Nature's Nether Regions

by Menno Schilthuizen

  A couple of years after his Science article, Waage turned to spreadwing damselflies, so named because they do not properly fold their four wings when they alight, but leave them hanging in a rather disheveled fashion. The females of one spreadwing species, Lestes vigilax, have a sperm storage organ that is very spacious—it can accommodate more than one male’s ejaculate, and its large size makes it more difficult for the male to scrape out any predecessors’ sperm. Not to be outdone, males still manage to keep their sperm in the game by using their penis to pack any existing sperm into out-of-the-way corners of the female’s sperm storage organ, where it is not likely to be used for fertilizing any eggs. If the score was 0 for the girls and 1 for the boys in the first species that Waage studied, in Lestes vigilax it’s girls 1, boys 2.

  Among Calopteryx xanthostoma, a species related to the one that Waage did his pioneering work on, the deeper recesses of the female’s sperm storage organ are so narrow that the flaps on the male’s penis cannot get in. Given his penis’s bulk, he has to accept that some rival sperm will remain unreachable to his sperm-scooper and that many eggs laid by her will be fertilized not with his, but with other males’ sperm hiding deep inside her. Girls against the boys: 2-1.

  The same would be true for yet another species, Calopteryx haemorrhoidalis—which, like C. xanthostoma, also has penis horns that are not slim enough to penetrate the deeper female genitalia—were it not for the following clever trick, revealed by Mexican entomologist Alex Córdoba-Aguilar. All damselflies have two plates in the walls of the vagina. The sense organs embedded in these plates feel when an egg passes through the vagina and send a signal to the spermatheca; this elicits the release of a droplet of sperm to fertilize the egg. What has happened in Calopteryx haemorrhoidalis is that this female fertilization system has been hijacked by the male. The shape of the penis is such that, each time it pushes into the female vagina, it buckles the vaginal plates in the same way that a passing egg would. The sense organs in the vaginal plates, duped into “thinking” that an egg is being laid, send a signal to the spermatheca to release previous trysts’ sperm, which drips out of the spermatheca and is removed by the male with his penis. There is no egg—but the female physiology is tricked by the male’s egg-shaped penis, and the male wins the game after all.

  To show that the C. haemorrhoidalis penis indeed has a shape that persuades a female to empty her sperm stores, Córdoba-Aguilar has done experiments in which he tied down females of other species and, holding a detached C. haemorrhoidalis penis in the tips of a pair of tweezers, stimulated their vaginas in the same way that a copulating C. haemorrhoidalis male would. And, lo and behold, these other species also helplessly released large quantities of the sperm held in their spermathecae.

  In yet other species of damselfly the female has got the upper hand again. A female of Paraphlebia quinta from forested hill streams in Central America will often interrupt a copulation after a male has finished scraping but before he has begun depositing his own sperm—thereby losing her sperm stock, but denying the male the opportunity to replace it with his own. And even if she allows the male to ejaculate into her, after mating she often ejects a small droplet from her vagina: the familiar, if unsavory, act of sperm dumping.

  What this little odonatological foray shows all too clearly is that damselflies do not seem to fit with the picture of penile persuasion by internal courtship that I have painted in the previous chapters. Yes, the males have penises that are shaped differently in each species, and, yes, they do pump them up and down in the vagina of the female, who may or may not decide to remain in mating wheel position until the ejaculatory culmination. But against this familiar backdrop of internal courtship and cryptic female choice, the plot thickens into a genital drama of rivalry, male-female conflict, and deceit. Males use their penises to manipulate other males’ luck in love, as well as females’ sexual autonomy. And damsels in distress evolve ways to limit the success of males in getting their way with them. Experts call it “sexually antagonistic coevolution,” which is a mouthful but reveals quite accurately what goes on. It is sexually antagonistic in the sense that what evolves in males is not always good for the females, and vice versa. And it involves coevolution, meaning that both sides, though antagonizing the other, evolve hand in hand: an evolutionary step taken by females is sooner or later countered by an evolutionary response from across the sexual divide.

