Nature's Nether Regions Read online

  Peschke and Gack have been studying two European species of Aleochara: A. curtula and A. tristis. Both are parasitoids of flies—their larvae seek out the pupae of blowflies in dung (A. tristis) or animal carcasses (A. curtula). (If you’re going to be gory, then why not go all out?) They nibble a hole in the shell of the pupa, squeeze in, and then start sucking away at the developing fly inside. In the end, the rove beetle larva is ready to pupate into a mature beetle, leaving only the empty husk of the fly pupa behind.

  But Gack and Peschke have risen to biological fame not for unveiling the Aleochara life cycle, but for the beetles’ sex game of who draws the shortest straw. Let’s start with Aleochara curtula, the species that frequents cadavers. Like all Aleochara, they mate in a rather unusual “head over heels” fashion. The male crouches behind the female and then, like a contortionist, flips his long abdomen over his head to couple with the female in front of him. Once securely fastened inside her vagina (and forced to pace along with her in a rather awkward manner if she decides to move about while mating), he unfolds from his penis the internal sac that, as in Jeannel’s cave beetles of Chapter 2, inflates only upon “erection.” Although the internal sac extends the effective length of the penis, this is still nowhere near long enough to reach into the female’s spermatheca, which lies behind a sort of valve, at the end of a long, narrow tube. But the male has another trick or two to play. The first of these is his so-called flagellum, a long, thin rod affixed to the internal sac that, when the sac inflates, gets pushed into the female’s narrow spermathecal tube. All along the length of this rod runs a furrow, creating an open space that blazes a trail for the next trick to appear from the male’s penile sleeve: a self-inflatable spermatophore.

  You remember spermatophores, right? They entered this book in a painful way by ejecting themselves into diners’ gums in Chapter 1 after the consumption of freshly deceased male squid. Like squid spermatophores, the ones produced by Aleochara also seem to have a life of their own. As the male begins to withdraw his genitalia, a tube starts to grow from the far end of the pear-shaped spermatophore he has left inside the vagina. Fueled by osmotic pressure only, this tube quickly fills the space left by the flagellum, traveling up the tunnel leading to the spermatheca, and forces through the valve at the end. To complicate things, inside this traveling spermatophore tube, an “inner tube” filled with sperm begins to grow, quickly catching up with the leading tip of the first tube and eventually ballooning to fill the entire space of the spermatheca, meanwhile—and this is the crucial part—forcing out, via the valve, any sperm of previous males lingering inside. Finally, a sharp tooth inside the female’s spermatheca tears through the spermatophore and the semen is released for further use.

  “Why easy if you can also do it complicatedly?” asks Gack. This complex system of getting your sperm inside a female seems to have evolved via several evolutionary steps. The female, by hiding it behind a long tunnel and a valve, has “tried” to keep the male from putting his sperm directly into her long-term storage site. Meanwhile, the male has evolved a succession of penis extensions: the probe-like flagellum on his internal sac and an autonomous sperm package that finds its own way up the female’s labyrinth and manages to push out previous males’ sperm. Still, it’s important to note that, in the end, whether a male’s sperm is going to be released in the spermatheca is still under female control, because it is she that has to flex her inner muscles to make that large tooth inside her spermatheca rupture the bag of semen. So, again, the race is more like a game with rules set by the female.

  Bizarre as all this may seem, the strangeness of Aleochara does not end there. I did not yet mention the length of the flagellum on the internal sac of Aleochara curtula: it is about 1.5 millimeters (0.07 inch). For a beetle of slightly under 10 millimeters (0.4 inch) in body length, that’s sizable but not extraordinary. In Aleochara tristis (the one found in dung), however, the evolutionary contest between the length of the flagellum and the duct to the spermatheca seems to have run a bit out of control. This beetle is about 6 millimeters (0.25 inch) long, but its flagellum is a whopping 16 millimeters (0.6 inch) and is held rolled up like a spring inside the male’s penis when not in use. And so is the equally long duct of the spermatheca inside the female.

