In this extended state, the pair hung still, meanwhile squeezing their spermatophores to the very ends of their penises. As soon as the spermatophores of both partners reached the end of the line, both slugs suddenly began hoisting in their penises while at the same time expelling the spermatophores from the orifice at the end of the penis. Then, with a sleight of hand so rapid that Gerhardt could dissect the events only by filming them at sixty-four frames per second, the comb-shaped penis tip unfolded to form a scoop-like tool, which first caught its own spermatophore, stuck this to the scoop of the partner, and simultaneously received the partner’s sperm package. Both animals then withdrew their penises with lightning speed, meanwhile sucking in the foreign spermatophore through the penis’s opening. By 11:00 a.m. the couple began to separate; half an hour later the final bits of penis were tucked away inside their respective genital openings, and both partners, hopefully as satisfied with the outcome as Gerhardt was, slithered away.
Sexy slugs. Limax slugs engage in exchanging sperm via their lengthy, dangling penises, which, in these hermaphrodites, are used to give and also to receive sperm.
The genitals and the behavior of this Limax proved so exceptional that Gerhardt considered the Swiss slug a separate species, which he named Limax redii to honor the discoverer of their unique mating behavior. Like many a lab rat, the two specimens that allowed Gerhardt his first peek into their love life then donated their bodies to science: they float, paled by almost eighty years of immersion in spirit, with pickled penises, in two glass flasks on a shelf in the natural history museum in Berlin.
In recent years, Limax has become a popular object of study among amateur and professional biologists in Austria, Switzerland, France, and Italy. Several Web sites are devoted to their biodiversity, which has led to the discovery of many new species. Rather than the handful known in Gerhardt’s day, the count now stands at thirty-three, and several of those—all occurring in Italy, Switzerland, and France—are now known to have similarly long penises as L. redii. On the Italian Web forum NaturaMediterraneo .com, latter-day disciples of Redi excitedly report their discoveries. Photos show proud malacologists standing by trees from which mating Limax hang, holding tape measures to document the record-breaking lengths of slime threads and penises. In one, of a Limax pair from Corsica, penis length reaches a calibrated 92 centimeters (37 inches). “Nuovo record del mondo,” the caption reads.
Besides confronting us with the unsettling notion that a penis can be both a sperm-delivering and a sperm-receiving organ in a hermaphrodite, the exaggerated Limax phallus is a good example of one of the main differences of opinion in the field of genital evolutionary biology. On the one hand, it could be the result of cryptic female choice. Or rather, “cryptic choice,” since we are talking hermaphrodites here. If longer penises are a preferred ornament, like a peacock’s tail, they would grow longer and longer during evolution. However, it could also be a sign of sexual manipulation: a struggle over who ultimately gets to play a more male-like role. The exact mechanics of the prestidigitation that goes on at the end of Limax copulation are not fully known yet, but perhaps a slug with a slightly longer penis is able to donate its spermatophore while at the same time avoiding accepting the partner’s.
And the remarkable copulation of Aeolidiella glauca may have evolved in a similar way. Other nudibranchs place their spermatophore closer to the genital opening, but there the receiving slug may easily remove it if the receiver feels so inclined. By placing the spermatophore out of reach on the partner’s back, and having its sperm sneak into the genital opening stealthily when the host isn’t looking, the ancestors of A. glauca would have had an advantage, at least until sperm sucking evolved. Koene admits that, faced with such bizarre hermaphrodite sex, he tends to think of arms races rather than of cryptic choice. “They have manipulation written all over,” he says. But then he adds that it is very hard to disentangle the two. “After all, even slugs may like to mate with manipulative partners,” he concedes.
Left Right After Sex
In this last section, I will showcase some of my own research in genital evolution to add yet another, final layer of complexity. After thoroughly immersing you in the baffling ins and outs of sexual selection acting on the genitalia of animals that come in male and female versions, I then asked of you to wrap your head around the confusing dualism of hermaphrodite reproduction. In this final section of the book, we will journey briefly into the strange looking-glass world of mirror-image hermaphrodite genitals, where everything is the same and yet completely different. At the end, we’ll come to see that, under certain conditions, genital evolution can even influence the shape of the entire body of an animal.
