Nature's Nether Regions

by Menno Schilthuizen

  Males find their mates by a simple sit-and-wait strategy. Whenever anything resembling an engorged female lumbers past, a male bedbug will climb her right flank, push ahead until his head falls over her left shoulder, and then forcefully drive his syringe-like penis into her. (Ironically, the “penis” is actually a modified paramere, the brush-like organ that in other insects is used for gentle tapping and stroking.) Although the female has a perfectly fine vagina located at her rear end, this is of no interest to the male, as the vagina’s only reproductive function is to lay eggs, not to receive any sperm. Instead, the male injects his sperm directly into the female’s body by poking his penis through her skin on the right-hand side of the fifth segment of her abdomen. The sperm cells then squeeze their way through her body, even wiggling through individual cells, eventually finding the ovaries, where they fertilize ripe egg cells. There are even some unsubstantiated reports, involving other bedbug species, that males sometimes inseminate other males, where the sperm then reach the testes and proceed to be transferred, together with this male’s own sperm, to the next female he traumatically inseminates! If true, this would be bisexuality and cuckoldry rolled into one.

  In a way, such traumatic insemination is the ultimate insult to female cryptic choice. The male forgoes courtship, genital rubbing, and any negotiations of vagina, spermatheca, and other hurdles put in place by the female. Breaking all the rules of the genital game that we have come across in this book so far, he gets his way by crude copulatory treachery. And the females suffer the consequences. When a single female is housed with as many as twelve males, she is often dead within a day from the many wounds inflicted by her suitors’ penises. And even a single male can shorten a female’s life span considerably. Alastair Stutt, a student of Siva-Jothy’s, did experiments in which he let females mate either with regular males or with males in which he had rendered the penis harmless by sticking it to its belly with a droplet of superglue. He found that the females housed with these incapacitated males lived for more than four months, whereas the females that had to suffer functional males survived for only eleven weeks or so.

  But all is not as it seems. Female bedbugs have evolved a complex system to cope with the worst effects of traumatic insemination. First of all, they carry a so-called spermalege. This amounts to a brand-new set of genitalia, developed in the site where the male normally impales her. In Cimex lectularius, this includes a slit-like organ, effectively a second vagina, on the right-hand side of her belly, and when the male adopts the copulatory position and launches his stylet-like penis into her flesh, his penis is usually guided into it. Underneath this pseudo-vagina lies a large organ, the mesospermalege, which has two functions. It receives the male’s ejaculate, guides the sperm cells into the blood, and sends them on their way toward her single ovary. It also has a sanitary role: the grimy conditions under which bedbugs live mean that a male’s pointed member is covered in harmful bacteria and fungi that it inoculates the female with as he inserts his penis into her. To deal with this, the mesospermalege houses a massive immune system that neutralizes most of these sexually transmitted diseases. Entomologists have done experiments by stabbing female bedbugs all over their bodies with infected replica bedbug penises. (Siva-Jothy: “There’s actually a guy in my lab whose pleasure it is to produce glass penises.”) They have discovered that when the females are jabbed into their spermalege, their lifetime egg output is not affected, but when they are stung in other parts of their body, they get so diseased that their offspring production is much less.

  In a different kind of bedbug, Stricticimex (“batbug” would be a better term for them, since they feed on the blood of bats in caves), the mesospermalege has evolved into such a complex system that traumatic insemination effectively has become regular insemination again: rather than traveling like unguided missiles through the female body, the sperm, after having been squirted into the tissue underneath the pseudo-vagina, are directed via a set of tubes and storage chambers to the ovaries, and the female in fact regains full control of her sex life again. So, just like the long and coiled penises and vaginas of ducks, the evolution of traumatic insemination in bedbugs also seems to be the product of a series of male adaptations to bypass cryptic female choice along with female countermeasures to gain the upper hand again.

