Nature's Nether Regions Page 17

  While we’re at it, Tidarren has more surprises in store in the mating plug department. Knoflach discovered an even more extreme case in another species, Tidarren sisyphoides—the same species for which Margarita Ramos proved that having one pedipalp is less cumbersome than having two. In this species, it turns out that the male uses his entire body as a chastity belt! As soon as copulation has begun, the puny male, his oversized pedipalp happily pumping away, stiffens and dies—just like that. The female does not cannibalize him, but for hours after mating walks around with her dead lover affixed to her genitalia. Only hours later does she remove his corpse-cum-plug and discard it.

  Since in most animals males normally hope to use their genitals more than once, not many animals besides spiders have evolved mating plugs that require the amputation of parts of their penis or even of their entire penis. But there are other ways to produce a mating plug. One option: add two-component glue to your ejaculate.

  Solid Semen

  A well-known zoologist once said, “If you want to discover something new, then don’t read old German literature.” And indeed, the time-honored Central European tradition of meticulous dissection and painstaking monographic description of anything that walks, crawls, swims, or slithers also produced the very first discovery of a glue-like mating plug. Back in 1847, Leipzig zoologist Karl Georg Friedrich Rudolf Leuckart first winkled what he called a “vaginal plug” from the pudenda of a guinea pig. As we now know, in this and many other rodents, immediately after ejaculation part of the male’s semen solidifies inside the female and turns into a solid plug that forms a perfect cast of her vagina and remains stuck there for up to several days, rendering her genitalia inaccessible for the rest of the fertile period of an estrus cycle.

  And not just in rodents. Insects, shrimp, nematode worms, snakes and lizards, and many other mammals besides rodents produce such plugs. This includes primates. In 1930, a scientist named Otto L. Tinklepaugh was the first to discover that even our closest relative, the chimpanzee, makes solid sperm plugs. Working in Yale’s primate center, he was studying the sexual cycle of one female chimp and her consort by flushing her vagina daily with a blunt-tipped syringe and doing smear tests on the effluent. During the female’s estrus, often his syringe would get clogged by strange bits of hard material. In the end, he managed to retrieve from her vagina a hard, solid plug measuring 7 centimeters long and 1.5 centimeters thick (or 2.75 by 0.6 inches). “Shaped much like the finger of a glove,” Tinklepaugh wrote in the short article in the Anatomical Record that he devoted to the matter.

  Since Tinklepaugh’s days, primatologists have taken to observing up close the sex lives of all imaginable monkeys and apes, and we have already come across a few memorable examples in this book. The spoils of these decades of sexual scrutiny include a veritable catalog of mating plugs in lots of primate species, and in 2002 Alan Dixson and Matthew Anderson of the San Diego Zoo published a compilation. Even among our closest relatives, the great apes, three different types of plugs could be discerned. First, there were the solid finger-like plugs produced by chimp and bonobo semen. Second, in orangutans, semen in the female’s vagina coagulates into rubbery globules but does not form a single solid plug. And third, in gorillas and humans, semen congeals into a squishy, shapeless gelatinous mass. Mapping these three types across all forty primate species in their list, Dixson and Anderson saw an interesting pattern: the more promiscuous the females were known to be, the more likely it was that the male left behind a heavy-duty mating plug of the chimp/bonobo type—a sure sign that plugging, also in mammals, is a way for males to counter sperm competition.

  But how does liquid semen manage to turn into something with the consistency of putty? Fortunately, decades of research into male (in)fertility have given us a very detailed insight into the various proteins, salts, sugars, and other constituents of semen and how they work together. Allow me a brief recap of mammal male sexual function.

  The sperm cells are, of course, produced in the testicles and, when half-baked, are moved to the epididymis, a tightly coiled tube (stretched out, it would be six meters long in humans!) that is packed into a slug-like lump at the back of each testicle. While moving along the length of these six meters, the sperm cells mature and accumulate, poised for action, in the tail part of the epididymis. On the verge of orgasm, tight packs of these mature sperm cells are squeezed out of storage and pushed along the thin tube (vas deferens) that passes around the bladder and then, behind it, meets the seminal vesicles. These glands sit at the confluence of the two vas deferens tubes coming from both testicles, and they produce some two-thirds of the liquid of the semen. They also add a cocktail of proteins, including so-called semenogelin. Remember that name.