The story begins in 1989, when I was a young biology student arriving in Kuala Lumpur, Malaysia, to spend five months studying the particulars of a minuscule parasitic wasp called Trichogramma as it searched for the moth eggs that its larvae grow up in. (It was actually somewhat less frivolous than that may sound: the wasp was to be used to help control the caterpillars that were destroying crops of sweet corn.) But before starting my project—which turned out to involve mostly the staking out of fields of corn, inspecting the growing stalks for caterpillar frass while chasing off rampaging water buffaloes—I went on a short vacation to the sandy, rural, peaceful east coast state of Terengganu. On the recommendation of a local fisherman, I took a boat to a small offshore island named Kapas.
Today, Kapas is a bustling tourist destination where a dozen beach holiday operators ply their trade for boatloads of local and foreign visitors. Back then, it was deserted, save for six A-frame chalets rented out by a stray Englishwoman. The island’s two kilometers of pristine coconut-palm-fringed beach were the sole territory of the handful of chalet guests, the occasional green turtle paddling up the beach, and thousands of ghost crabs. It was my first time in the Tropics, and I could not get enough of trekking along the shore and through the forest and the coastal scrub. I saw my first hornbills there, my first flying lizard, and my first Nephila spiders—hand-sized frights that spin gigantic golden gossamer orb webs. But even more memorable than those were the Amphidromus snails suspended from trees and branches all over the island.
I knew about Amphidromus because the year prior to my Malaysian adventure I had spent in the malacology department of Leiden’s natural history museum, where my adviser, Edmund Gittenberger, had taught me that the snails of this genus—large, colorful tree snails occurring everywhere in Southeast Asia—are the only ones in the world that come in what appear to be even roughly mixes of clockwise- and counterclockwise-coiled individuals (in fact, Amphidromus means “turning both ways” in Greek). Almost all other snails, all 150,000 species of them, are either clockwise or counterclockwise, but never both.
The reason why snails normally don’t come in both types is easy to understand if we read an article written a century ago by the German naturalist Johannes Meisenheimer. Meisenheimer had found a contrarily coiled Burgundy snail (Helix pomatia). Normally, this snail twists clockwise, meaning that when one holds its shell with the tip up, the aperture (the opening from which the animal emerges) would be facing the viewer on the right-hand side. But the mutant that Meisenheimer had found was a mirror image, coiling counterclockwise, so with the aperture on the left. Such mutants occur now and then in most land snails, but they are extremely rare—often just one in ten thousand, or even rarer.
When Meisenheimer put his mutant in a jar with a regularly spiraling animal, it was clear that, at least in snails, being each other’s opposite does not make for a happy marriage. After all, it is not just the shell that is reversed; the animal’s whole body is also back to front. Its genital opening is on the left side of its head, not its right; its dart shoots leftward, not rightward. Its entire genitalia are mirror-imaged, and so is its brain—even its sexual behavior. The result was that “for days and weeks the animals fatigued each other in courtship, without ever achieving a final copulation,”
Meisenheimer observed with some sympathy. This means that a left-handed snail, if it should appear smack in the middle of a population of right-handers, would be dead on arrival, evolutionarily speaking: it would not have anybody to mate with. That is why all snail species are either clockwise or counterclockwise. And that is why Amphidromus snails, flouting this rule so openly and brazenly, are so special.
I dug up from long-term storage my memory of the Amphidromus of Kapas when, many years later, I landed a position in a Malaysian university and began a search for interesting research projects. The island of Kapas, with its particularly high density of Amphidromus snails (not to mention the idyllic setting), seemed the perfect place to solve that still puzzling conundrum of left- and right-coiled snails living side by side. So with a motley crew of colleagues, students, and volunteers, I set up a research project on Kapas (no longer pristine, but still very pretty) to unveil the secret of its mollusk inhabitants.
