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  Later that same year, in the Journal of Experimental Biology, Koene and Chase revealed what must be the true evolutionary reason behind dart shooting: sexual manipulation. They had noticed that when shot, the dart is covered with a thick mucus, produced by glands that sit on the dart sac. They then surgically removed the female reproductive organs and, keeping these alive in a petri dish, applied this mucus to them. Immediately, peristaltic movements began to ripple through the tube-like organs.

  To understand what this means, we must explain what happens in the boy bits and girl bits of a snail during hermaphroditic sex. As copulation starts, the male genitalia begin packaging a large amount of sperm into a parcel, the spermatophore. This parcel is then placed via the penis into the so-called diverticulum (a blind side pocket) of the partner’s female genitalia. From there, the spermatophore is eventually transferred to another organ, the bursa, which is a kind of stomach dedicated to digesting the spermatophore, sperm and all. So how do snail eggs get fertilized if all the sperm is consumed? Well, at some point between deposition in the diverticulum and transfer to its nemesis, the bursa, a few sperm cells (usually just a few hundred out of the more than a million that sit inside the spermatophore) gingerly escape via the tail of the spermatophore and travel up the oviduct toward the eggs. The more sperm escape, the more eggs may be fertilized. And this is where the love dart comes in: the mucus that the dart is laced with contains a hormone-like substance that, when the dart is shot deep into the snail’s skin, triggers those involuntary ripples of the diverticulum. These help to absorb the spermatophore more quickly; they also close off the entrance to the bursa and thus increase the shooter’s chances of fatherhood.

  That these chances are indeed improved was proven a few years later by Chase and his student Katrina Blanchard in a beautifully simple experiment they published in the Proceedings of the Royal Society B. They had managed to perform microsurgery on snails—yes, this meant anesthetize them, make an incision, amputate the dart sac, sew the patients up again, and let them recover. When they then let these dartless snails mate with other snails, and injected the partners using a syringe filled with either dart sac extract or innocuous saline solution, they found that the saline had no effect, but the dart extract boosted the number of baby snails fathered by the dartless snails to twice what it would otherwise have been.

  It is not unimaginable, says Koene, that whatever substance it is that Deroceras slugs deposit on their partners’ skin at the end of mating serves a similar function as the hormone-like substance that the snail love dart is spiked with. Still, why is there so much diversity in the parts of the genitals that are involved in chemical persuasion? The biggest differences among different Deroceras species are in the sarcobelum, and we have seen that the molluscan Cupid has likewise provided thousands of snail species with all manner of love’s arrow: long, short, thick, thin, curved, straight, round, or flanged. So why this diversity? Wouldn’t we expect that all species would eventually converge on the kind of device that works best? Well, yes, we would—if simultaneous hermaphrodites weren’t such sexual schizophrenics.

  The male portion of a snail’s or slug’s genitals—its entire apparatus for packaging and delivering sperm together with the chemical cocktail injected into the partner to boost the sperm’s chances—is optimized by generations of success in acting like a male. But at the same time, its female genitals—the part of the body that receives and processes spermatophores—is designed to serve its female interests best. For a healthy egg clutch it may be much better to fertilize only a few of your eggs with sperm from each mate. And digesting most of a mate’s spermatophore might be one way of achieving that aim.

  The evolutionary result of this conflict of interest is not a status quo. It is the same kind of never-ending dance that we have seen in the mutual accommodation and evasion of the genitalia of males and females. Here, however, it has its impact not on separate sexes but on the separate parts of the genitalia of a single hermaphroditic animal. Improvements to the male system, such as transferring more hormone-like substance by adding flanges to the dart or multiplying the number of darts, will meet a response in countermeasures in the female system, like making the diverticulum deeper and thus harder for sperm to escape from. This will then be followed by a new round of male measures (perhaps stabbing repeatedly rather than just once, and loading the dart with fresh mucus each time it is withdrawn), and yet again female countermeasures (maybe adding side pockets to the diverticulum). And since these histories of making love and war are basically unpredictable and can go in different directions and involve different “inventions” in different species, diversity is the result.

