hunting days. However, he also admits that, aside from pinning and identifying them, he did not study his beetle catches very intensively and performed no dissections, so he may indeed have missed the genital wonders that lay hidden beneath their elytra. Then again, the genital diversity of barnacles, which Darwin did study and dissect with abandon for eight years (because he felt he could not begin his evolutionary work without first having written a decent zoological treatise), had no secrets for him. He was the discoverer of the penis that still counts as the longest in the animal world: the male organ of the burrowing barnacle (Cryptophialus minutus), a whopping eight times longer than its body. (This is explained by the fact that barnacles live their lives affixed to a rock or a ship’s hull and the only way to fertilize their neighbors, in a wave-swept environment where casting sperm into the water would not work, is by extending long, prehensile penises to seek out mates. A particularly steamy day in the barnacle colony shows dozens of elongated penises snaking their way among the denizens, probing crevices wherever they can. Sometimes there are so many at the same time that it is impossible to determine who is mating with whom.)

  No, the reason that Darwin steered clear of all too explicit mentioning of sex and genitals in his books (aside from his publications intended for a specialized audience of barnacle aficionados) was probably Victorian caution. A popular image of Charles Darwin is often that of a sideburned, sunburnt Victorian explorer in breeches, clambering about the volcanic rocks of the Galápagos Islands in search of evidence for evolution. But the reality is that by the time he celebrated his greatest successes, Darwin did most of his exploring in his head and library, while his daily life was particularly humdrum. Father of seven, he doted on his children and, next to penning down earth-shattering scientific theories, his main concern was to be patriarch of a harmonious upper-middle-class family.

  Well endowed on wave-swept rocks. Darwin discovered that barnacles, which cannot approach each other to mate, have the longest penises in the animal kingdom (relative to their body size, that is). Here, the animal on the bottom left is seen penetrating the one on the top right with its snake-like penis, while another one (far right) is just beginning to probe around for a mate.

  Not surprisingly, these two ambitions sometimes clashed. While Darwin and his wife, Emma, held a long-standing but good-humored difference of opinion over evolution versus divine creation, his struggle with the subject of sex seems to be personified in his eldest daughter, Henrietta (“Etty”). Working on the manuscript for The Descent of Man, and Selection in Relation to Sex, Darwin had managed to resist the efforts of his publisher to remove the word “sex” from the title and had rescued some passages (about colorful swollen monkeys’ “bottoms,” for example) by relegating them to footnotes in abstruse Latin. But he yielded to Etty, who, while proofreading the manuscript, pulled out her red crayon whenever she felt that Dad had strayed beyond the confines of Victorian propriety.

  To be fair, although Darwin biographers often portray Etty as a prude with a negative influence on her father’s work, her recently published diary shows a much more thoughtful personality, and she was also the one who vehemently fought the rumor that Darwin had converted to Christianity on his deathbed. Still, the story that, later in life, she started a campaign to single-handedly rid the English countryside of the obscenely shaped stinkhorn mushroom (Phallus impudicus), because of the bad influence the fungus’s appearance would have on maidens, gives one pause. . . .

  Darwin and the Cost of Eggs

  So the conspicuous absence of genital diversity (except perhaps those monkeys’ bottoms) from Darwin’s sexual selection writings left the subject up for grabs. And grabbed it was, by Bill Eberhard, albeit somewhat belatedly. But before checking out Eberhard’s take on the genitals and sexual selection, let’s have a closer look at the theory of sexual selection itself. You probably recall its basic principle from Chapter 1: if a male possesses a heritable “sexy” attribute that gives him the edge over other males in the competition for copulations with females, he will sire more offspring and his heritable attribute will be overrepresented in the next generation; hence, evolution takes place. (And I gave the example of what happens when female birds prefer a fawn-feathered mutant over the regular maroon-backed ones.) Now, you would be completely justified in wondering why the reverse could not a
lso be true: if some females are more attractive to males than others—not unimaginable, right?—wouldn’t they also experience sexual selection?