We had two study sites. Site 1 was in a bit of forest behind the Lighthouse Inn, a ramshackle hostel run by Din, a magnanimous, lanky, long-haired Malay with Rastafari leanings. Site 2 was farther north, in trees just behind the only beach that was still quiet enough for turtles occasionally to land there to bury their eggs (only to have them consumed immediately by the huge, dinosauresque water monitor lizards). In both places, the snails were plentiful and clearly came in two mirror-image versions: about 35 percent clockwise coiled, the rest counterclockwise coiled. We set about interrogating them in the only way that field biologists know how: by getting our hands dirty and scrutinizing their lives up close in the trees.
Enveloped in clouds of mosquitoes and against the background reggae music wafting in from Din’s place, we first checked if, like in all other snails, the coiling direction is genetic in Amphidromus. It was. Baby snails take the coiling direction that is dictated by their mother’s genes, so all young snails hatching from a nest of eggs should coil in the same direction. And that is precisely what we saw in the jelly-pearl-like egg clutches that the snails deposit in wet crevices in rotten branches and stumps: a family of newborn snails were either all clockwise or all counterclockwise.
Next, we figured, perhaps the lefty and righty snails have different roles in the ecosystem. Did they eat different things, live in different parts of the vegetation, or were they themselves being eaten by different predators? Nope. We spent a year writing numbers on the shells of live snails and following them around, but whatever their bent, the snails all mixed with alacrity, feeding and resting side by side in the same places. And the island’s forest rats that bite off the top whorls of the shell and then suck out the flesh like true gourmands also did not seem to care between left and right. They cracked and ate both in the exact proportions at which they occurred.
But while clambering around the foliage tracking marked snails, we began to notice something peculiar: now and again, on wet days, we found a left-coiled and a right-coiled snail having it off. Unlike Meisenheimer’s snails, they did not “fatigue each other for days on end” without ever consummating their desires. We began paying more attention to copulating snails. This was not easy, because the snails are not of a very passionate demeanor and mate only occasionally, usually during the onset of the monsoon season. Still, over the course of several years, we caught more than a hundred pairs of snails with their trousers down, as it were, and a surprisingly large number of those—in fact, more than expected even if they paired off randomly—were of a clockwise copulating with a counterclockwise. Apparently these mixed couples did not mind the fact that all their organs were in the wrong places, or perhaps even preferred to mate on the other side of the mirror-image divide.
One evening, as the thunderclouds were building up rapidly over the Terengganu coast, three of us sat down on a fallen coconut stem to work in assembly line style on marking a large pile of live snails with permanent marker, covering the marks with clear nail varnish, and writing down the details. Meanwhile we discussed the problematic sex lives of our snails. Ignoring the stunned stares of passing vacationers in swimming gear, we decided that we needed to find out what went on inside a mating pair of snails. How and, more important, why would Amphidromus seek out mates of opposite coil while all other snail species don’t and won’t?
Do you recall the Silhouettella spiders whose genitalia Matthias Burger studied, back in Chapter 3? And Helen Crudgington’s study of mating in seed beetles (Chapter 7)? They could discern the exact internal workings of the genitalia of these animals by pouring liquid nitrogen over mating pairs. As against my malacophile grain as this would be, we had no option but to replicate the same dreadful deed on these mating Amphidromus snails. Since bringing a gallon of liquid nitrogen to Kapas was not feasible, I brought the next best thing: freezer spray. Applied as a local anesthesia and also for cooling electrical components, a volatile liquid that freezes whatever you spray it on would also do the trick. So one year, as the snails began to respond to the first monsoon rains with their amorous escapades, I hiked around the island catching pairs in the act and booking them for eternity. After a few deft sprays, each couple, joined forever, sank to the bottom of a flask of alcohol—even death did not part them.