  In the end, every snail or slug is saddled with the outcome of this generations-old conflict of interest: its male genitals try to do exactly what its female genitals won’t allow. Perhaps one of the reasons that simultaneous hermaphrodites have been eschewed by scientists studying sexual evolution is that it is so hard for us—gonochorists as we are—to learn to think like a hermaphrodite. But once you do, says Koene, the insights gained are not to be sniffed at. “Having two sexes in one animal makes hermaphrodites twice as interesting!” he proclaims, and drops another lettuce leaf in the snail aquarium.

  Castration Anxiety and Penis Envy

  I once watched an Irish mollusk researcher, in a fit of slug chauvinism, try to convince an audience of biologists that slugs are superior lab rats. “Behaviorally speaking, a slug is basically a rat,” he told them. “Cover a rat in slime, amputate its legs, pull its genitalia up behind its right ear, and film it in slow motion, and you’ve got a slug!” Where their genitalia and sexual behavior are concerned, slugs indeed are a gold mine for research with seams even richer than Rattus norvegicus. We have already seen what amazing tricks a single slug genus has up its sleeve. But Deroceras is just the tip of the iceberg. Malacologists (this is what mollusk aficionados call themselves) are slowly beginning to dish out the slug sex smorgasbord that lies hidden under rocks and stones, both on land and in the sea. And, as we shall see, this is throwing up yet more surprises about how genital evolution works in simultaneous hermaphrodites.

  Sea slugs are perhaps best known for their wonderful psychedelic colors, especially in one particularly prominent and species-rich group, the so-called nudibranchs. Nudibranchs—“nudis” to friends—are named after the gills (branchia) that many species carry uncovered (“nude”) on their backs. One of the more modestly colored nudis is Aeolidiella glauca, a species that inhabits the cold shallow-water eelgrass beds along the shores of Northern and Western Europe. They prey on small sea anemones and they carry frills along their flanks in which they store the anemones’ venomous nettle cells, appropriating them for their own defense. But that’s neither here nor there. I mention A. glauca because it is one of the few nudibranchs—out of the more than three thousand species that exist—that have had their sexual behavior properly studied.

  We can credit our knowledge of A. glauca to Anna Karlsson of Uppsala University and Martin Haase of the University of Greifswald. Back in the late 1990s, Haase explains as I chat with him in the office he shares with his wife, ornithologist Angela Schmitz-Ornés, his boss ran into Karlsson at a conference and invited her to join forces with Haase. She was a novice Ph.D. student of reproductive biology in this common marine nudi, he a skilled anatomist of mollusks willing to try his hand at something new. Together they embarked on a series of discoveries that had their jaws dropping. And dropping. “Everything the church forbids is present in this species!” Haase exclaims.

  Aeolidiella glauca sex goes like this. When a randy individual runs into a potential partner, it first starts tailgating it. Sooner or later, the object of its love will turn around and face its suitor. Within a minute, this face-to-face phase then merges into “sidling”—the pair sliding past each other’s right-hand flank, where the genital openings sit. If necessary, the most eager of the two will nibble at the other’s genital opening
, as if to arouse the partner. First anchoring one with the other using flaps around the genital opening, the slugs then produce their huge penises. To Haase’s and Karlsson’s surprise, the slugs don’t insert these into each other as most other sea slugs do—the organs are too large for that. Instead, they release a sausage-shaped spermatophore from their penis, which they carefully place on each other’s back. Then they lift their penises and tap down on the spermatophore several times, as if to hammer it firmly in place. Usually both slugs accomplish all this in perfect synchrony.

  This phase of sperm transfer lasts only a minute or two, after which the two slither their separate ways. The real magic starts only once the mate has left. Within a few minutes, a slug with a spermatophore on its back will crane its head over its right shoulder to reach and then eat part of the spermatophore, increasing the distance between the genital opening and the spermatophore. Then it waits. Some three hours later, a thin file of sperm is seen to begin to break free from the spermatophore and to start marching over the slug’s skin toward its genital opening. The sperm being tiny, it takes several hours for them to reach their destination, despite the fact that the column takes shortcuts by swerving between the nettle-cell-containing lobes on the slug’s back.