  Having received the seminal vesicles’ contribution, and orgasm now well under way, the semen rushes on via the vas deferens tubes (which here and beyond are fused into a single tube) to meet the next gland, the prostate. This adds some additional liquid of its own, containing, among many other constituents, an enzyme called transglutaminase 4, or TGM4. But rather than mixing the prostate-derived component with the rest of the semen, tight coordination of the muscles in the walls of the prostate and the vas deferens, which by now is called the ejaculatory duct, ensures that the portion added by the prostate remains a separate wave riding in front of the droplets released by the seminal vesicles. Finally, the stream of semen passes along a pair of small glands called Cowper’s glands, which have been busy oozing clear lubricant into the ejaculatory duct since well in advance of orgasm, and much of which is added to the bow wave of the semen as it picks up speed at the base of the penis and is finally ejaculated in a series of pulses caused by those familiar 0.8-second genital spasms that we met in Chapter 4.

  Biochemists have made use of the spasmodic nature of ejaculation by catching separate ejaculate droplets in separate cups and studying the constituents of such “split ejaculates.” It turns out that, thanks to the successive contributions of the various glands, the first few drops of ejaculate contain mostly sperm cells and semen produced by the prostate and the Cowper’s glands—including TGM4—whereas the later droplets are poor in sperm cells but rich in seminal vesicle fluids and therefore contain a lot of semenogelin. Once inside the vagina, TGM4 and semenogelin come in contact with each other and start a biochemical interaction. Like all proteins, semenogelin consists of a long chain of amino acids. TGM4 specifically singles out one kind of amino acid (called glutamine) in these chains, and connects this to another amino acid, lysine, in neighboring semenogelin molecules, creating a tangled web of cross-linked chains. It is the same process that is responsible for the toughness of our skin. And it is what causes the solid mating plug to form.

  Obviously, semenogelin and TGM4 should not meet each other before it is time for a mating plug to form, which explains why they are produced and stored by two separate glands inside the male’s body. Like the two constituents of two-component glue, they mix only when squirted out. Now, genes to produce semenogelin and TGM4 are present in the DNA of all apes and humans, so why the big difference in plug consistency? The answer lies in the exact structure of those DNA blueprints.

  While still an undergraduate student at Brown University, primatologist Sarah Kingan did a research project on the DNA code for semenogelin in humans, chimpanzees, and gorillas. She discovered that the code in gorillas was so garbled that it had stopped producing a functioning protein. And Sarah Carnahan of Duquesne University in Pittsburgh found that the same was true for TGM4. This makes sense, since gorilla males monopolize their females, so their semen rarely, if ever, needs to compete with that of other males—mating plugs would be superfluous. No wonder that mutations rendering their glue components useless could have accumulated in these apes without doing any evolutionary harm. In fact, Carnahan found this held true in the siamang gibbon, a smaller species of ape that fosters long-term monogamous pair bonds, also freeing their semen proteins from the task of dealing with
rival sperm.

  As Kingan and Carnahan discovered, however, the situation is different in chimps, bonobos, orangutans, and humans, where sperm competition is a greater risk (although we like to think of ourselves as basically monogamous, humans are still much less faithful than siamangs). In these species, the genes are all still functional. Not only that, but especially in chimpanzees and bonobos, the DNA sequences show telltale signs of rapid evolution. Their semenogelins have become much bigger, creating additional lysine-glutamate links to be forged by TGM4 and, hence, producing a more sturdy mating plug. The story does not end there, though, because recently the female side of the story has also become clearer—albeit in mice, not men.