  Carrying on with such a formidable legacy of millennia of sexual selection is not easy for these beetles, as Gack and Peschke found out when they observed the beetles mate. Hard as it may be for the male to thread all sixteen millimeters of his flagellum up the female’s narrow duct, even harder is it afterward to stow it back in a neat, ready-for-use coil inside the penis. If, after the deed, the male would simply pull his flagellum out of the female, its springiness would immediately make it tangle up hopelessly, effectively emasculating him for good. So how do they do that? Gack and Peschke wondered. And as the beetles performed their dismounting ritual under their microscopes, the researchers’ amazement mounted concomitantly.

  As it turns out, the males literally sling their long flagellum over their shoulder. A male first pulls his flagellum a little bit out of the female’s vagina. Then, his abdomen stuck into the air, he tilts his chest a little bit sideways, creating a notch between thorax and wing covers, and clamps the flagellum loosely in there. Thus secured, he gently continues to pull the flagellum out of the female by straightening his abdomen, all the while holding the flagellum taut to prevent any knots or tangles, and slowly begins feeding it back into the space inside his penis. As the flagellum is halfway in, he turns around, pulls the last bit of it out of the female, and, still keeping it tight for as long as possible, continues to push it back into the penis like one of those spring-loaded measuring tapes.

  Aleochara tristis is not alone in the long-flagellum business. Taxonomists have found similarly lengthy flagella in the male genitals of many other beetle and bug species, which probably function in a similar way—most just haven’t been studied in detail yet. It remains to be seen whether all are the result of sexually antagonistic coevolution. The genitals of other, more familiar animals, however, have such male-female contests written all over; in the next section, we shall learn why the duck family comprises the bird species with the world’s longest penises and deepest vaginas. Brace yourself for some unsavory sex.

  A tape measure up your back end. The male rove beetle Aleochara tristis carries a so-called flagellum in his penis, which he keeps tightly rolled up when not in use (bottom right). When it’s in use, he threads it up the female’s vagina during mating (A), and afterward has to pull it out of her (B), halfway clamping it under his shoulder (C–E), and then reel it in again (F).

  Not for the Fainthearted

  This story begins with two famous dead drakes. One is an Argentine lake duck (Oxyura vittata), shot in Argentina’s Córdoba province and stored in the collection of the University of Alaska’s museum. We’ll get back to that one in a short while. The other is specimen NMR 9989-00232 of the Rotterdam Natural History Museum, a male mallard (Anas platyrhynchos) that ended its life with a bang—in more than one sense—on June 5, 1995.

  On that day, at five minutes to six in the afternoon, museum curator Kees Moeliker looked up from his work as his ears registered the familiar thud of a bird hitting the museum’s glass facade. Despite the bird silhouettes painted on the new building’s exterior, birds kept flying themselves to death at regular intervals, and Moeliker had resigned himself to bagging the deceased pigeons, blackbirds, and waterfowl for the museum collection. But as he descended the stairs to see what large bird had this time bequeathed itself to the museum’s holdings, he was in for a surprise. At the foot of the glass wall lay a very dead male mallard duck, facedown on the sand. Next to it stood another, very much alive drake in a state of great sexual arousal, which, as Moeliker watched from behind the glass, proceeded to mount his dead companion and start copulating with it with great abandon.

  Rather perplexed, Moeliker sat down on a guard’s stool and, always the obse
rvant biologist, pulled out his notebook and began recording what he saw. For one and a half hours, the live male continued mounting and dismounting and repeatedly copulating with his dead conspecific. By 7:10 p.m., having covered a full page of notes, Moeliker decided he had had enough of his first observation of homosexual necrophilia, shooed off the still testosterone-heavy live male, stuffed the brutalized corpse of his dead lover in the museum freezer, and went home for dinner.

  Only six years later, after having been repeatedly nudged by his colleagues, Moeliker got around to publishing his observation in the museum’s scientific journal. In his paper “The First Case of Homosexual Necrophilia in the Mallard Anas platyrhynchos (Aves: Anatidae),” Moeliker tried to make sense of his observation. As an ornithologist with a special interest in the uglier aspects of ducks’ lives, he knew that besides monogamous pairing, male ducks also engage, often in groups, in what can only be described as gang rape. Not seldom such sexual frenzy escalates in numerous males, quacking loudly, giving chase to a single female. Such so-called “rape-intent flights” usually end when the drakes eventually corner the female in some park pond, where, much to the consternation of human duck-feeding bystanders, she then almost (or sometimes actually) drowns under their repeated “attentions.”