  Well, yes and no. It’s complicated. So complicated that it has required sixty-five years of scientific papers crammed with mathematical formulae. But don’t worry—I’ll brief you in four math-free paragraphs. The main character in this evolutionary debate is not Darwin but an English geneticist named Angus Bateman. In 1948, Bateman wrote a paper in the journal Heredity, in which he observed: “Darwin took it as a matter of general observation that males were eager to pair with any female, whereas the female, though passive, exerted choice. He was at a loss, however, to explain this sex difference, though it is obviously of great importance.” In other words, if it is generally true in nature that males, not females, are the ones with one-track minds, then why would this be so? What causes the sexes to have such different priorities? Although Bateman’s paper has caused a lot of controversy, even years after its publication, we have to thank him for spelling out the core issue, namely: the price of eggs.

  Bateman’s rationale went like this. Imagine a breeding colony of animals—say, a covey of those partridges. Now imagine you could look inside the bodies of those birds. Inside the ovaries of all the transparent females you would see lots of eggs, and inside the testes of all the see-through male partridges you’d discern zillions of sperm. Hold on to that image. In an evolutionary sense, those clumps of sperm and eggs floating in midair are the raw material that is going to make up the colony’s next generation, and the transparent bodies of the birds that carry them are the vehicles that are going to get them there.

  As you gaze at those ghostly creatures with their valuable cargo, you will notice that the eggs are relatively big and few whereas the sperm are small and numerous (we know why this is—remember the organelle wars of Chapter 1?). Since for each new partridge only a single egg and a single sperm need to unite, there is a surplus of sperm. In fact, the sperm from a single male would probably be more than enough to fertilize all the eggs of all the females in the colony for many years to come. This means that eggs, not sperm, are the sought-after commodity and, evolutionarily speaking, the sperm should make their males do their best to ferry them to the maximum number of eggs. This basic inequality leads to an asymmetry in sexual selection: males benefit from more copulations, whereas females don’t—or, at least, not as much. So anything that makes a male more attractive to females will be sexually selected. Females, on the other hand, are always desirable to males, as long as they carry eggs that still need to be fertilized.

  This, said Bateman, leads to “undiscriminating eagerness in males and discriminating passivity in females.” And he proved his point with a series of experiments with banana flies in milk bottles. He placed males and females in the bottles, provided plenty of food, and counted the number of flies that were born to a female if she had mated once, twice, or more often, and also counted how the number of offspring a male sired depended on the number of times he got to mate. The results were unequivocal: females always produced a few dozen larvae, no matter how often they mated. For males, on the other hand, their success in fatherhood depended entirely on their sexual prowess: the more copulations, the more children. As a consequence, the numbers of babies, while more or less the same for all females, varied from a measly ten or so to several hundred among the males.

  Bateman’s principle—“sperm are cheap, eggs are expensive, so females are choosy and males are wanton”—has since then become a central tenet of sexual selection theory. But it has also been criticized. Not only have later experimentalists found flaws in Bateman’s fly experiments, but so many exceptions have been discovered of big and expensive (not small and cheap) sperm, of cheap (not expensive) eggs, of choosy (not promiscuous) males, and of wanton (not finicky) females that some scientists argue the principle is violated so often that it should be binned. I think that would be too drastic. Granted, the world is more complicated than the one created by Bateman in his milk bottles. Yet the basic tenet of Bateman’s principle (and, indeed, perhaps we’d better tone it down to “Bateman’s Rule of Thumb”) still stands: the investment per child is usually less for males than for females and it therefore normally pays for females to be choosier than males.

  So much for Bateman. Now back to Darwin, who simply took it for granted that males would be inclined to chase females rather than the other way around. Still, he recognized two different ways in which the chasing could be done: through bullying other males or through wooing females. As for bullying, he said, “The strongest and most vigorous males, or those provided with the best weapons, have prevailed. . . . Through repeated deadly contests, a slight degree of variability . . . would suffice for the work of sexual selection.” Anyone who has ever watched stags (or stag beetles) battle over a female would not contest the sense in Darwin’s words.

