Nature's Nether Regions

by Menno Schilthuizen

  Van Helsdingen obtained the spiders from the artificial caves left after centuries of marl excavation in Mount St. Peter near Maastricht (at 170 meters, this hill is hardly a “mount,” but in a flat country like the Netherlands one has to lower one’s elevational standards). Having collected several dozens of immature males and females from between pieces of agricultural equipment parked in the caves by local farmers, he then took them to the cold, damp, dark basement of the zoology lab in Leiden. There, under quasi-cavernous conditions, he hoped to induce the virgin spiders, after their final molt into adulthood, to mate while he watched them through his microscope under the illumination of a tiny lightbulb.

  To his surprise, Van Helsdingen discovered that mating couples of this spider blatantly ignored the arachnological handbooks. Shivering over his microscope in that dank cellar, he saw that a male spider, once copulation was imminent, would not fill his pedipalps with sperm, but instead would embark on a lengthy period of repeatedly and swiftly locking his still empty pedipalps onto the female’s epigyne, the complicatedly shaped entrance to her uterus. In the beginning, Van Helsdingen noticed, there would be some clumsy flubs where a male’s pedipalp would slip off the female’s epigyne, but after some time the male usually would get the hang of it. Each time, a pedipalp would remain locked on the female’s epigyne for a few seconds only, followed by a few more seconds of cleaning and resting, and the male would tirelessly continue with these “dry” intromissions for hundreds or even thousands of times, a feat lasting up to six hours! By interrupting the coitus, isolating the female, and waiting for her to lay eggs—all of which proved unfertilized—Van Helsdingen confirmed that indeed no sperm was transferred during this phase.

  After the drawn-out dry phase, the male would abruptly walk off and, at the edge of the female’s web, start constructing a minuscule triangular sperm web on which he would deposit a drop of sperm, suck it up into both of his pedipalps, and eagerly return to his female to start copulating “for real,” pushing his pedipalps into her epigyne and emptying them.

  For years, Van Helsdingen would ask his colleagues at spider conferences whether they had ever observed the same, but nobody had—or rather, they’d all assumed that when any male spider started mating, he had already filled his pedipalps with semen beforehand. Only gradually, as more biologists began observing the spider deed with a critical eye, did it become clear that a protracted “dry” phase is a common feature of copulation among all sheet web spiders and a few other spider families as well. The sierra dome spider (Neriene litigiosa), for example, is a North American sheet webber that copulates in a way very similar to Van Helsdingen’s cave species. Evolutionary biologist Paul Watson of the University of New Mexico has been studying these spiders—named for the dome-shaped webs they build among branches—at his field station on the shore of Flathead Lake in Montana for more than three decades, taking investigations of dry and wet spider sex a step further.

  Dry/wet spider sex. Many sheet web spider males first copulate with empty pedipalps, then run off to fumble with a droplet of sperm and a specially fashioned sperm web before returning to the female to inseminate her.

  Watson placed mating spiders in an instrument called a respirometer, which accurately measures the amount of energy that an animal expends. As it turned out, during a bout of frantic dry copulation, a male Neriene spider would reach an energy output of about a tenth of a milliwatt. To the average lightbulb buyer, that may not sound like much, but, as Watson writes, “[T]his is about as hard as a spider can work”—literally as much work as running at full speed on all eights. This is due to the fact that locking the pedipalp onto the epigyne requires the laborious inflating of the so-called hematodocha. To do this, the male has to force blood into this large fluid-filled sac inside the pedipalp, which makes it unfurl like a party hooter. This then allows various mobile parts of the complex pedipalp to expand, slide, and penetrate into corresponding spaces provided by the female genitals. Watson found that the faster a male inflates, deflates, and reinflates his pedipalps (which ranged from once per minute to more than ten times per minute), the higher his energy output—and, possibly, the more desirable he would be as a mate.