  Although traumatic insemination sounds extremely bizarre and eccentric, the fact that it has appeared in so many unrelated kinds of animals means that it is not that unimaginable a route for evolution to take. This probably has to do with the fact that sperm are already designed to wander foreign territory and search and penetrate (egg) cells. It is a rather small step from doing that within the legitimate confines of the female reproductive tract to doing it cross-country, as it were. In fact, free-swimming sperm are also found in the female bodies of animals that do not normally perform traumatic insemination, having apparently escaped from vagina or spermatheca. In certain mites, some sperm escape from the female genitals and are encountered traveling aimlessly in the female mite’s blood. And already in the 1950s veterinary researchers discovered the very effective way of artificially inseminating female guinea pigs and chickens by simply putting sperm in a hypodermic needle and injecting it directly into the animal’s belly!

  The evolutionary distance from fellow vertebrates to ourselves is small. Indeed, human sperm are also sometimes caught escaping from the reproductive system and wandering the body cavity of human females. To estimate how often this happens, a group of three American gynecologists made clever use of a rare congenital condition known as “noncommunicating uterine horns.” In the embryo, the uterus develops from two tubes, known as “Müllerian ducts.” In boy embryos these gradually degenerate, while in girl embryos they grow and fuse into a single uterus with two fallopian tubes. In about one in four thousand women, however, the Müllerian ducts fail to fuse properly, leading to a uterus that is split down the middle into two chambers—or “horns”—only one of which connects to the cervix and the vagina.

  Gerard Nahum of Duke University Medical Center and two of his colleagues surveyed the medical literature for pregnancies in women with such noncommunicating uterine horns. They found that a fetus was just as likely to be found in the chamber of the uterus that had a connection with the vagina as in the one that had no such connection. The inescapable conclusion was that all these (obstetrically problematic) pregnancies in the “blind” uterus chamber must have been caused by sperm cells migrating through the other chamber, up the fallopian tube, then into the woman’s abdominal cavity, entering the other fallopian tube from the back entrance. There, one of them fertilized a ripe egg cell, which then embedded itself in the blind uterus chamber.

  The staggering implication of this study is that in all women—including those without this congenital condition—sperm might be traveling outside of the accepted reproductive avenues all the time, taking the shortcut via a woman’s belly if there are eggs to be fertilized in the other fallopian tube over yonder. When you think of it that way, the traumatic insemination in bedbugs with their intrepid innards-traversing sperm cells is perhaps not that foreign after all.

  Traumatic insemination evolved because it helps ejaculates to elbow their way in front of other males’ sperm depositions. Just like the other tricks we have witnessed in this chapter—forced copulation, sperm flushing, scooping, and scraping—it is a way in which evolution has dealt effectively with the clear and present danger of other males simultaneously vying for a fertile female’s favors. Clearly, we are well within the territory of sexually antagonistic coevolution now. But there is more. Current sperm competition is not all that a male has to worry about. Since females usually store sperm for a long time, future suitors are just as much of a headache. In the next chapter, we will meet yet another category of sexually antagonistic tricks up evolution’s sleeve—genital innovations that hamper such subsequent suitors’ success.

  Chapter 7

  Future Suitors


  Tucked away in a far corner of the northern German lowlands on the shore of the Baltic Sea, the small university town of Greifswald is a harmless vestige of Hanseatic commerce and rows of preunification apartment buildings. Its main claim to fame lies in being the birthplace of the Romantic-era painter Caspar David Friedrich. And as my old VW Beetle trundles its way along Greifswald’s access roads, snow still piled high on the sidewalks, nothing in the townscape (and certainly not the many austere Reformed Church spires), immortalized two centuries ago by Friedrich, betrays that the city is the hub of German genitalia research.