  In a 2013 article in the journal PLOS Genetics, Matthew Dean of the University of Southern California gave a new spin to the mammal mating plug story by using mouse knockout. Rather than an unfair kind of boxing match, “mouse knockout” refers to the geneticist’s trick of disabling certain genes in lab mice. There’s even an International Knockout Mouse Consortium (don’t laugh), a worldwide collaboration to create families of genetically engineered mice that lack certain genes. For many of those genes, even though the geneticists know exactly how to knock them out, the precise function is still unknown. Finding out those functions is what knockout mice are for, by studying which faculties are impaired in a mouse with a particular gene knocked out. What Dean did was ask the IKMC for a couple of mice that had had their TGM4 knocked out and set up tests in the lab to compare these males’ mating success with that of regular mice.

  As expected, the semen of mice lacking TGM4 proteins failed to congeal to a proper mating plug inside the vagina of Mrs. Mouse. But in addition to making the male prone to sperm competition from other males, the absence of the TGM4-induced plug seemed to have more effects. Dean found that far fewer sperm managed to migrate up the female’s reproductive tract after insemination with TGM4-less semen than with regular, coagulating semen. This means that, in addition to blocking subsequent males, the mating plug may also help prevent sperm dumping by the female. Dean discovered that of the TGM4-lacking sperm that did make it to the fallopian tubes, fewer pregnancies resulted than would normally be the case. So, apparently, a mating plug also prevents active embryo abortion by the female (see Chapter 4), which, says Dean, may be due to continued “physical stimulation” of the female by the plug long after the male’s penis has disappeared from her vagina.

  Again, we see that a mating plug, which superficially seems just another nasty trick by the male to enforce chastity in his female, may actually have a more subtle role. Yes, it makes it harder for subsequent suitors to add their sperm, but at the same time a plug may prevent sperm dumping and be a postcoital echo of the penis’s sensory courtship. Moreover, as we saw in the Tidarren spiders in which the female helps the male detach his pedipalp to act as a chastity belt on her epigyne, females sometimes cooperate in letting a male plug her genitals.

  Research in squirrels has likewise shown that the female’s role in the whole plugging business may not be passive. In two consecutive winters, zoologist John Koprowski woke every morning before dawn to observe the morning mating rituals in the two species of tree squirrels on his University of Kansas campus grounds. During the winter mating season, gangs of squirrel males hang around impatiently near the entrance of a female’s den and try to mate with her as soon as she, sleepy eyed, makes her appearance. Registering copulations through his binoculars, Koprowski saw that in more than half, as soon as mating was over, the female would nibble away at the mating plug—roughly the same size and shape as a cigarette butt—or chuck it to the ground. But in all other cases a female seemed happy to keep the plug sitting in her vagina until it naturally dissolved a day or so later. Perhaps a nice and solid plug is a good thing to keep in your vagina for a little while. Either for “physical stimulation” or because a male that can lay down a decent mating plug is the kind of father you’d like for your sons . . .

  Substance Abuse

  Let’s wallow in semen a little while longer, shall we? We have already seen that, even in humans, there is more to this substance than meets the eye. It contains proteins that, when mixed together, can forge a mating plug. It also contains sugars as sperm fuel, proteins that protect the sperm cells from the acidic vaginal environment, zinc that keeps the sperm’s DNA in good shape, and chemical compounds that prevent the sperm cells from becoming overenthusiastic prematurely.

  But this list of ingredients is just the tip of the iceberg. Human ejaculates are home to hundreds of different proteins (which in certain women cause a kind of “sperm hay fever,” an allergic reaction to semen). And those are not trace amounts either; most of them occur in considerable concentrations, so they must be doing something important—we just don’t know what. Even in the ejaculate of the lowly banana fly Drosophila melanogaster, researchers have identified no fewer than 133 different kinds of proteins. One hundred and thirty-three! And this excludes the many proteins that are in the sperm cells themselves. These 133 are all produced by the banana fly version of the prostate, which releases them into the liquid portion of the semen.

