Nature's Nether Regions Read online

  It seems that semen may be full of manipulative substances: the male using the female’s reproductive system to wage a chemical warfare against her reproductive autonomy or even, in an act of evolutionary paranoia, against potential future competitors. But this view of semen as a magic cocktail may be too one-sided. After all, for these semen compounds to do their job properly, they need to pass through the wall of the female’s genitalia into her bloodstream. And although very tiny molecules may do so unassisted, larger proteins are too bulky to slip through the cracks in the female’s tissues—they need help from the female to do so. Take the grasshopper Gomphocerus rufus. When researchers injected extract from one of the male’s genital glands directly into a female’s blood, nothing happened. But when they injected it into her spermatheca, she promptly started kicking away at any male that approached her. They traced this to compounds from the semen latching on to receptors on bristles in the spermatheca wall, which then set in motion a physiological reaction leading to this irritable behavior. So this means that the female must be mediating the action of these so-called manipulative substances. The upshot is that rather than chemical warfare, many of these semen compounds are engaged in what might better be termed chemical communication. The female’s cellular apparatus needs to open molecular valves to allow the males’ proteins to activate her physiology. So, again, female discretion is key.

  But even at this molecular level, there are some males that won’t take a chemical no for an answer. Take the housefly. This all too familiar insect is so common that you’ve probably witnessed, willingly or not, two of them mating on a wall—the female absentmindedly preening her forelegs. Next time, imagine the following. Within minutes after mating commences, the male places his ejaculate in the female’s vagina, the liquid portion of which is received in small vaginal pouches. Ten minutes into the copulation, aggressive chemical compounds in the semen begin leaching holes in the vagina wall. The thin layer of cells begins to disintegrate and the semen starts leaking into the female’s blood. This goes on for at least another half hour, by which time large, gaping holes have appeared in the vagina wall, the semen has been absorbed by the female’s bloodstream, and antiaphrodisiac proteins are beginning to do their work. The male then flies off, leaving the female frigid for at least three weeks (if she can dodge rolled-up newspapers for that long).

  Corrosive compounds, mind-altering molecules, subversive substances . . . in all kinds of animals, the male’s ejaculate appears to contain not-so-innocent ingredients. What’s the impact of such chemical onslaught on a female animal’s body? Could all this male-administered medication become a health hazard for a partner? Indeed, in some animals the consequences of semen on a female’s health may be dire. Back in 1995, British evolutionary geneticists Tracey Chapman and Linda Partridge discovered that repeated exposure to male semen reduces a female banana fly’s life expectancy by 20 percent. They proved this by comparing the impact of regular male flies with that of males genetically engineered so that they could produce sperm, but none of the seminal proteins. Females that mated with the latter kind of males survived for more than forty days, whereas the ones whose bodies had to endure the male’s chemical warfare usually keeled over by week four.

  Now, toxicity of substances sloshing around in a male’s semen sounds paradoxical. Why would a male jeopardize the health of the female that is to bear his children? Researchers Alberto Civetta and Andrew Clark provided the answer. They discovered that some male banana flies are genetically predisposed to having more harmful semen than others. And those males were also the ones more successful at fathering a female’s babies. In other words, the more noxious semen was also better at persuading the female to use the sperm cells in it for fertilizing her eggs. So despite being his mate’s ultimate downfall, a male with particularly nasty ejaculate would still reap reproductive benefits. On the female side, however, there is also something going on. In seed beetles, which likewise fill their ejaculates with female-unfriendly substances, some females have more genetic immunity to the toxic effects than others.

  With male genes that make semen proteins differ in their toxicity, and female genes that cause variation in how susceptible a female will be, the stage is set for rapidly spiraling evolution, in which both sexes will continuously evolve to deal with semen in the way that best serves their own interests. And, as Bateman has taught us, those interests are not one and the same. The outcome, on a longish timescale, is a sort of evolutionary tango, with any male step (add manipulative protein X to the mix) answered by female countersteps (evolve an antidote to X). This explains why Rama Singh found that those semen proteins are in the fast lane for evolution, because there is a constant pressure to change and adapt the blueprint for these proteins—something that is true not just for flies, but for most animals.

  But what if males do not only evolve more efficient proteins to spike their semen with, but also more efficient ways of administering it? That is when spiking takes on a painfully literal meaning.

  Love Hurts

  “Well, that’s about it,” says Gabriele Uhl as she slaps shut the latest student report she had pulled off her shelf and adds it to the sprawling heap of books, reprints, and spiders-in-spirit that has grown on her desk over the course of our interview. We have meandered from wasp spiders’ mating plugs to what goes on in the mind of a copulating female cellar spider and along the way touched on the constituents of spider and other semen. And just as gaps begin to fall in our conversation, there is a knock on the door and in breezes Uhl’s husband, beetle enthusiast Michael Schmitt, who briefly pumps my hand and then drops himself into a desk chair in the corner. “He just had to give an exam,” Uhl explains to me, with a wink. “Which he only remembered minutes beforehand.”