  Sexually antagonistic coevolution is, in fact, unavoidable. Cryptic female choice sets up a conflict of interest during each and every copulation. For the female involved, it is best to maintain control over the fate of any male’s sperm. She needs to weigh her options: if it is an extremely handsome male, then passing his attractive genes on to many of her sons would be a good strategy. If he is a lesser male, it may be good to use his sperm only for a small proportion of her offspring, if at all. In any case, not having all her eggs fertilized by a single male will usually be a good thing. By creating genetic diversity among her clutch she reduces the risk that all of them will succumb to a disease or carry some genetic defect: she’d better not put all her eggs in one genetic basket. So, in evolution, female tubing and wiring that maximize her ability to make these (unconscious) choices will be favored. But for the male, these calculating intentions of his mate are bad news. For him, it would be best if the female were to fertilize as many eggs as possible with his sperm, and evolution will allow any ways in which he can coax, coerce, or con her into doing so.

  So even if the evolution of sex in a species may start off in a pleasantly cooperative way—males show females what they have on offer, females make their choice, the unsuccessful males try their luck somewhere else, no hard feelings—it can quickly escalate to an evolutionary concatenation of tricks to get the upper hand in the sexual conflict. As Richard Dawkins and John Krebs have written, “[S]words get sharper, so shields get thicker. So swords get sharper still.” Such a conflict, remember, is inherent in Bateman’s principle: males gain more reproductive success the more sperm they manage to get accepted by females, whereas females gain reproductive success by choosing their males prudently. In other words, for males sex is more about quantity; for females it is more about quality. Hence those sperm-scoopers, unfathomable female sperm stores, and egg-mimicking penises in damselflies.

  As you will realize, our story now enters uncharted and treacherous territory. Here be monsters. In the next few chapters we will observe the dubious role genitals may play in these evolutionary arms races throughout the animal kingdom. But we should always remember that casting these evolutionary escalations in human terms can be misleading. Tempting and illustrative as it may be to speak of the “battle of the sexes,” “evolutionary arms races,” or “tug-of-war,” I will try to avoid this as much as possible. Not only because it taints the sex acts of these innocent animals with the uglier kinds of human aggression, but also because the comparison is faulty. In warring factions, the two groups that are in conflict with each other will always remain separate and every point scored by a group member will benefit his clan only. Males and females are not to be confused with such separate clans, for the simple reason that they spawn their own enemies: males also get daughters and females also get sons. So it may actually be beneficial for a female to mate with a male that manipulates or overrides her cryptic female choice, if her sons inherit the same ability and will play that trick upon their mates in the next generation. Once again, in sex, all is not as it seems. . . .

  Sperm Bank Robbers

  One cannot help but wonder how the financial office of the State University of New York reacted when it received reimbursement claims from the psychology department for latex dildos and vaginas. But then again, perhaps it was already used to the unusual research needs of biopsychologist Gordon Gallup on the Albany campus. Famous for his early work on the ability of chimpanzees to recognize themselves in a mirror, he has since focused his attentions on the evolution of human sexuality, and has not shirked f
rom producing unorthodox articles with such titles as “Does Semen Contain Antidepressant Properties?,” “The Unique Impact of Menstruation on the Female Voice,” and “On the Origin of Descended Scrotal Testicles.”

  In 2002, he and his student Rebecca Burch decided to take on a new project: figuring out whether the same sperm-scooping trick so prevalent in damselflies was also at work in our own species. Aside from the matter of how such scooping should work mechanically, this may seem a rather strange idea at first glance. After all, unlike in damselflies, human sperm cells survive for a maximum of two to four days inside a woman’s body, so how likely is it that men face true sperm competition? How often would their penises meet live, foreign sperm inside the vagina of their mate?

