Nature's Nether Regions

by Menno Schilthuizen

  Incidentally, geneticists have figured out that, not too long ago, our immediate ancestors must also have had spines on their penises. When a team of biologists and bioinformaticians led by David Kingsley of Stanford University compared the genomes of mice, men, and chimpanzees, they discovered that humans lack a large chunk of DNA containing the switch that controls the gene responsible for keratin spines on mouse and chimpanzee penises. Presumably, somewhere along the evolutionary line between us and the common ancestor of us and chimps, this DNA got nixed. Some people believe that the wreath of soft “pearly penile papules” that about 20 percent of all men carry on the rim of their glans may be a vestige of the penile spines that our ancestors once may have had. But Kingsley thinks this unlikely. First of all, he writes on his Web site, all men, with or without papules, lack the DNA switch for spines. And second, the papules are soft lumps, not hard spines like in other primates.

  The answer to the function of penile spines in other primates is up for grabs. Perhaps someday soon an intrepid primatologist with a tube of over-the-counter depilatory will take up the gauntlet—and perhaps figure out how humans got to lose them, too.

  •••••••••••

  With that, we have come to the end of our evolutionary tour of the genitalia of primates, insects, and other so-called “gonochorist” animals—the term used when an individual comes as either a male or a female. We have seen that male genitals can do anything from gentle persuasion to all-out coercion, sometimes aided by sinister semen. Likewise, females’ crotches are not passive sockets but rather sophisticated sorting machines that select the best of the males on offer, while at the same time trying to stay one step ahead of their mates’ manipulation.

  But our story is not finished yet, for not all animals that copulate and have genitals are gonochorists. Get ready to ante up: in the final chapter, we will turn to those jacks of all sexual trades, the hermaphrodites. A hermaphrodite has the tools to be both male and female, to produce eggs and sperm, and to fertilize and be fertilized. So what do we expect for the evolution of their genitalia? Wouldn’t they be the epitomes of compromise? Well, quite the contrary, as we shall see.

  Chapter 8

  Sexual Ambivalence

  The two mating Deroceras praecox slugs on the video screen have been circling each other for more than two minutes now, languidly licking each other with some kind of tongue. A few of the students in Joris Koene’s mollusk anatomy class are beginning to go glassy-eyed and look away. This is not the spectacular slug sex they had been promised! But then Koene calmly announces, “Here it comes,” and forty pairs of eyes, some in midyawn, see how the two gently mating slugs—suddenly, without any warning, and with un-slug-like rapidity—eject huge, bluish blobs from their genital openings, from which is thrown a delicate translucent multifingered organ. A collective exclamation of awe rises from the crowd of students. Precisely simultaneously, like nets cast by fishermen, the glove-like protrusions that descend over both mates’ backs are then—together with the blobs to which they are attached—withdrawn almost as quickly as they appeared, and that is the end of it: two white masses are glimpsed to change owners, all genital bits are neatly tucked away in the slugs’ sex openings behind their right cheeks, and the slugs part and slither their own way. “Okay,” says Koene. “Who knows what they just saw?”

  What the students saw, of course, is just one snippet from the exotic world of simultaneous hermaphroditic genitals. Slugs, like most other land mollusks, many flatworms and earthworms, and lots of even more obscure animal types, are male and female at the same time. They produce eggs as well as sperm, they own a penis and a vagina plus the necessary plumbing, and they apply both of them in one go when they mate and fertilize each other’s eggs. (Most hermaphrodites will not resort to the ultimate narcissism of fertilizing themselves unless under duress—some species even put their own sperm in minuscule “condoms” to prevent self-impregnation.) And mutual fertilization—two-way copulation—makes for some spectacular footage, like the video produced by German slug researcher Heike Reise that Joris Koene showed to his students. Similar footage has slowly begun to leak across the divide between taxonomists and evolutionary biologists.