  Watson also employed a kind of genetic fingerprinting to work out which of the two to five males that a female normally mates with during one season would father most of her spiderlings. He found that although the first male would normally be the most successful, the success of any subsequent male depended to a large extent on his “copulatory vigor,” a combination of the rate of dry intromissions, the number of flubs, and the duration of the dry mating phase. In other words, a female sierra dome spider chooses, from among the sperm she receives in a season, those that were donated by the males that stimulated her epigyne in the most energetic and memorable way. And one way in which she can exert such a choice is by deciding not to stick around for the wet phase and make herself scarce while the male is busy filling his pedipalps, thereby denying him his chances of fathering any of her eggs, despite his many hours of copulatory courtship. In many other animals where dry precedes wet, making a move in the lull between both phases is also a very effective way for a female to express her choice.

  This New and Useless Part

  When you think about it, a copulating pair of sheet web spiders is a powerful, though somewhat drawn-out, advertisement for the supremacy of cryptic female choice. If we did not know better, we might view the pair with Victorian eyes and see a male who has chosen his female and is now busy exercising his successful-suitor’s rights. But in reality, it is the male who is dancing to the tunes of the female. He is wasting many hours of his short life on vacuous copulation with empty pedipalps, even though he would much prefer (if his spider brain were capable of such sentiments) to charge his pedipalps with semen before approaching the female and simply inseminate her immediately upon their first encounter. The fact that he, and many other male animals, have been forced by sexual selection to go through a lengthy copulatory process in which ejaculation seems not to be the be-all and end-all shows the extent to which his reproductive fate is in the hands of his female. Still, one could argue that even if a female might run away before he is through, or she may dump some of his precious sperm, these risks do not justify such extravagances as extended periods of useless, dry pedipalp thrusting. Or, to put it more generally, why don’t male animals stick to a simple hit-and-run (or penetrate-and-ejaculate) strategy? That way, the time saved could compensate for those females that in the end do not use their sperm.

  The reasons for this lie in the fact that there is female plumbing to consider. It is not just that premature ejaculation lowers a male’s chances of fertilizing his female’s eggs. In many organisms, it literally ruins his chances. This is because there are few kinds of animals in which males dump their sperm directly onto a female’s eggs. In the vast majority of animals, the male’s ejaculate only reaches a staging area to what may be a labyrinthine female system of valves, locks, narrow corridors, sluices, and blind alleys. In humans, for example, the male leaves his sperm cells in a puddle on the uterus’s doorstep, after which they have to be transported up through the mucus-clogged cervix, along the walls of the womb, and through the valve-like entrance to the one fallopian tube that carries a fertilizable egg. They stand a chance at fertilizing that egg only if they make it all the way up to the ampulla, the sharp bend in the fallopian tube close to the ovary. And all along the way there are outward-directed microscopic hairs, narrow passages, and other obstacles.

  Finding one’s way through the reproductive maze inside a human female is still a breeze compared with the odyssey a sperm cell has to undertake through the piping of, say, the female hamster, in which the narrow fallopian tube opens next to a blind alley in the back of the uterus and is folded up into more than fifteen zigzag loops. In featherwing beetles and certain banana flies, the female tubing is similarly exaggerated. Or, in fact, in sheet web spiders, where the tunnels leading f
rom the epigyne to the sperm storage site are sometimes ridiculously long and convoluted, consisting of two stacks of up to ten loops. This drives home the fact that insemination is not fertilization. If you’re a male intent on reproducing, ejaculating into a female is only your first step. For your sperm to be actually guided through the maze that is your female’s inside, you are going to need her help.

  Labyrinthine plumbing. Females of many animals have their eggs hidden behind extensive systems of coiled tubes and valves. Here: (A) featherwing beetle; (B) banana fly; (C) sheet web spider; (D) exploded view of the stacks of coils in the latter.

  And a female may open her internal doors to a male’s sperm only if the stimulation he has given her during the dry stage of copulation was acceptable to her—a fact that frequently frustrates artificial insemination in livestock. As those working in the “veterinary fertility” business know, a sow’s response to a polyethylene pipette is decidedly lukewarm compared with a real male pig with real genitalia—and, crucially, she allows much less sperm to enter her uterus if it was administered by a man in a lab coat than by a proper boar. Artificial insemination efforts in pigs therefore resort to using real boars for mood enhancement and a latex pipette shaped to have an uncanny tactile resemblance to a boar’s penis (sometimes with a special vibrator attached to it)—and indeed reap the reproductive benefits of this bit of swine sensory theater.