  The slug is not a passive bystander to the sperm parade on its back. It seems to monitor the progress closely, and when it decides that enough sperm have entered its genital opening it will interrupt the flow by sucking up the sperm from its back. “You can really watch that!” Haase says. Then, its stomach full of hapless sperm, it will begin laying eggs, using the sperm that it did not eat up to fertilize them. Haase goes on: “I even watched two animals that interrupted the sperm with their mouths, then started to lay a batch of eggs, and when that was finished resumed sperm uptake from the thread that was still traveling across their back.” Haase winks at his wife at the desk opposite him. “When Angela first met me,” he says, “she googled my name and to her consternation found all these Aeolidiella publications of mine.”

  Sea slug sex is sure to come up with more surprises, Haase thinks. Only in 2012 were details revealed of copulation in another nudi, the Pacific species Chromodoris reticulata. Japanese researchers discovered that, though this species copulates in a more conventional way (penis in vagina), after mating the penis drops off, only to be replaced by a spare length of penis that the animal keeps coiled up inside the body. The coil is long enough for three matings before the whole system needs to be regrown. Nobody understands yet why such a throwaway penis evolved, but since sperm were found snagged by the barbs at the end of the penis, it may be a way to remove and then discard sperm from previous mates—a disposable hermaphrodite version of the sperm-scooper we have seen in damselflies.

  Land slugs also sometimes lose their penis. There is a report from Kazakhstan of a species of Deroceras (yet another one) that occasionally, at the end of copulation, bites off its own penis and then presents it to its partner as a meal. And the large yellow “banana slugs” (Ariolimax) of California do it the other way around: they sometimes chew off their partner’s penis at the end of coitus, sending it (now her) packing in emasculated state.

  Slug salacity reaches its pinnacle in the large, up to 20-centimeter-long (8-inch) “tiger slugs” of the genus Limax. These animals are native to Europe, but one species, Limax maximus, was accidentally introduced into the Americas, Australia, South Africa, and many other temperate and subtropical parts of the world—hence, they will be familiar to many. The animals are nocturnal, slithering around under cover of darkness, leaving thick shiny mucus trails on the ground and on trees they climb. But even by day they are hard to miss: with their pantherine, pied sandy-and-black presence they take up a lot of psychological space whenever one inspects underneath a log or stone or when pulling away a piece of dead tree bark. Though Limax maximus is the best known and the most widespread, there are in fact dozens of species, ranging in color from cream via deep red to sooty black, often with darker spots and stripes. And many of these lesser-known Limax species inhabit small areas in the Alps and other mountainous parts of Europe.

  Still, the diversity of Limax would probably have long remained unknown and unstudied if it weren’t for their peculiar genitalia. Remember barnacles? In Chapter 3, the burrowing barnacle Cryptophialus minutus was hailed as the animal with the world’s longest penis relative to its body size—eight times longer. As it turns out, some species of Limax are serious contenders for this title—a reputation that seems to speak to the imagination of some people. So much so, in fact, that a veritable scientific dynasty of respectable gentlemen-naturalists, three and a half centuries’ worth of them, have crossed swords over the nitty-gritty details of courtship, copulation, and—especially—penis length in Limax.

  The debate was opened in 1678 by English naturalist Martin Lister. In his treatise on English animals, Historia Animalium Angliae, he described, in Latin, how he had seen two large spotted slugs lower themselves in passionate embrace along a foot-long slime thread from a tree trunk while extruding and entangling their large, pale bluish penises into a bulky pear-shaped knot. A few years later, in 1684, his Italian colleague Francesco Redi (more famous for disproving the old belief that maggots are spontaneously generated in rotting meat) published a book containing his own observations on the mating of Limax. They could not be more different from Lister’s account. Redi did not mention any long slime threads, but instead spoke of entwined slugs, dangling down in apposition their extremely long penises, longer than a “florentine yard”—about 75 centimeters (30 inches)! He even provided a plate showing two rather cheerful-looking spotted slugs in possession of extremely long, intertwined penises that extended to the bottom of the page, far enough for Redi to use the rest of the space for other detailed drawings of slug anatomy.