  Well, perhaps more often than you’d think, as Gordon and Burch found out. They interviewed almost five hundred female New York college students and learned that 12 percent say they have had, at any point in their lives, sex with more than one man in succession within a twenty-four-hour period. And one in twelve reports having engaged in group sex with multiple men at the same time. Sperm competition may be a thing to be reckoned with, after all. On the grimmer side, sex violence statistics from several countries show that about one-fourth of all rape cases involve multiple perpetrators. If similar figures would have applied in our evolutionary past, sperm-scooping ability may have evolved in humans as it has in damselflies.

  But how could it work? This is where the products of California Exotic Novelties, Inc., come in. In an article published in the journal Evolution and Human Behavior, Gallup and Burch and their team report how they used the latex genitals to test whether the rim behind the glans on the human penis might be effective at displacing previous males’ sperm from a vagina. They went about it with gusto. Testing various recipes for “artificial semen” by mixing water and cornstarch, they reached a texture and consistency that, as they write, “three sexually experienced males” deemed similar in texture to human semen. They placed an ejaculate-sized amount of the mock sperm deep inside the artificial vagina, and then inserted their dildos. The wall of the vagina was helpfully transparent, which made the fate of the cornstarch semen clearly visible. It worked! When the dildo went down, the semen in the vagina flowed via the space around the frenulum (the stringy bit of tissue bridging the glans and the shaft) and got trapped behind the rim of the glans. When the researchers pulled the dildo up again, this piston-like action lifted much of the semen up and out of the vagina. Thus, some 90 percent of the semen was scooped out with every stroke—at least when “lifelike” dildos were used. They also tried a smooth vibrator (switched off) without a glans, but this one hardly removed any semen.

  Could this mean that the shape of the human penis has partly evolved to tackle sperm competition? It’s an intriguing thought, but I am skeptical. Our closest relative, the chimpanzee, engages in much more “group sex”—where female chimps associate with groups of males and mate with several males in succession—yet the chimp penis is smooth, dagger-like, with no scoop-like glans whatsoever.

  That is not to say that sperm scooping does not occur outside the realm of damselflies and dragonflies. In fact, it is probably quite widespread. The male flour beetle (Tribolium castaneum), for example, has a furrow on his penis studded with bristles, which proves very effective at brushing out other males’ sperm from females. So effective, in fact, that it can backfire, as a Belgian-British team of researchers found out. When a male, his rival’s sperm still sticking to his penis, dismounts from one female, only to run into another, he may actually fertilize this new female not only with his own sperm but also with the sperm he has just removed from his previous mate: paternity by proxy.

  Douche bag. Male sharks, which carry two penises (or “claspers”), have a so-called siphon sac, with which they can squirt seawater into the vagina of their mate, perhaps to rinse out previous males’ sperm. The siphon sac as well as the sperm duct both exit through a groove in the claspers.

  And some animals may flush, rather than scoop. Male sharks are thought to give their mates a kind of vaginal douche before injecting their own sperm. I say “are thought to” because depressingly little is certain about sex in these iconic but little-understood fish (until the 1970s, shark mating had been observed only twice!). What is known is that sharks are blessed with two penises—actually the modified tips of their pelvic fins—each ending in a complex system of movable flaps, prongs, and levers (which is why the penises are normally called claspers, as biologists originally thought they were used to hold the female). During mating—which seems a rather violent affair, involving the male biting the female in the head or pectoral fin, wrapping his body around her, and pinning her to the seafloor—a male will push one of his two penises into her vagina and use the set of flaps to open her oviduct. Along each penis runs a groove that is connected to the testis as well as to the so-called siphon sac, a muscular bladder in the belly of the fish that can suck up a surprisingly large amount of seawater; in the dusky smooth hound, a shark from the western Atlantic, this large reservoir occupies a third of the body length. The siphon sac seems to provide the hydraulics to jettison the sperm into the female, and some shark researchers claim it is also used for swilling out the vagina. Whether this is true is still a matter of contention, but since groups of males often harass single females, each mating with her in turn, such sperm flushing would seem a sensible thing to do.

