Nature's Nether Regions

by Menno Schilthuizen

  Although Baker went on to write the partly pornographic, partly popular science book Sperm Wars and was heavily criticized by some of his colleagues for blurring the distinction between scientific fact and science fiction, those two 1993 papers by Baker and Bellis still stand. They are, so far, the only experiments ever performed on “flowback” in humans.

  What is “flowback”? Rather than just the unavoidable consequence of the messiness of copulation, flowback—or, more crudely (but probably more accurately), “sperm dumping”—is now seen as one of many different ways in which females can actively control which male gets to fertilize her eggs, even after having been inseminated. Throughout the animal kingdom, females are seen to eject anything from droplets to gushes of semen immediately after copulating with a male, and humans are no different.

  Baker and Bellis somehow persuaded their colleagues and students at the University of Manchester to share with them—quite literally—something very personal. For several months, thirty-five heterosexual Mancunian couples (consisting of thirty-three men and thirty-three women—there was some partner swapping going on) obediently dropped into Baker’s mailbox envelopes bearing the liquid testimony of their sex lives: properly labeled and tied-up condoms with ejaculate resulting from either masturbation or protected vaginal sex, as well as condoms with collected flowbacks if sex had been unprotected (women were advised to collect these by squatting over a beaker and coughing). The couples also dutifully kept logbooks of their sexual activities and specifically of the woman’s orgasms. In the end, Baker and Bellis were the proud owners of a freezer filled with unique samples: 67 masturbation ejaculates, 84 copulation ejaculates, and 127 flowbacks. It was time to pull out their microscopes and start counting and calculating.

  For each sample, they used standard microscopic methods to determine the sperm content. They first had a look at the two types of ejaculates—those deriving from masturbation and from intercourse. Based on the sperm counts and the information written up in the logbooks, as well as other personal details, Baker and Bellis were able to work out, for each individual man, a formula that predicted quite accurately how many sperm there would be in his ejaculate based on how long ago his previous masturbation and/or previous copulation had been, how much time he and his partner had spent together since they had previously had sex, and, rather surprisingly, the weight of the woman. Then they turned to the flowback samples.

  They also counted the number of sperm in the flowbacks. Of course, there was no way they could directly determine what proportion of semen had been dumped by the woman, because the remainder had been left behind inside her vagina and uterus and had not made it to Baker and Bellis’s freezer. But they had their magic formula, and with this they could calculate quite precisely for every flowback how many sperm must originally have been in the man’s ejaculate. The results were so intriguing that when the duo presented its work at a congress in Princeton, the auditorium was packed, “while speakers in a parallel session were talking virtually to themselves,” as one commenter recalls.

  First of all, some semen was dumped by any woman after almost every copulation. And although on average about 35 percent of the inseminated sperm was flushed out again in the flowback, there was a lot of variation to this number. Sometimes the flowback contained almost zero sperm, so the woman had retained the entire ejaculate inside her reproductive system. At other times (about 12 percent of all the flowbacks) she managed to return virtually all the sperm her mate had just donated to her. In other words, in theory, sperm dumping could provide a woman with a way to make or break a man’s reproductive success. But did she? And if so, how? This is where the orgasm comes in.

  Baker and Bellis found that the proportion of sperm the woman expelled was determined by her orgasm. If she did not climax or if her climax was more than a minute before the man’s ejaculation, she retained little of his sperm. If, however, she had an orgasm during or after the man’s ejaculation, she retained a lot. In other words, women can “use” their orgasms as one way to manipulate the likelihood of a particular man fertilizing an egg of hers. (Even in humans, the word “use” should not be construed to imply that this is a conscious decision; rather, it is the evolved complexity of our physiology that makes this happen involuntarily.) We will come back to women’s orgasms later (yes, this book will provide you with multiple orgasms!), but for the moment let’s leave our own species behind and turn to sperm-dumping females in somewhat less prominent species. As we shall see, human females share the habit with many, many animal species.