  Wooing has been more problematic. I happen to be writing this paragraph on a balcony in Borneo and the star fruit tree I am overlooking is the territory of a lively crimson sunbird male who spends much of his time sipping nectar from the purple flowers. However, whenever a (drab greenish gray) female visits his tree, he temporarily abandons sucking from his favorite flowers and instead starts sucking up to her: hopping from twig to twig, quivering his wings, and seemingly making sure she notices how nicely the sun bounces off his brilliant red, yellow, and metallic purple plumage. Sunbirds do not use their colorful attire to bully rivals; they are dandies that use it to dazzle the female senses. As Darwin wrote, “The females are most excited by . . . the more ornamented males, or those which are the best songsters, or play the best antics. . . . In the same manner as man can give beauty to his male poultry, so it appears that in a state of nature female birds, by having long selected the more attractive males, have added to their beauty.”

  The reason that this particular version of sexual selection did not go down too well in Darwin’s day was that, in those male-biased Victorian times, women—and, by extension, all females—were supposed to be docile and not desirous or capable of making any choices of their own, sexual or otherwise. Trying to preempt such criticism, Darwin wrote, “No doubt this implies powers of discrimination and taste on the part of the female which will at first appear extremely improbable,” and then went on to show that female animals were, in fact, quite capable of such delicate choices among ornamented males that, to the human eye, all looked more or less the same. Still, it took until the sexual revolution of the 1960s before female choice became a fashionable topic of zoological research, and biologists started to perform experiments that eventually proved Darwin’s dandy theory correct: female animals—be they primates, birds, insects, or spiders—do indeed often prefer to mate with males that look particularly pretty, are sweet voiced, or carry themselves in a “beautiful” manner.

  What remains a bit of a mystery, even today, is why females would prefer a male with, say, an extra-long red crest on its head. What good does it do her? For a while, debate about this was carried on from two entrenched camps. There were the “Fisherians,” taking their nom de guerre from the legendary English evolution theorist Ronald Fisher, who thought that females simply were, as Darwin said, “most excited” by the more elaborately adorned males and chose on the basis of arousal per se. Opposite the Fisherians stood the “Good-Geners,” who found it hard to accept that females would make such arbitrary choices as to prefer males with long red crests simply “because they look smart.” They suspected that females used these sexual ornaments to gauge males’ “genetic quality,” so that a male with a particularly striking ornament would also be particularly strong or healthy—and be able to supply the offspring with those good genes in his sperm.

  Only in the past ten years or so have biologists begun to realize that the difference of opinion between the Fisherians and the Good-Geners is only an illusion. It is immaterial what kind of benefit a female’s offspring get from her mate choice. If her sons are sex
y because her mate was sexy, they will benefit by being as successful suitors as their father. And if her offspring are extra strong and healthy because their father’s attractiveness signaled his superior disease-fighting and survival genes, they will also benefit. So although in different species different kinds of benefits are gained by mating with an attractive male, the genes that females go for are always “good.”

  Martine Maan, then working at the University of Texas, now at the University of Groningen, revealed that in the poison arrow frog Dendrobates pumilio from the Bocas del Toro archipelago in Panama, females benefit from both variants of goodness. These tiny frogs accumulate deadly toxins in their skins (they do not make these toxins themselves, but steal them from the ants they eat) to prevent themselves from being eaten by birds and other animals. To warn predators of their inedibility, they have evolved striking warning colorations: orange with black spots, red with blue legs and arms, or yellowish green with black blotches, for example—throughout the archipelago, frogs on different islands have different color patterns. Maan and her colleagues discovered that the more brightly colored frogs were also the most poisonous (which a battalion of unfortunate lab mice proved for them). “Thus, potential predators can tell from the colors of the frogs how toxic they are,” explains Maan. They then gave females a choice between two males, one of which seemed brighter than the other. (I say “seemed” because the researchers—to make sure they were really testing only the effect of brightness—used two equally bright males, but put one of them literally in the spotlight.) As it turned out, the females mostly preferred the males that appeared the brightest to them. So, in the real world, even if the females simply liked the more brilliant males in a Fisherian sense, the effect was that their offspring would inherit the good genes that gave them better protection against predators.