  Up in the university’s bird observatory I locate, rather paradoxically, the office of snail-genitalia researcher Martin Haase, whose name will come up in the next chapter, on hermaphrodite sex. And downtown, the two buildings of the Greifswald Zoological Institute house a group of experts on arthropod sex. My first appointment is with retired professor Gerd Alberti and his colleague Antonella di Palma, who receive me in the institute’s lecture theater. Accidentally comical, kindly, and speaking in a husky, high-pitched voice, Alberti hands me a CD that, as he casually remarks, contains his life’s work: 242 scientific papers on the reproduction of mites, spiders, and a few other kinds of invertebrates. He sits me down on one of the theater’s benches and then unleashes a one-hour travelogue through the amazing world of mite and spider sex, starting each new episode with the exclamation “And this is really very funny and exciting!”

  One of those funny and exciting points: spiders and mites are rather unusual in that the females often have separate body orifices for sperm input and egg output. Whereas most animals have to use a single multipurpose orifice for both procreational activities, many mites (especially the ones Alberti and Di Palma have been studying) receive sperm through small openings at the “hips” of their legs and yet lay their eggs through a different opening at their rear end. And most spiders practice the same division of labor: the males empty their pedipalps into a female spider’s two insemination ducts, which flank a third, egg-laying opening in the middle of her abdomen. The significance of this dawns on me only as I cross town toward the institute’s other branch, where institute director Gabriele Uhl has her office.

  For many years, Uhl, a charming and cheerful arachnologist, has been studying so-called mating plugs in spiders. Much to the annoyance of spider taxonomists, who need a clear view of the female genitalia for proper identification of the species, spider females’ private parts are often clogged with “dirt” or unidentifiable bits and pieces. On closer inspection, this debris often turns out to consist of male body parts—more precisely, tips of their pedipalps. In a very large proportion of spiders, Uhl says, after copulation a male breaks off a part of his own genitals and leaves it behind in his mate’s. Not as an unsavory souvenir or as the result of an accident during his hasty getaway, but rather in an attempt to secure his paternity.

  Spider researchers suspect that these bits of pedipalp obstruct the female’s genitalia against penetration attempts by subsequent suitors. And, says Uhl, the fact that spider females usually have separate insemination and egg-laying openings is one reason why spiders are “preadapted” for the usage of such arachnid chastity belts; after all, unlike in many other animals, the plug will not be in the way once the female starts giving birth to spiderlings. Sure enough, plugging happens everywhere in the animal world, but it proves particularly popular among spiders.

  But Uhl raises her index finger and allows her eyes to twinkle. “Ah, when we say ‘plug,’ this does not mean that they are plugs,” she warns. In the black widow spider, for instance, a pedipalp tip in the female genitals does not fully prevent later males from mating with that female as well, since up to five pedipalp tips can be found lodged in a female’s genitalia. This means that the first mate’s “plug” does not dissuade numerous subsequent males from mating with the female and leaving pedipalp tips of their own. A male with broken pedipalps is effectively neutered—they never grow back—so why would males perform such acts of self-mutilation if they do not completely prevent copulation by other males? To find out the answer to this question, Uhl and her student Stefan Nessler and colleague Jutta Schneider have been studying mating plug effectiveness in the wasp spider.

  The wasp spider, or Argiope bruennichi, is a striking orb-web-building spider, easily recognized by its main design feature of black and yellow cross stripes on its body as well as its habit of hanging in its webs with its eight legs held two by two in an X shape. In recent years, probably thanks to climate change, the large spider has been staging an invasion of the UK, the Netherlands, Denmark, and northern Germany from its original stronghold in Central Europe, bringing the spectacular species more urgently to the attention of researchers like Uhl.

  She gets up and walks across her office to look for the research project papers. Scanning the shelves, flipping through heaps of papers, and sighing melodiously (“Hhhhhmmm, it’s gone. Oh, no—here it is!”), she returns with a small pile of student reports and reprints of published papers, which she fans out in front of me. Pointing at a color photo showing a closeup view of a male wasp spider’s pincer-like pedipalps, she explains that they used CT scanning to work out precisely how the male uses his pedipalps to grasp the female genitalia, then reaches deep inside her and pumps his sperm into her, and finally snaps off the tip of one of the pincers’ prongs at a predefined breaking point, leaving behind a sizable chunk of his anatomy in the female after copulation.