  Taxonomists have delved into the genitalia of hermaphroditic animals with as much gusto as they have in animals with separate males and females. The finger-like protrusions on the penis of Deroceras praecox are well known, as they had been duly recorded in the 1960s when Polish taxonomist Andrzej Wiktor discovered and named this species. Most of the hundred or so Deroceras species, occurring throughout Asia, Europe, and North America, are very similar on the outside and resemble, well, slugs: thin on one end, a bit thicker in the middle, and thin again on the other end. But their penises are all different. Actually, “penis” is a bit too simple a word to describe the intricate structure, which is why Deroceras specialists prefer to speak of the “penial complex.”

  Mutual consent. The hermaphroditic slug Deroceras praecox, at the cusp of mutual insemination, throws a multifingered gland onto its partner’s back, which probably contains hormone-like substances that increase the partner’s willingness to accept its sperm.

  The penial complex features—of course—the penis, which looks puny at rest but when aroused can be explosively inflated to almost half the slug’s body length. The penis is usually not a simple schlong, but is adorned with one or more pouches and finger-like extensions. These play a role in the transfer of the slug’s own sperm to the tip of its mate’s penis (we will see more of this penis-to-penis copulation later in this chapter) and in transferring its mate’s sperm into its own vagina—the white masses that were seen to trade places at the end of the copulation. Attached to the base of the penis is a tongue-like organ called the sarcobelum (the name is derived from the Greek term for “fleshy sting”), which is what the students saw the slugs licking each other with during courtship, in the early part of the video. At the end of the penis sits the penial gland. During courtship it engorges with a certain hormone-like compound, which is then splashed upon the mate when the penial gland is cast in the final throes of copulation.

  Slug taxonomists have been using the shapes of all these constituent parts—sarcobelum, penis, penial pouches, sacs, and glands—to distinguish those otherwise identical Deroceras species. The penial gland, for example, can be simple or branched, it can be small or large, and the fingers can be smooth or ribbed. And the sarcobelum is even more variable, ranging from the short, stout one of the widespread D. laeve to large structures like the one in the Central European D. rodnae that pretty much resembles a human tongue and with which the slugs lap each other’s bodies all over.

  So what do these things tell us? First of all, that Deroceras copulation is curiously complex for an animal that, superficially, seems rather humdrum. Why the long licking foreplay? Why carry a tongue on your penis? Why the explosive erection, but then no penetration? Why is sperm exchanged outside of the body? What is in the substance that this multifingered organ deposits on the partner’s skin? And second, the Deroceras penial complex apparently evolves like greased lightning: it is the only organ that really differs dramatically among a large number of closely related species. And Deroceras is not alone. In virtually all simultaneous hermaphrodites, be they slugs, snails, earthworms, or flatworms, exaggerated penis shapes and other genital exuberance is the rule. Of course, after seven chapters of genital extravaganza, this hardly comes as a surprise. We have seen the same in many, many kinds of gonochoristic animals (animals with separate male and female individuals, as you’ll recall).

  Yet that such genital profligacy should also appear in simultaneous hermaphrodites is unexpected. Although Darwin, in The Descent of Man, and Selection in Relation to Sex, quoted his contemporary Louis Agassiz, “Anyone who has had the opportunity to observe snail love, cannot question the seductive effects of the movements leading up to the dual embrace of hermaphrodites,” he assumed hermaphrodites to be
immune to unbridled sexual selection. After all, with both sexes imprisoned into one body, sexual evolution in these animals would be a matter of compromise, not of radicalism. And besides, Darwin thought them too dim-witted to see a difference between this or that mate: “[T]hey do not appear to be endowed with sufficient mental powers . . . to struggle together in rivalry, and thus to acquire secondary sexual characters,” he wrote. Up until the 1970s, received wisdom remained that sexual selection was lame in the hermaphrodite world.

  But Koene, an assistant professor at VU University Amsterdam and an expert on hermaphrodite sex, has seen evolutionary biology make an about-face on this, as he explains to me while feeding the freshwater snails he keeps in the basement of his lab. “We’ve come to realize that hermaphrodites, just like gonochorists, follow Bateman’s principle and compete to fertilize a limited number of eggs,” he says, stopping at a bubbling aquarium in which some twenty hermaphroditic pond snails crawl around. As he lifts the lid off the aquarium and plops in a few lettuce leaves, he explains: “Each of these snails carries some one hundred eggs, so let’s say there are two thousand eggs waiting to be fertilized in this tank. If everybody mates with everybody else, then each snail receives sperm of all nineteen other snails. So any way in which a snail can tip the balance in favor of its own sperm will be evolutionarily selected.”