Back in the lab, I dissected the copulas. Mating in Amphidromus is not a fleeting affair: it lasts from dawn till dusk, and my specimens showed all the stages in this drawn-out process. As soon as mating takes off, both partners begin producing a 6-centimeter-long (2.5-inch) looped spermatophore. (Remember, we’re still talking simultaneous hermaphrodites here, so they fertilize each other at the same time.) They build this sperm package in the epiphallus, an extension to the penis, the inside of which functions as the mold in which the spermatophore is cast. As it turned out, the very tip, where the sperm eventually leave the package, was produced in a corkscrew-shaped appendix of the epiphallus. And what do you know? The coiling direction of the corkscrew turned out to be the same as the coiling direction of the snail itself: a clockwise snail has a clockwise corkscrew at its spermatophore tip, a counterclockwise snail a counterclockwise one! This feature is rather unique to Amphidromus; most other snail species have straight spermatophore tails.
This was beginning to get interesting. Now let’s move to the female side: the recipient. There, the spermatophore gets crammed in the bursa, that organ whose task it is to digest most of the spermatophore and all that is in it. Only that corkscrew tip sticks out of the bursa into the spot where the tube leading up to the eggs attaches. And this is where the magic happens. When I cut open the female genitalia, I saw that this tube attaches to the bursa under an angle; this angle is to the right in a clockwise snail, to the left in a counterclockwise snail. As I was quietly sitting on my lab stool behind my microscope, dissecting away, it began to dawn on me: the upshot of all this mirrored and contorted genital plumbing was that the mesh between a spermatophore tip and the female genitals is better if the mates are of opposite coiling direction! And this would probably also mean that more sperm made it out of the spermatophore and into the tube heading for the eggs! I made a little pirouette on my lab stool when I finally figured this out.
Mirror-image mating. Amphidromus inversus snails come in two forms: coiled clockwise and counterclockwise. This applies not only to the coil of the shell but also to the tip (A) of the elaborate sperm package (B). As it turns out, a clockwise sperm package fits better in the female reproductive system of a counterclockwise animal (C) and vice versa (D).
The situation in Amphidromus perhaps reminds you of the duck genitalia of Chapter 6 that show the reverse: a counterclockwise penis does not fit properly into a clockwise vagina. The funny thing is that fifty-fifty mixtures of clockwise and counterclockwise vaginas will never evolve in ducks, because the female will not benefit from making it easier for a male to penetrate her. In a simultaneous hermaphrodite like Amphidromus, things are different, because both partners, since they are both acting as males, benefit from mating with a countercoiled partner.
Paul Craze of the University of Sussex (and current editor of the esteemed journal Trends in Ecology and Evolution) came to Malaysia to work on Amphidromus with me, and he wrote a computer program to simulate what the effect of the snails’ hand-in-glove-like genitalia would be. Sure enough, Paul’s computer simulations showed that this would indeed produce a snail species with both coiling directions forever living side by side. We published our results in 2007 in the Journal of Evolutionary Biology as the first example of sexual selection and genital shape affecting the blueprint (clockwise or counterclockwise) of the entire body in an animal. And I present it here as the final example that genitalia hold the mirror up to nature.
•••••••••••
What have we learned from this tour through the bizarre world of hermaphrodites? First, that their genitals are every bit as weird as those of “regular” animals. In fact, they are often even weirder and more exaggerated. Contrary to what Darwin thought, sexual selection holds sway in their evolution as well. Although every amorous slug or snail is wired the same way as the object of its desire, this does not lead to mundane, matter-of-fact, “you want it and I want it” sex. Quite the contrary: since each prefers the male role, they have evolved a whole battery of tricks to bring out, as it were, the feminine side of their partner. Love darts, sperm transferred at the ends of exaggeratedly long penises, sperm nibbling, and ridiculously large spermatophores are all strategies that have evolved to persuade the other to be the one that accepts more sperm. The outcome of this struggle is an amplified and more manipulative version of what we have already seen in gonochorists. The pinnacle, if you will, of what genital evolution can do to a species, right up to and including turning your whole body back to front.
Nature's Nether Regions Page 21