  To work out what benefit the male gains from crowning his copulation with an act of self-neutering, Uhl and her team first visited meadows and picked almost three hundred immature males and females from their webs. Letting each spider grow up in its own plastic cup in the lab, they generated a large number of mature virgin males and females. Then, in Plexiglas cages, they gave some their first sexual experience by releasing a male into the web of a female. The male wasp spider is much smaller than the female. He mates with her by crawling between her and her web and then, belly to belly, going through the ritualized motions of emptying either his right pedipalp into her right spermatheca or his left one into her left spermatheca, the whole process usually lasting only seconds. Under natural conditions, coitus then ends rather abruptly with the female sinking her fangs into the male, swiftly wrapping him in silk, and eating him. But in the lab, the researchers rescued the males by snatching them from the females’ claws as soon as his pedipalp tip had broken off and copulation was done.

  Chastity belts. When the large female wasp spider (A) mates (B) with the small male, a prong on his pedipalp breaks off and is left behind in her genitalia. C shows a complete pedipalp; in D the prong is broken off; and E shows two detached prongs clogging a female’s genitalia, with a side view shown in F.

  Having thus created a collection of females, some with, others without one of their insemination ducts plugged, they then turned to another batch of fresh males and proceeded to amputate one of their pedipalps to create a battalion of males with either their left or their right pedipalp missing. Now the stage was set for a clever experiment. The spiders’ mating behavior is so predictable that a male will always insert his right pedipalp in a female’s right insemination duct, and never into her left one, so the researchers could engineer sexual encounters in such a way that they could be sure that the duct a male was inserting his one remaining pedipalp into was either plugged by a previous male or still vacant. Then they measured how long the male kept his pedipalp inside the female. And since sperm is injected into the female with an ongoing pumping action, the longer the pedipalp remained inside, the more sperm was transferred.

  Sure enough, the results showed that plugging the female’s genitalia, though not completely preventing a second male from mating with her, did make it harder for subsequent males to do their thing. A male forced to put his pedipalp into an already plugged insemination duct left it in there only half as long as a male ejaculating into a vacant hole. This means that to a wasp spider
, there is a benefit to leaving part of his pedipalp behind: it does not stop later males from also inserting their pedipalps, but it does hamper them in ejaculating with full force. A male that successfully plugs a female’s genitalia therefore has a higher chance of getting his just deserts than a male that doesn’t plug. And because many males do not survive their defloration anyway, they gain much but lose little by such self-emasculation.

  So, the generally poor prognosis for any male spider’s sex-life expectancy conspires with strong competition among males to produce another reason why spiders are preadapted for evolving mating plugs. Faced with such a high chance that your first time is also going to be your last, converting your genitals into a paternity-securing device is a small sacrifice given the benefits gained from protecting yourself from posthumous sperm competition.

  Chapter 5’s Tidarren spiders, which twist off one of their own massive pedipalps the better to move about, are another example of a spider that has opted for plugging and self-sacrifice. Since his single remaining palp can be used only once, and since he will die a certain death in the female’s embrace, Tidarren argo uses his entire pedipalp as a mating plug. This works as follows: as soon as he has begun pumping his sperm into the female, she then grabs him and twists him round and round until he gets detached from his securely fastened pedipalp, which continues to actively pump sperm into her for several hours after having been detached. As the female snacks on his body, he rests assured in the knowledge that his pedipalp will keep his sperm in and prevent other males from adding theirs. Barbara Knoflach of the University of Innsbruck, Austria, who has been responsible for discovering many of these details about Tidarren’s bizarre sex life, ran experiments to test the effectiveness of such a plug made from a whole pedipalp. She introduced fresh males to females that had a previous male’s pedipalp still stuck to their epigyne and discovered that these females tended to be barred from copulating again as long as the plug was in place.