  In other words, just like in gonochorists, a particular snail that has ways to persuade fellow snails to fertilize a larger than average proportion of their eggs with its sperm will cast its genes more widely in the next generation. Over a number of generations, most snails will be this successful snail’s descendants and will have inherited his/her superior persuasive or manipulative skills and devices.

  Still, following Darwin’s argumentation, we might expect hermaphrodites to be less amenable to such evolution, right? What with their being sexual generalists, rather than specialists? Wrong. “What Darwin was thinking of when he wrote that,” explains Koene, “is things like colorful displays and ornaments. Indeed, you don’t often find those in hermaphrodites.” But this seems to be more than compensated for by the evolution of particularly vicious genitalia. We have already come across a fair bit of traumatic insemination and harmful genitals in gonochoristic animals. Those examples pale in comparison to what is considered normal in the hermaphrodite realm.

  There are several reasons why hermaphrodite genital evolution has been taken to such extremes, according to Koene. You have to realize that for, say, a male insect to manipulate the reproductive system of a female, evolution has had to “invent” substances that latch on to key spots in the female physiology. After all, most of the genes that could produce real female hormones are switched off in a male insect. But in a hermaphrodite, the full set of male and female functions is turned on in all individuals. So a hermaphroditic slug could simply take some of its own female hormones and splash them onto its partner. Provided it packages the hormones properly so that they don’t interfere with its own female system, nothing stands in the way of this much more efficient way of manipulation. Therefore, hermaphrodites have much easier access to the tools needed to wield manipulative genitals.

  Another reason why genitalia and sexual behavior are somewhat different in hermaphrodites compared with what we are used to in animals with separate genders is that they have fewer reasons not to copulate. Whereas a female animal will mate only if she stands to gain something—usually meaning better fathers for her offspring—a hermaphrodite always has two options to weigh: it may not need to receive any more sperm for its eggs, but it would still be interested in donating some of its own sperm to the gene pool. The result of such split personalities is that when two hermaphrodites meet, there are four reproductive decisions to take, four roles to play, rather than just two, as is the case in male-female encounters. This means that in the complex maze of sexual opportunities that present themselves to a roaming hermaphrodite, a biochemical “yes!” will form in its brain much more frequently than in gonochorists. So, paradoxically perhaps, having done away with males and females has opened a portal to a more sexual, more promiscuous universe in which evolution has greater, rather than reduced, opportunity for experimentation.

  And experiment hermaphrodites have. Over the past fifteen years or so, evolutionary biologists have woken up to the fact that hermaphrodites live in a world where bizarre and often gruesome mating rituals involving particularly outlandish sex organs are the norm. Take, for example, the penis fencing in Pseudoceros bifurcus, a hermaphroditic marine flatworm of the Indian and Pacific Oceans. Practicing hit-and-run traumatic insemination with paired dagger-like penises, these worms, upon meeting a potential partner, generally prefer to inseminate rather than to be inseminated. So they rear up and engage in a duel of striking and parrying. An even better example is the love dart of land snails. The function of the calcareous arrow that many snails “fire” at close range from a special organ at the base of the penis had remained a mystery until the late 1990s. For a long time, it was thought to be a kind of courtship—a dowry in the shape of a bit of packaged chalk to be considered in cryptic “female” choice. But, as we shall learn in the next section, the truth is less pacific.