  So an important incentive for a male to use his penis as an internal courtship device is to persuade the female to open inner doors that remain shut to lesser males. Biologists have discovered that the female reproductive system in most animals, great and small, carries one or more such valves, the operation of which is under unconscious female discretion. In mating spotted cucumber beetles, for example, the male rhythmically strokes the female with his antennae while he has his aedeagus inserted into her. All the while, though, the female keeps the muscles in her vagina taut, so that his aedeagus cannot penetrate all the way to her sperm storage site. Only when the female decides that the male has stroked fast enough will she relax her vaginal muscles for him. If not, the male will stroke endlessly and eventually dismount in disgust. In this section, however, I will focus on mammals, since the inner workings of their female genitalia are usually better known than those of other animals. Moreover, it will give me the chance to keep my promise of Chapter 3, to come back to the female orgasm, which may be crucial in the opening and closing of such reproductive valves.

  You might be forgiven for thinking that hype and controversy surrounding the female orgasm and, by association, the clitoris are limited to the crowded layout of modern glossy magazines. However, the scholarly literature on the subject is a similar minefield of heightened sensitivity, hype, and hyperbole. In the mid-sixteenth century, the heated exchange between anatomist Gabriele Falloppio, who claimed to have “discovered” the clitoris (discovered for male-dominated science, that is; women had been aware of it since the dawn of time, of course), and the great Vesalius, who retorted that this “new and useless part” was likely found only in hermaphroditic freaks, is indicative of the roller coaster that would be the next 450 years of discourse on the clitoris.

  For much of the seventeenth century, anatomists considered the clitoris as little more than a cue for them to draw their clitoridectomy tools, under the misapprehension that, as the authoritative Vesalius proclaimed, it was something that oughtn’t be there on a woman. But around 1672, Dutch physician Reinier de Graaf published a detailed account of the full extent of the clitoris (and we shall see below how large this extent really is), exclaiming, “We are extremely surprised that some anatomists make no more mention of this part than if it did not exist at all in the universe of nature.” He was also rather lucid in stating that obviously nature must have provided women with such a pleasure spot; otherwise why would they ever run the risk of pregnancy and labor?

  With De Graaf’s rediscovery, things were looking up for clitoral awareness—if it hadn’t been for the fact that De Graaf soon took his own life in a fit of depression over an anatomical dispute with his rival Swammerdam. Its main advocate gone, the clitoris sank into medical oblivion again for more than 150 years. It resurfaced only in 1844, in the brilliant book Die männlichen und weiblichen Wollust-Organe des Menschen und einiger Säugetiere (The Male and Female Lust Organs in Humans and Some Mammals) by the German anatomist Georg Ludwig Kobelt.

  Even in the late twentieth century, history repeated itself in a final (for now) cycle of discovery, oblivion, and rediscovery. When De Graaf and Kobelt described the human clitoris, their dissections revealed that the well-known, and usually minute, button-like glans and the elbowed ridge of the clitoris immediately underneath are really just the tip of the iceberg. Most of the clitoris is hidden away by pelvic fat and bone but is nothing to be sniffed at: two thin, 10-centimeter-long (4-inch) stalks branch out toward the buttocks and embrace two shorter, thick, pear-shaped “bulbs” that lie on either side of the deeper part of the vagina. The four together form a large pyramid, only the acme of which, the clitoris proper, is visible on the outside. The whole organ is richly supplied with blood vessels to make it swell, and wired with incredibly thick bundles of nerves, of which Kobelt wrote: “Here they are, even before their entrance so very thick that one scarcely imagines how such an abundance of nerve mass can still find room between the countless blood vessels of this very tiny structure.”

  Not so puny. The true size and complexity of the human clitoris have been forgotten and rediscovered several times over the centuries.