  Fortunately, banana flies being the lab biologist’s workhorse, we know quite a bit about what their seminal proteins do—or at least more than we know about their human counterparts. To begin with, we know that they evolve as fast as the genitalia that deliver and receive them. Rama Singh of McMaster University in Hamilton, Canada, has been studying the protein cocktails in different species of banana flies and has discovered that the DNA codes for these genes, while remaining functional, are constantly and rapidly changing along the branches of the banana fly evolutionary tree. “The fastest evolving proteins we know,” he says. And a sure sign they are perpetually pushed around by sexual selection.

  Banana fly researchers are quite confident that some of the ingredients of these biochemical cocktails are involved in a kind of neuropsychological manipulation. They hijack a female’s hormonal system by shutting down her sex drive, causing her to go completely off males for up to several days after having received a load of semen. Females that have recently been inseminated start kicking away their suitors or, when harassed, extend their egg-laying tube, which blocks access to the vagina. They even begin exuding a scent that renders them unattractive. All this is induced by semen components that end up in her bloodstream. Usually, females prefer to have multiple fathers for a clutch of eggs—to generate healthy genetic diversity. But by usurping a female’s decision to add other males’ sperm to the mix that she is using to fertilize her eggs with, a male thus can prevent sperm competition. The whole process is akin to leaving a mental mating plug.

  One of the substances that have such an “antiaphrodisiac” effect is sex peptide, a small protein molecule—small enough to pass straight through the wall of the vagina into the female’s bloodstream—that is produced in the glands that sit next to a male fly’s genitalia. It is present in the semen but also sticks to the tails of the sperm cells. The sex peptide that is floating free in the semen does its work quickly: even before mating is fully over, it has already seeped through the vagina wall into the female’s blood, and within minutes begins to stick to receptors near her brain, where it makes the female’s interest in other males plummet. For up to seven hours, the initial shot of sex peptide causes females to give males the cold shoulder. Meanwhile, the sex peptide that sits on the sperm tails is beginning to break free, sustaining a steady IV drip of antiaphrodisiac that lasts for about a week—enough time to give the sperm a free passage, unchallenged by other males’ sperm.

  Sex peptide is only one of the multitude of chemical compounds in semen that a female banana fly receives each time she mates with a male. What do the rest do? Well, research in other insects can give us an inkling of what such substances might be capable of. The semen of the American fire beetle Neopyrochroa flabellata, for example, is spiked with the poisonous compound cantharidin. Although in the human world this subst
ance is known as the infamous aphrodisiac “Spanish fly,” the benefit gained by the male fire beetle is not his mate’s increased ardor, but rather the fact that the stuff ends up in the eggs fertilized by his sperm, which protects them against being eaten by ladybird beetles. Another substance, the protein PSP1, is ejaculated by the male corn earworm moth into his mate and there immediately shuts down the production of pheromones, meaning that other males (which totally rely on scent) can no longer find her. And then there’s Argas persicus. In this tick, believe it or not, the male produces a soda-bottle-like spermatophore from his genitalia, takes it into his jaws, bites off the cap, and then sticks it, neck first, into the female’s vagina. The appearance of carbon dioxide bubbles inside the spermatophore then forces out the sperm and other contents into the female. And at least one of these contents is a compound that cranks up the female’s egg production rate—which may mean more offspring to be sired by these sperm.

  This list makes one wonder whether some of the many proteins in human semen could also have such manipulative effects. If they do, then this would be one way to explain the results of a study by Gordon Gallup and Rebecca Burch, whom we already caught red-handed in Chapter 6 while applying a dildo to a latex vagina filled with artificial semen. In this other study, they had almost three hundred female students fill out questionnaires relating to sex and mental health. The results showed that women who always use a condom—and so are protected against the effects of proteins in the semen—score almost 50 percent higher on a scale of depression-related symptoms than women who never use condoms, which might indicate (but doesn’t prove) that substances in semen interfere with the female nervous system. And there is also evidence that pregnant women who have unprotected sex with their partner during pregnancy are less likely to suffer from so-called preeclampsia than women who use a condom. Since preeclampsia is a kind of inflammation of the woman’s body induced by her fetus—basically the mother becomes allergic to her own child—this might mean that substances in the semen take over part of the regulation of the woman’s immune system.