  Apparently, mate choice is not something that interferes very much with the sex drive of such males: for a drake who’s single and aroused, any duck will do, be it drake or dame, dead or alive. Bruce Bagemihl, in Biological Exuberance, his amazing book on the homosexual animal, writes that drakes often copulate with other males or with dead females. Apparently, it was only a matter of time before the opportunity presented itself to a drake to combine both inclinations—in this case right in front of an interested ornithologist. Somehow, Moeliker’s paper caught the attention of the committee for the Ig Nobel Prize, an annual fun-filled scientific parody event at Harvard University, where in 2003 he was awarded the Ig Nobel Prize for biology. As a commemoration, each year on the anniversary of its unglorious death, specimen NMR 9989-00232 is honored at the Rotterdam Museum with Dead Duck Day—capped off with a communal dinner party (Peking duck) in a local Chinese restaurant.

  The habit of forced copulation, which is rife among males in the duck family, and which led to the Rotterdam mallard’s death and subsequent defilement, is also responsible for the most eye-catching aspect of the second dead duck in this story. The journal Nature of September 13, 2001, ran a one-column article by duck researcher Kevin McCracken of the University of Alaska Museum of the North and his colleagues. Despite the paper’s brevity, the accompanying Figure 1 was hard to miss. It showed a dead male Argentine lake duck (Oxyura vittata) suspended from its wings against a whitewashed wall, with a drooping 42.5-centimeter-long (17-inch) coiled and spiny penis hanging from between its lifeless flippers. Now stored for good in the museum’s collection, the specimen was the first one found with its record-setting penis extruded. A year earlier, McCracken had studied seven dead Oxyura vittata and had already noticed that their penises were unusually long, but those, being tucked away inside their bodies, made it hard to get a good estimate of the actual length.

  Celebrated bird-sex researcher Tim Birkhead of the University of Sheffield recalls his thoughts when he first noticed this paper: “Breathtaking! My first thought was, What about the poor female? Where does all that go?”

  Birkhead knew that, although extreme, the length and complexity of the Argentine lake duck penis was by no means unique among ducks. While most birds copulate by simply pressing their cloacas against one another, ducks are among the few that have a real penis, which, once the cloacas are pressed together, is everted into the vagina under lymph pressure. Along it runs a groove that carries the sperm from the cloaca deep into the female’s inner sanctum. Presumably this system evolved because ducks mate in the water, where semen would wash away if they copulated with a simple cloacal kiss. In fact, at duck farms, where the birds have no option but to mate on dry land, a recurrent problem is that many a drake loses his penis because the females mistake them for a postcoital worm snack.

  Among duck species, size and shape of the penis vary a lot. The harlequin duck, for example, is very modestly endowed, with a 1.5-centimeter-long (0.7-inch) penis, whereas the pintail—considered the pinnacle of duck endowment until McCracken published his Argentine lake duck photo—is blessed with a 19-centimeter-long (8-inch) coiled and spiny one; the mallard has one that is a bit shorter but similar in design. The vaginas of female ducks, however, had always been claimed to be short tubes—simple, mundane, and nothing to write home about.

  At the time that Birkhead was still reeling from the photograph he saw in Nature, a postdoc named Patricia Brennan was working in his lab, and Birkhead suggested to her that she look at the female side of the duck story. Birkhead: “She turned out to be a master at dissecting. Halfway through her studies she called me over and she said, ‘Look what I’ve found!’” What Brennan showed him was that the vagina of a female mallard was just as complex as the male’s penis, with blind-ending side branches and twists and turns. Intrigued but skeptical, Birkhead called his friend Jean-Pierre Brillard in France, who had a lot of duck dissecting under his belt. Birkhead asked him, “Have you ever seen this?” to which Brillard replied, “Non!” and went off to check a few specimens of his own. “In five minutes he called me back and exclaimed, ‘You’re absolutely right!’”