  Nobody knows whether females of Silhouettella loricatula experience orgasm, but they certainly do sperm dumping. These miniature “goblin spiders” live in soil and in the leaf litter underneath carob trees, which is where Swiss arachnologist Matthias Burger found them. When he took some males and females to his lab at the Natural History Museum of Bern, he noticed how the females would release a tiny bag of sperm from their genitalia during the copulation with a male. If you recall from Chapter 1, spider males mate by first loading their pedipalps or “sex legs” with sperm, and then working these from below into a female’s genital opening. This is not, by the way, a simple hit-and-run affair. In fact, copulation can be a lengthy process during which the male makes all manner of complex prying and twisting movements (internal courtship?) with his pedipalps.

  Burger discovered that, unlike in human females, the sperm dumped by his spider ladies was not that of the current male, but of her previous mate. To find this out, Burger had to do two things. First of all, he had to flash-freeze copulating pairs by pouring some liquid nitrogen over them—about minus 200 degrees centigrade (−328°F); talk about a cold shower!—and then performing painstaking dissections of the genitalia “frozen in action.” (Awe is in order: these spiders are about 1.5 millimeters long—that’s 0.07 inch!)

  What Burger discovered was a surprisingly sophisticated sperm-processing mechanism in the female. Whenever a male’s pedipalps would gain access to her genitalia and squirt in a droplet of sperm, they would not get any farther than a vestibule, the so-called receptaculum. Beyond, closed off by a solid valve and unreachable to his pedipalps, lay the uterus, where eggs could be fertilized. Burger found that lining the receptaculum was a sheet of glands with which the female would secrete a capsule around the male’s sperm. At its tip, this capsule was extended into a narrow tube, which was clamped between plates leading to the uterus. In other words, the female goblin spider packages sperm from different males separately and can, at least in principle, “decide” (note the quotation marks) whether she will use the sperm to fertilize her eggs or will instead dump the whole bag when a better spider (one that wields his pedipalps even more elegantly, for example) comes along.

  Silhouettella loricatula and Homo sapiens are just two of the many species known to practice sperm dumping. It has been studied in other spiders (including the well-known cellar spider Pholcus phalangoides, which lives in houses all over the world and shakes its web vigorously when disturbed), lots of insects, and some mammals. Female Grevy’s zebras, for example, release a large amount of semen after mating, and the zoologist Joshua Ginsberg measured (quickly, before they would be soaked up by the dry soil of the Kenyan plains) diameter and depth of these puddles of semen. He estimated that they amounted to an average of 0.3 liter. Rebecca Dean and colleagues performed similar experiments in a Swedish chicken coop, where they videotaped more than a thousand copulations and, after analysis of the footage from two video cameras that had been trained on the females’ cloacas, determined that females dumped more sperm if they had been mounted by cockerels lower in the pecking order.

  Even such humble creatures as nematode worms can make sophisticated “choices” about keeping or dumping sperm. Caenorhabditis elegans is a microscopic soil-dwelling roundworm that has been the workhorse of embryologists since the 1960s. Given its simple millimeter-long (0.04-inch) body made up of exactly 959 cells, you wouldn’t expect the many i
ntricacies of its mating behavior that David Barker lovingly describes in a 1994 article. When a male meets a female, Barker writes, he extends his so-called bursa, a fold-like extension of skin around his genitalia, wraps it around her, and inches up and down the female until he has located her vulva. Worms being what they are, there are not many orientation points along her body, so sometimes the male searches up and down her flank until, puzzled, he decides to try the other side and there finds what he is looking for.