  After reviving himself with a cup of tea, Schmitt gets up, grabs his coat, and takes me downstairs to his own room to chat about spiny beetle penises—as promised.

  Ouch! Spiny penises occur throughout the animal kingdom, including in bush babies (A) and king cobras (B) as well as beetles (C) and moths (D), with their caltrop cornuti.

  One of the things Schmitt shows me in his cozy, bookshelf-clad office is an article one of his students, Lasse Hubweber, wrote on longhorn beetle penises. As we have seen before (when discussing René Jeannel and his cave beetles), the beetle penis usually consists of a tough capsule from which it can conjure an inflatable internal sac, and longhorn beetles are no exception. Like cave beetles, the internal sac of the longhorn beetle penis is studded with painful-looking spines and bristles. The electron microscope photos in Hubweber’s article don’t leave much to the imagination. The penis of the graceful European species Alosterna tabacicolor carries rows and rows of shark-tooth-like backward-pointing spines. And the black-and-white Southeast Asian Chlorophorus sumatrensis can extrude a ghastly-looking, rasp-like tube with solid outward-pointing teeth. “Quite something, huh?” says Schmitt.

  Of course, having spines on your penis is nothing peculiar to longhorn and cave beetles. Many beetles have this, as do banana, carrion, and caddis flies, and certain larger animals, too—in this book we have already come across the spiny penises of elephant shrews, rodents, and ducks. Then there are the colubroid snakes, proud owners of two penises, each a fascinatingly beautiful bouquet of red and deep purple grooved, multitoothed spikes, like a clutch of medieval halberds. Hoary bats sport long needles on their glans that are longer than the glans itself. And finally the mysterious but aptly named “caltrop cornuti” on the penises of certain moths. These star-like multipronged thorns, similar in shape to the caltrops scattered on the ground in warfare to slow down pursuing armies, are detached from the penis during mating and stay behind in the female moth’s genitals.

  Nobody knows what sinister purpose caltrop cornuti serve, but to understand what the more run-of-the-mill spines on the penises of, say, seed beetles are for, we have to turn to Swedish researcher Göran Arnqvist of Uppsala University.


  The first time I meet Arnqvist is in a small, crowded seminar room at the University of Groningen, where we are both attending a symposium on sexual selection. Slim, friendly, and sharp faced, his chin adorned with an infinitesimal goatee and his left ear with an earring, Arnqvist shows me a photo of a toilet-brush-like seed beetle penis and confides, “It looks nasty and it is nasty, too, but it is a fascinating structure!” Having first worked with water striders, flour beetles, and the occasional bedbug or bird, Arnqvist has spent much of his research time since 2002 studying the genitalia of the seed beetle Callosobruchus maculatus. Not that there’s anything special about this species compared with the many other beetle species that have spiny penises. It’s just that seed beetles are really easy to keep in the lab. Regularly furnish them with petri dishes of dried mung beans and they breed like rabbits.

  In 2000, a few years before Arnqvist turned to Callosobruchus, Helen Crudgington, a student of Mike Siva-Jothy’s (whom we met in the context of traumatic insemination), had already published an article on seed beetle genitals in the journal Nature. She had poured liquid nitrogen over copulating pairs, and then dissected the genitalia, frozen in action, to figure out what the spines are really for. As it turned out, the spines were certainly no harmless ticklers: they pierce the wall of the vagina and, in females that have mated several times, leave lots of tiny scars. Not surprising, then, that females try to kick away at males that keep these instruments of torture inside them for too long. When Crudgington immobilized a female’s hind legs with droplets of glue so she could not kick anymore, copulation lasted twice as long as in unhandicapped females, leading to twice as many intravaginal wounds.

  Crudgington and Siva-Jothy came up with two explanations for the evolution of these perforating penile bristles. Perhaps, they said, the wounds would make a female so sore that this would bolster her determination to resist subsequent males—which would be good news for the male responsible for the damage. Another, more interesting possibility was that the punctures caused by the spines would be a way for manipulative substances in the semen to enter the female’s bloodstream directly.

  Unable to decide between both options, Crudgington and Siva-Jothy left it up in the air—until, a few years later, Arnqvist took a stab at the problem. Literally. Together with colleagues Ted Morrow and Scott Pitnick, he carried out an experiment with several species of insects, including seed beetles, in which they caused “sublethal postmating harm” to the females—a euphemism for scientifically sanctioned insect harassment. This is what they did: As soon as a male dismounted, the researchers would hurt the female by puncturing her thorax and elytra with the tip of a very fine needle. Then they waited to see if this painful experience would make a female once bitten, twice shy about any more sexual encounters. It didn’t—not in insect species with spiny penises or in species with smooth ones. If anything, the female would mate again more quickly than if she had not been hurt.

  With this one hypothesis struck off, Arnqvist and his team turned their attention to the alternative explanation: that the spines would help semen substances enter the female’s bloodstream more easily. Over the next few years, they (and in particular graduate student Cosima Hotzy) carried out an intricate series of experiments that proved that, like the flesh-eating substances in housefly semen, their role is to perforate the female’s thick inner vagina wall, creating a passage for the male beetle’s semen. They figured this out in a remarkable way. First, they fed males a radioactive diet, causing them to ejaculate radioactive semen, and after mating with nonradioactive females, the researchers could see the radioactivity seep from within her vagina into her blood. So far, so good—semen was passing into the female’s blood. Next they needed to show that the spines were responsible for this. For this, they contacted Michal Polak and his laser gun.