  Crickets also flush. Except that they don’t use water but their own semen. The pretty green Japanese tree cricket Truljalia hibinonis has a huge (relative to its body length) member that it can push all the way up the female’s spermatheca. When it then ejaculates, its sticky mass of sperm will force backward any sperm that is already in there, pushing it out of the female’s vagina and onto the penis shaft of the male—who then bends over and proceeds to nibble away at the freshly removed rival sperm as a postcoital snack! And in another cricket-like insect, the European katydid Metaplastes ornatus, sperm flushing is a part of sex in which male and female actually collaborate. The male inserts his genitalia, moves them in and out for a bit, and then withdraws. Since his genitalia are jagged and crenellated, pulling them out of the female brings forth a large portion of the female reproductive system, momentarily exposed inside out. What then happens is rather remarkable: the female doubles over and licks out the inside of her own genitalia, eating up any sperm packages of previous mates that still remain in there. This ritual is repeated several times before the male finally deposits his own sperm.

  This last example may seem a little puzzling: why would a female join in on a male’s attempts to empty her sperm stores? Again, we have to remember that a female has a vested interest in whatever the male does. A male that is able to persuade her to give up her stored sperm reserves probably has qualities that she’d do worse than to pass on to her sons. So, in some species, the whole sperm-scooping business has evolved to become incorporated into the mating ritual and, in a way, has become part and parcel of cryptic female choice—merging imperceptibly with sperm dumping.

  Rather than converging on cooperation, another outcome might be an evolutionary race over which sex is in charge of a female’s stored sperm. One obvious way in which such a race could be run is by the male and female alternately taking an evolutionary step to take control, like the variety of measures and countermeasures we have seen in damselflies. The female may evolve a somewhat deeper spermatheca, pulling her sperm reservoir out of reach of the male. Sooner or later, a mutation on the male side may then appear that either gives him a penis extension or some other way to regain his sperm-scooping ability. This may then be followed by yet a further deepening on the female side, and so on. Since there is no way back, such evolutionary races might eventually spiral out of control, leading to ridiculously long penises and ditto spermathecae.

  One kind of animal whose innards seem to have been seized by such unstoppable evolutionary convulsions is the rove beetle. Chances are tha
t you have managed to live your life without rove beetles ever having claimed any of your brain waves. Let me remedy that lapse, for rove beetles, with their sleek, somber bodies, sit at the high table of insect biodiversity. They come in all colors, sizes, textures, and walks of life, but your standard rove beetle is a few millimeters (about one-tenth of an inch) long, dark, and has its wings tucked neatly underneath shortened wing covers that leave much of the long abdomen uncovered—a bit like a tiny earwig, which they resemble but are not related to. They move fast, and when alarmed stick up their abdomens in threat, though there is no sting in the tail. To biologists (who prefer to call them Staphylinidae), their nastiest habit is their unidentifiability. Some fifty thousand different species are known, and counting (fast), with experts estimating that in reality at least four times as many exist, most living unobtrusive lives in the soil. In fact, it’s likely that there’s a rove beetle underfoot with every step you take in a forest or meadow.

  Though most rove beetles are predators, quietly catching and digesting even less glamorous creatures like springtails, mites, and insect larvae, some lead rather more bizarre lives. Aleochara is one of them; it belongs to that select group of insects with a so-called parasitoid lifestyle. Reminiscent of the movie Alien, the habit of a parasitoid (which means “parasite-like predator”) to grow inside the body of another animal—to eat it from the inside out while the “host” remains alive and active until the parasitoid ruptures the skin and emerges—strikes most people as gruesome rather than “fascinating,” the term preferred by Aleochara aficionados like Klaus Peschke and Claudia Gack of the University of Freiburg in Germany.