  Having located the vulva, he then inserts his spicules. These are essentially the nematode worm’s penises. Unlike the rest of a worm’s squishy body, spicules are tough and rigid, of complex and tortuous form (as we now have come to expect of penises). They often come in pairs, and are used to open the female’s vulva, and also, again, for something that resembles internal courtship: a repetitive thrusting motion preceding the actual two-minute-long copulation. (Given the worms’ four-day generation time, this is not as fleeting as it may sound.) These small nematodes are helpfully transparent, so Barker could observe exactly what happened to the sperm inside the worms’ bodies once copulation had started. Ten seconds after he had stuck his spicules into the female’s vulva, the male’s sperm began to collect in the tubules leading from his testis to his spicules and was then, in small bursts, pumped into the female’s vagina. Toward the end of the two minutes, the amounts of sperm transferred became smaller and smaller and eventually the male began to withdraw his spicules. At that point (and it is hard not to imagine Barker staring wide-eyed into his microscope eyepiece and uttering a muffled expletive), the female would sometimes return the whole amount of sperm just received in a manner suggestive of blatant refusal. Barker writes: “The vulva would open and the entire mass of seminal fluid would appear to be blown out of the uterus under pressure. This usually resulted in the spicules of the male also being blown out of the vulva.”

  The widespread fact that insemination, as for these male worms, sometimes quite literally backfires leads to what Eberhard has called “a sad conclusion from a male’s perspective,” namely that copulation does not necessarily lead to insemination and fertilization. Just like putting a coin in a slot machine does not automatically lead to a jackpot, inserting a penis into a vulva is just the start of a hurdles race in which the risk of sperm dumping is just the first obstacle. As Eberhard has written, “[F]emales, because fertilization takes place within their bodies, generally have the last say in reproduction and can exercise ‘cryptic female choice.’”

  As Bateman has shown us, a unit of sperm is, to a male, relatively cheap to donate and any copulation is worth the shot, just like sticking a coin in a slot machine and not winning anything is an acceptable loss to any gambler. For females, the balance is different; she has a limited number of eggs to lay, so she has to hand out those jackpots prudently—either only to the males with the best genes or by spreading them evenly among males so as to create some genetic diversity among her clutch. It is, therefore, in the female’s interest to retain control over the series of hurdles between his ejaculation and her conception and turn each of those hurdles into points of decision in her favor. That’s why sexual selection does not stop with copulation. After a female has used her entire sensory apparatus to gauge a male’s assets to decide whether she allows him to mount her, there is a whole range of sexual selection opportunities after copulation has begun, and sperm dumping is one of them. Besides sperm dumping, female animals (including humans) employ a broad range of additional filters to select from among the males whose penises their vaginas encounter. And in the next chapter, we learn a few more of these filtering tricks.

  Chapter 4

  Fifty Ways to Peeve Your Lover

  Well, perhaps not fifty ways, but at least twenty-three, says Bill Eberhard in his 1996 book Female Control: Sexual Selection by Cryptic Female Choice. This book, a successor to his Sexual Selection and Animal Genitalia of a decade earlier, served a single purpose: to point out that, counterintuitively, when a female mates with a male, this should not be taken to mean that she has yielded to his desires to sire her offspring. Copulation is not “the criterion for final acceptance in female choice,” Eberhard writes. Rather, it is just one stage somewhere in the middle of a whole concatenation of hurdles put in place by the female. These hurdles start way before copulation, where they have been the territory of traditional studies of sexual selection. But—and this, certainly back in the 1990s, was not yet fully appreciated by biologists—they also continue long after copulation has begun. Copulation does not necessarily lead to insemination, insemination may not mean fertilization, and fertilization is not the same as reproduction. Each of these steps is, in Eberhard’s opinion, controlled by the female in a set of strategies he calls “cryptic female choice”—cryptic because these decisions are taken deep inside the female’s body, out of view of her mate and human observers alike.