  Dr. Polak’s lair at the University of Cincinnati houses an extremely accurate microlaser—the only one of its kind in the world. “It’s a great system,” says Arnqvist. Like a Dr. Evil of entomology, Polak can train his laser beam at a helplessly prone insect fixed in a minuscule operating theater under a microscope. The laser beam is so thin and can be maneuvered with such accuracy that Polak’s machine can zap away individual hairs—and, indeed, individual penile spines. “Prft! Tzieeeeeeuw!” goes Arnqvist, in uncanny imitation of a laser beam. “It’s amazing. It’s absolutely amazing!” He still cannot control himself at the recollection of his student taking out individual spines, 0.05 millimeter (0.002 inch) long, on the extruded penis of an anesthetized 3-millimeter-long (0.12-inch) seed beetle.

  Thus having performed microsurgery on a whole contingent of male beetles, the team managed to prove that male beetles with thirty spines removed from their penises mated just as long and ejaculated just as much semen as males with only ten spines missing, but they caused fewer wounds in the female vagina, and much less of their semen made it across the vagina wall into her blood. Finally, they also were able to show that this had an impact on the number of their mate’s offspring that the males fathered: the more spines remaining, the greater a male’s success at siring baby beetles. And if this weren’t convincing enough, the team repeated all these experiments by comparing males born naturally with longer or shorter spines. Again, long-spined males fared better in the baby-making department.

  The implications are clear: spiny penises in seed beetles probably evolved because they make it easier for the proteins in a male’s semen to be thrown directly into the chemical cogs and wheels of a female’s hormonal system, thereby reducing her tendency to mate with other males or in some other way hijacking her sex life to suit his interests. But this does not mean that all priapic spininess in the world evolved in the same way. And it also does not explain why early humans lost theirs.

  Humans are among the smooth minority of primates. The males of most species of ape, monkey, tarsier, lemur, galago, and loris, on the other hand, have tough little spikes on their glans or sometimes all along the shaft of their penis. Even our close relative, the chimpanzee, has such roughness in the groin area. And although the spines, little nail-like outgrowths of the skin, are minute in many primate species, they can sometimes become quite impressive. In galagos, for example.

  Galagos—or bush babies as they are sometimes called because of their wailing calls that emanate from the forest at night—are small nocturnal gremlin-like primates from Africa. Most of the species are tiny, weighing in at just a few hundred grams, and live much of their big-eared, large-eyed lives clutching tree trunks in the forests of the great continent. Only a few decades ago, zoologists thought there were at most seven species. Now the number stands at forty and counting. And most of those new species have been discovered not by exploring far-flung fragments of rainforest, but by intent peering between the legs of known galago species. As it turned out, many new species were hidden among more familiar species.

  The male genitals of galagos proved to be a taxonomist’s gold mine. While many newly discovered bush babies are pretty similar on their furry outside, their penises betray their distinctness. Skin markings, shape and size of the glans, the extent and form of the penis bone—all these are features that help distinguish one galago species from another. But prime among these characteristics are their penis spines. Most galagos have them, but some species have small ones of just a fraction of a millimeter, whereas others, such as the critically endangered Rondo dwarf galago (Galagoides rondoensis), discovered in 1997, has a bunch of mean backward-pointing teeth of up to 3 millimeters (0.12 inch) long. On a thin club-shaped penis of barely 2 centimeters (0.8 inch) total length, that’s massive. And there is not just variation in the spine size, but also in their design. Alan Dixson, whom we met before in this chapter in his role as primate mating plug classifier, has cataloged all manner of spines on galago penises, and distinguishes three different kinds: type 1, small and short; type 2, large and thicker at the base; type 3 (hold your breath), multipointed.

  It’s a pity tha
t we do not yet know whether these primate penile spines serve the same function as the ones in seed beetles. On the face of it, it seems likely that they, too, could rupture the skin of the inner vagina, allowing some of the semen proteins entry into the female’s blood. It is known from rodents with spiny penises that after a couple of copulations, females’ vaginas get so raw that they refuse any more hanky-panky.

  Alan Dixson came close to answering this question. Back in 1991, he published an article in the journal Physiology and Behavior in which he described his penis despining experiments on male marmoset monkeys, tiny treetop primates from Central and South America. Not with a microlaser, as Arnqvist used on his seed beetles, but with simple commercial depilatory cream. Since the spines are made of keratin, the same substance that hair consists of, dehairing cream removes penile spines just as it does unwanted facial or other hair. Dixson discovered that the males that had lost their spines had more trouble finding the female’s vagina after mounting her, leading the researcher to speculate that the spines may have a sensory function. Unfortunately, he did not test their effect on females, so we still do not know whether perhaps they also are important in sperm competition.