  Evildoers, Evil Dreaders

  Naturalists have marveled at snail sex and the associated wielding of love darts since the days of Aristotle, and one of the nicest descriptions comes from early nineteenth-century British zoologist Thomas Rymer Jones. “The manner in which [snails] copulate is not a little curious,” Jones writes in his General Outline of the Organisation of the Animal Kingdom. “After sundry caresses between the parties, during which they exhibit an animation quite foreign to them at other times, one of the snails unfolds from the right side of its neck . . . a sharp dagger-like spiculum or dart. . . . Having bared this singular weapon, it endeavours, if possible, to strike it into some exposed part of the body of its paramour, who, on the other hand, uses every precaution to avoid the blow, by speedily retreating into its shell. But, at length having received the love-inspiring wound, the smitten snail prepares to retaliate, and in turn uses every effort to puncture its assailant in a similar manner.” He then goes on to describe the “more effective advances” (penis erection and mutual insemination) that ensue, but closes with a sentence that drily encapsulates the wonder of the naturalist who thought he’d seen everything: “Such is the peculiar manner in which the amours of snails are conducted.”

  Peculiar indeed. In the edible escargot Cornu aspersum, during mating both snails launch a loose, nearly 1-centimeter-long (0.4-inch) limestone needle into each other’s flank. (At least, that’s where it’s supposed to go; it sometimes misses its target and ends up on the floor—or, worse, impales the partner’s head.) Next time you eat snails, you’ll know what it is that’s crunching between your teeth. But love darts are not unique to escargots, although this is probably the species in which Jones observed them. Similar weaponry is employed by many families of land snails and also by sea slugs and earthworms. In Europe, all Helicidae (the family to which Cornu aspersum belongs) have them, and also Chinese camaenid snails, the colorful Polymita from Cuba, and the ariophantid snails and slugs that live all over Southeast Asia.

  And although all are fired from the same sort of “dart sac,” a muscular bag that sits at the base of the penis, love darts differ quite a bit among snail species. In the Eastern European Monachoides vicinus, they look exactly like medieval archers’ arrows, complete with head, shaft, and fletchings. In Everettia corrugata from Mount Kinabalu on Borneo, they are hollow and furnished with a row of holes along the side, and in the Italian Marmorana snails they are, quite fittingly, the spitting image of a Roman soldier’s sword.

  Not only do the darts look different, they are also differently employed. Whereas Cornu aspersum carries a single dart that it shoots once, then growing a new one, the African slug Trichotoxon heynemanni has two darts, which it uses simultaneously, and in the Japanese “samurai snail” Euhadra subnimbosa ma
tes stab each other a staggering thirty-three hundred times during a single bout of courtship. Some snail species always shoot a dart; others do so only with certain partners. Some shoot before penetrating each other with their penises, others during, and yet others after. With such a diverse array of darts and dart-wielding behavior throughout the world of snails and slugs, there must be some important advantage to it, since, in evolution, elaborate organs and behavior will be done away with if they are useless.

  Cupid’s arrow. Many land snail species, when they mate, impale each other with a “love dart” (A). In different species the darts have different shapes (B). Without dart shooting, almost all sperm is broken down in the balloon-shaped bursa of the recipient (C). The dart is laced with a hormone-like substance that closes off the bursa and keeps the sperm in the “safe” diverticulum (D).

  For years, biologists had speculated that that advantage might be a “nuptial gift” of calcium. Snails build their eggshells, like the shells they themselves inhabit, from calcium carbonate, which can be hard to come by in some habitats. So if you supplement mating with a generous gift of calcium to your partner, conveniently deposited hypodermically, your partner may be able to lay more eggs, gratefully fertilized with your sperm.

  It was such a plausible hypothesis that it went untested for decades, until, in the 1990s, Canadian biologist Ronald Chase of McGill University in Montreal decided on a proper check of the idea. To do so, he hired Koene, then a young graduate student. “We were skeptical of the nuptial gift notion,” Koene explains. “Nuptial gifts may serve a purpose if they are given by a male to a female, but in simultaneous hermaphrodites, it doesn’t follow: I give you a box of chocolates, you give me a box of chocolates. What would be the point of that?” Together Chase and Koene started a lab colony of Cornu aspersum snails and began measuring the quantity of calcium in the dart, the amount of dart material taken up by the “victim,” and the amount of calcium needed by the maturing eggs. The results, as they reported in 1998 in the Journal of Molluscan Studies, simply did not add up: only one in twenty snails internalized a dart—the rest eventually squeezed them out of their skin. And on top of that, a single dart contained barely enough calcium to supply material for one egg. It was the death knell for the nuptial gift hypothesis.