  Ignoring this internal extension of mate choice, says Eberhard, is a serious error on the part of biologists. Females are not “passive offspring-generating machines” but, instead, very sophisticated products of evolutionary selection that have been optimized for serving their own and their offspring’s interests. And such optimization applies to reproductive decisions taken before as well as after a male has begun to insert his penis into her. In the stage before copulation, decisions are taken by the female on the basis of a broad range of male signals (his color and size, pheromones, courtship dances and song, to name but a few) perceived with a broad range of her senses (vision, hearing, smell). But after copulation has begun, the male signals as well as the female senses and decision-making machinery involved shift to those concentrated in and on both partners’ genitals. And although genitals are just a small part of the body, this does not mean that the evaluation of the signals and the ensuing decisions are any less important or effective.

  Sperm dumping is one effective (though perhaps not particularly subtle) way by which females can choose from among the males that mate with her. In this chapter, we will explore the many other strategies that females have in their arsenal to thwart the reproductive intentions of certain suitors.

  One particularly cunning strategy is the kind of two-stage coitus that is practiced by certain rodents. Neotominae are a group of 130 species of native American mice that includes deer mice and pack rats, and we would probably still be in the dark about the sexual preferences of these small mammals if it weren’t for the tireless efforts of one researcher, Donald Dewsbury of the University of Florida. Starting in the late 1960s, Dewsbury published almost thirty articles all entitled “Copulatory Behavior in the . . .” (fill in your species of neotomine mouse). Each would give detailed observations for the mouse in question on duration, sequence, and frequency of discrete elements in rodent sex, such as “pursuit-mount,” “intromission thrust frequency,” “ejaculation latency,” “genital grooming,” and (my favorite) “lying down.” One can only imagine the dull fatigue that may have overcome a journal editor upon receiving yet another brown envelope with a mouse manuscript by Dr. Dewsbury, which is presumably why he targeted such a broad range of different journals, like Animal Behaviour, American Zoologist, and Journal of Mammalogy. Still, taken together, Dewsbury’s articles form an unrivaled sort of Kinsey Reports for rodents, and they show some noteworthy patterns—patterns that may reveal junctures during copulation at which a female mouse can exert that cryptic choice of hers.

  In most neotomines, the genitalia lock together during mating because the mace-like penis inflates and cannot be extracted, meaning sometimes the male drags the female around long after ejaculation, until finally his penis becomes flaccid. In some species, such locking is replaced by a more female-friendly style of copulation. A male California mouse (Peromyscus californicus) will mount a female several times in succession. Each time, he will grace her with a series of “deep pelvic thrusting” and then dismount, only to remount a second time and do the same, and sometimes a third, each time without eja
culating. Only on the final series of thrusts would he climax, easily recognizable “by the presence, after several deep thrusts, of a series of spasmodic muscle contractions with rapid shallow intra-vaginal thrusting, and a long period in which the male remains immobile, clutching the female.” Awww.

  Such bouts of “dry sex” preceding “wet sex” might be a particularly suitable way for females to select males. Using cues from his genitalia only—or, as Eberhard calls it, “copulatory courtship”—a female could, after the dry phase, decide to allow or disallow the crucial wet phase. And copulation in two or more stages is surprisingly common in a wide variety of animals. Tiger beetles do it, and so do certain moths, wasps, stick insects, jewel beetles, mites, rats, and some spiders. The discovery, back in the 1960s, of dry copulation in the sheet web spiders (a large family of small spiders, many of which build those small sheet- or hammock-like webs that collect early-morning dewdrops in tall grass and shrubs) was a bit of a surprise, at least to spider specialists. As you may recall from Chapters 1 and 3, the received wisdom about spider sex is that a male will build a small web, squirt some sperm into it from his genital opening, then suck up this sperm in his often bizarrely shaped pedipalps and wander off in search of a female to inseminate. This is how many species of spiders go about mating, so naturally Dutch spider specialist Peter van Helsdingen expected to find it when, in 1962, he began his undergraduate project on the mating behavior of the money spider Lepthyphantes leprosus, a European species from the sheet web spider family that dwells in caves and cellars.