  Despite these seventeenth- and nineteenth-century nuggets of accurate knowledge, until very recently many human anatomy textbooks either ignored the clitoris altogether or just briefly mentioned the minuscule externally visible bits. So, once again, it came as a surprise for many when, in 1998, Australian anatomist Helen O’Connell redescribed the full extent of the female clitoris using modern techniques. “Tens of times larger than the average person realises,” New Scientist exclaimed.

  Like its instigator, the female orgasm has met with a similar fate over the centuries. Men (it was always men) who were in the know either dismissed it as a vestige of our animal past or, as Freud did, viewed it as an infantile stage in female sexual maturation, to be replaced by proper adult vaginal pleasure later in life. Either that or they went completely the opposite way and glorified the female orgasm as a uniquely human capacity, evolved to enforce bonding between men and women. Such views, fashionable in the 1960s, were expounded by Desmond Morris, who wrote in his famous 1967 book The Naked Ape that the “female orgasm in our species is unique amongst primates,” having evolved because of “the immense behavioural reward it brings to the act of sexual co-operation with the mated partner. Like all the other improvements in sexuality this will serve to strengthen the pair-bond and maintain the family unit.”

  The reality is different. Neither clitoris nor orgasm is uniquely human, both probably occur in most mammals, and the family unit does not enter the equation.

  The existence of a clitoris in nonhuman mammals is the least controversial. In all mammals, the young embryo—in humans, until about the ninth week of pregnancy—has between its paddle-like hind limbs a small lump, the so-called genital tubercle. As the embryo matures, this tubercle then either extends at the top and grows into a penis in male babies or develops more at the bottom to form a clitoris in the females. Placental mammals like us, which develop in a comfortable, nourishing womb, are born with fully formed genitals. But marsupials, which are born much earlier in development and then hang around in the mother’s pouch for a long time, come into the world at such an early state that the male and female genitals are still identical. To, say, a wallaby family, the answer to the question “Is it a boy or a girl?” only gradually becomes apparent with regular pouch checking and cannot be certain until about four months of pouch life.

  But in marsupials and placental mammals alike, all females see their genita
l tubercles eventually mature into a full-blown clitoris, which can come in as many shapes and sizes as male mammals’ penises. Ewes have a discreet and well-hidden one, while the clitorises of bonobos, certain marmosets, and other South American monkeys, rodents, and many carnivores are large affairs, with the external part bulging out like a small penis, often rigidified with an internal clitoris bone and sometimes supplied with bristles on the outside. As clitorises go, those of the mole and the spotted hyena really take the cake, being almost exactly the size and shape of a male penis, complete with a urethra passing through it and erection capabilities. The female spotted hyena in particular has taken life with a 17-centimeter-long (7-inch) clitoris to extremes, giving birth through it—the birth canal passes through it and the female often perishes in the process—and rolling it up like a sleeve whenever she copulates with a male.

  Since in humans the clitoris is the seat of the female orgasm—so-called vaginal orgasms are thought to work via internal stimulation of the clitoris as well—it is likely that all female mammals experience orgasms. (In the next section, I will get around to explaining why this is important in the context of cryptic female choice—bear with me while I titillate you a little longer.) I say “likely” because it is hard to know for sure, of course. As behavioral biologist Tim Birkhead has lamented, “[H]ow do you tell if anything else is having an orgasm?” In their famous pioneering 1966 sexology book Human Sexual Response, William Masters and Virginia Johnson spent an entire chapter describing and dissecting the carnival of signs that betray “la petite morte” in a woman. They list an “increment of myotonic tension” in the long muscles of the entire body, “involuntary carpopedal spasm” (that is, clawing of hands and feet), rhythmic contractions of the anus, vagina, and uterus, as well as hypertension and hyperventilation. Since then, with improved technology, other features have been added to this list, such as a rush of the “cuddle hormone” oxytocin in the blood and a sudden change in activity of one particular part of the brain, the orbitofrontal cortex, as has shown up on MRI scans.