  In the following centuries, a whole procession of natural history authors added their penny’s worth on Limax coitus. And time and time again, the observations confirmed Lister’s account, not Redi’s. Some small discrepancies were resolved by figuring out that there were, in fact, two species: Limax maximus descending from a long slime thread and engaging in a tight penile handshake in the form of flanged knot; and Limax cinereoniger, hanging by its tail tips and entwining the penises to form a dense bell-shaped coil. But while the penis sizes of these two species were respectable, they never approached the lengths claimed by Redi. So, with the advancing knowledge of Limax coitus, Redi’s observations began to sound more and more ridiculous, and by the early twentieth century H. Wallis Kew dismissed them as “quite obscure.” Surely, Redi must have exaggerated the priapic prowess of his Latin slugs! Either that or he had mistaken slime threads for penises.

  But in the first few decades of the twentieth century, as northern European malacologists leaned back, secure in the knowledge that all Limax’s mysteries had been solved, isolated reports began to trickle in from Italian and Swiss authors that seemed to confirm that Mediterranean Limax were indeed unbelievably well hung. Confusion reigned, but then came 1933. In that year, German zoologist Ulrich Gerhardt of the University of Halle published the first of a series of groundbreaking papers on slug sex. Apparently adopting a broad interpretation of his mandate as staff scientist at the Institute for Anatomy and Physiology of Domestic Animals, he carried out meticulous studies of slug behavior in large indoor cages. He did dissections, timed and filmed copulations, and, in good German tradition, described his discoveries with painstaking detail, here and there quasi-respectfully lashing out at previous, less patient colleagues. Having thoroughly documented the mating in Limax maximus and L. cinereoniger in more detail than ever before, he turned to the problem of Redi’s generously endowed Limax.

  Bernhard Peyer, one of the Swiss biologists who had, a few years earlier, claimed to have seen the same as Redi, mailed fifty live Swiss slugs to Gerhardt, who housed them in tall cages (tall enough to accommodate dangling Florentine yards—just in case). One evening, about two weeks after the a
nimals had taken residence in their new accommodation, one slug began showing interest in another by persistently following the slime trail of the object of its desire. Two hours later, by 10:00 p.m., the pair was circling each other on one of the vertical slats supporting the cage, creating a puddle of slime in the center. Approaching each other closer and closer, they began to entwine and started to release their heads, then the rest of their bodies from the surface, until they eventually hung by their tails from the sticky blob of slime. Then, ever so slowly, their penises began to peek out from their genital openings.

  Gerhardt waited up, notebook at the ready. By 11:30 p.m., the penises were still only 2 centimeters (0.8 inch) long, and had just begun to touch and stick together. Mating in Limax normally lasts only an hour or so, so one can imagine that Gerhardt at that moment must have had his doubts as to whether those long slug schlongs were ever going to form. But he waited, and waited, probably with the aid of many cups of coffee, and through the night both penises steadily grew under a slow pumping motion that let the tips swell and then shrink again in lively dance-like motions. At 3:45 a.m., they were 8 centimeters (3 inches) long. By 7:00 in the morning, 26 centimeters (10 inches), and Gerhardt could record in his notes that rice-grain-sized spermatophores were seen to be descending in the thin, bluish-translucent penises. At 10:00 the next morning, a full twelve hours after mating had begun, the penises reached their maximum length: the combed tips clung to each other a whopping 80 centimeters (32 inches) below their owners, precisely as Redi had said 250 years earlier. Since the slugs themselves are some 13 centimeters (5 inches) long, this comes close to the record-setting barnacle penis.