  In 2007, Brennan, Birkhead, and their collaborators published in the journal PLOS ONE the results of their anatomical investigations of sixteen different species of ducks, which showed that the complexity of penis and vagina went hand in hand: whenever the penis was large and curly, so was the vagina. Two things revealed that this is likely to be the outcome of male-female evolutionary competition over who has the final say in fertilization. First, the species in which rape was rife were also the ones with the most complex genitalia. And second, as the team reported in 2010 in the Proceedings of the Royal Society B, the corkscrew shape of the vagina makes it harder for the penis to penetrate, because whereas the vagina is always coiled clockwise, the penis coils counterclockwise. By flexing the muscles in her vagina wall, the female would be able to block a rapist male from properly inflating his countercoiled penis into her vagina.

  The intrepid Brennan carried out a crucial experiment to back up these results. At a California Muskovy duck farm, she allowed drakes to mate with females, but at the cusp of the male’s explosive penis eversion, she would quickly replace the female’s cloaca with a glass tube. Though lined with lubricant on the inside, these tubes were otherwise designed to study how hard it was for the penis to unfold properly into the coiled vagina. And indeed, although straight or counterclockwise coiled tubes posed little problem, a glass tube resembling the female’s vagina, with its clockwise coil, proved impossible to penetrate, with the penis usually folding onto itself, getting stuck halfway, or flubbing altogether. Clearly, the more elaborate penis-vagina pairs had evolved in sexually antagonistic coevolution: a mutual series of steps in which any rapist intentions of the male had been countered by vagina blockades in the female.

  If the sexual ordeal that these female ducks endure sounds brutal, it is a minor inconvenience compared with the traumatic sexual experiences that beset the lives of certain invertebrates. And the term “traumatic” must be taken literally here, deriving from the Greek word for “wound.” Traumatic insemination is the term reserved for those animals that, somewhere along the evolutionary line, have found a way for the male to bypass the whole female system of valves and controls altogether, by injecting sperm directly through the female’s skin!

  Also termed “hypodermic insemination,” such drastic measures have evolved in leeches and earthworms, as well as in strepsipterans (tiny insects that parasitize bugs and bees), banana flies, several families of bugs, and the aptly named Harpactea sadistica. This latter species, a small spider that doesn’t make a web but hunts for insects on the floor of dry forest
s, was discovered only in 2008 in a nature reserve near Jerusalem. Most Harpactea species mate like all the spiders we have encountered so far in this book: the male charges its pedipalps with semen and pipes this into the genital openings of the female.

  Resisting rape. The clockwise-coiled vagina of a female mallard duck (A) blocks entry by the counterclockwise penis (B), unless the female relaxes her vaginal muscles.

  Not Harpactea sadistica. When a male of this species encounters a female, the pair adopts a mating position in which the male cradles the female, belly up, in his four long front legs, and then, with surgical precision, holding one pedipalp steady with the other, pierces the female’s abdominal skin and injects his sperm straight into her body cavity. Not content with a single jab, he then zigzags down her tummy, creating a double row of six to eight neat punctures, changing pedipalps each time as he shifts from left to right. The female, whose sperm storage organs are rudimentary, has her eggs fertilized by these sperm, which swim straight through her body to reach the eggs in her ovaries.

  Traumatic sex. A male (A, right) of the spider Harpactea sadistica does not bother with copulation. He cradles the female (A, left) in his forelegs and then injects sperm directly into her belly, piercing the skin with his needle-like pedipalps, leaving a neat pattern of eight punctures (B).

  Even more infamous is the traumatic insemination that is practiced by cimicids, blood-feeding bugs to which also Cimex lectularius, the common bedbug, belongs. Unforgettable to anyone who has ever been unlucky enough to spend several nights in bedbug-infested sleeping quarters, they will be truly memorable once you have learned about their sex lives. Living in densely packed colonies in crevices near the sleeping place of their “host,” sexual encounters are frequent, quick, and literally stabs in the dark. Bedbug researcher Mike Siva-Jothy of Sheffield University says: “When a female has not fed, she can avoid copulating males. But when she’s fed and bloated, she’s a sitting duck. There’s no courtship—it’s brutal in every sense of the word.”