Nature's Nether Regions

by Menno Schilthuizen

  Taxonomists never stop feeling privileged for being the ones to explore and discover firsthand this amazing diversity of form and shape. To them, dissecting out the genitalia of previously unstudied specimens is like unwrapping Christmas presents; never knowing what unexpected shapes will come to light, their concentrated, painstaking anatomical efforts behind the microscope are punctuated by muffled cries of delight. When I was still an impressionable grammar school boy and began frequenting the local meetings of the Netherlands Entomological Society (held in that deer antler lecture theater described in the Preliminaries), the first seminar I attended featured a famous Russian moth specialist. Frail and aging yet with such a youthful enthusiasm he could barely contain his glee, he told his audience how he had just finished studying a box of tiny pinned specimens collected in a faraway, previously unvisited corner of the Asian continent, home to lots of species new to science, and had been amazed by the genitals he discovered. Flashing some slides of shapely slivers of chitin covered in hairs and spines, he exclaimed in exasperation: “This. Is. Totally. Unheard of. And unseen!”

  To fully reveal the significance of this hidden beauty of sexual shapes, their sensuous implications, and the sheer endlessness of the terra incognita of forms requires not just science, but also art. Colombian-born artist Maria Fernanda Cardoso managed to pull this off with her project The Museum of Copulatory Organs. Throughout her career, Cardoso has used living and dead animal and plant parts to create mesmerizing sculptures from bones, dried reptiles, and butterfly wings. At the fifty-second Venice Biennale she represented Colombia with a large piece made out of dried starfish. And in the 1990s she gained international fame with her installation Cardoso Flea Circus, an artistic interpretation of the nineteenth-century circus sideshow performance.

  While researching for the flea circus, she came across a startling reference to the complexity and size of their genitalia. When the flea circus project was over, she decided to find out “if fleas were the only well-endowed arthropods or whether there were more.” Now based in Sydney, Australia, Cardoso spent a summer in the library of the Australian Museum, soon hitting upon Bill Eberhard’s book Sexual Selection and Animal Genitalia and realizing how much potential there was for this project. Collaborating with entomologists, 3-D modelers, and electron microscopists, she has since produced series of glass renderings of pseudoscorpion spermatophores, damselfly penises in bronze, and large-scale blowups of snail genitals.

  Most evocative are her representations of the penises of nine species of harvestmen from Tasmania. Starting from electron micrographs, Cardoso first had these fantastic shapes transformed into three-dimensional computer models and then printed in white plastic with a 3-D printer. Finally, she placed them under tight-fitting bell jars. As Elizabeth Ann Macgregor, director of the Museum of Contemporary Art Australia, said in a TV documentary on Cardoso’s work: “You see these shapes, and of course you immediately think of a penis, because she’s put them under these glass structures, which could be condoms. So immediately the references start. And then you begin to look closer. They’re extraordinarily beautiful—they become like flowers.”

  Hand in Glove

  Of course, the pressing question that this genital burlesque impels is, Why? Why would different species have completely different shapes for organs that perform the same simple function in all of them? Different species eat different food, so having different sets of teeth, as Cuvier emphasized, makes sense. But different penises and vaginas? For a long time, biologists smugly leaned back in their chairs, claiming they knew exactly what all this genital diversity meant. Even before Jeannel, deep in the nineteenth century, the naturalist Philip Henry Gosse already wrote about this: “If I see a number of keys, of very minute and elaborate workmanship, all different, I cannot doubt that every one is intended to fit some special lock.”

  The idea is that each species is provided with its own unique penis and vagina combination to assure that only members of the same species can copulate successfully. At the same time, crossbreeding with other species is barred (either because there is no fit or because it “doesn’t feel right”)—hence the aptly named “lock-and-key” hypothesis. Intuitive and aesthetically pleasing, the idea makes perfect sense. To begin with, hybridization between different species, when it happens, often leads to offspring that are sterile (think of mules), sickly, or poorly adapted, so it stands to reason that evolution would make sure that such poor bastards were prevented from being born. Furthermore, wasting time and, worse even, sperm and eggs on mates belonging to the wrong species could be prevented by a system of keys that don’t fit into other species’ locks. And finally, nature is full of situations in which there is a real risk of such sexual mistakes; closely related species often share the same habitat.

  A little foray into necrophagy illustrates this last point. If, like ecologist Petr Kočárek did, you were to take a close look (hold your nose!) at the beetles living on carrion in a Czech forest, you’d find that closely related cadaver-feeding species are rubbing shoulders with one another. Kočárek found up to eleven species of Catops beetles living together on the same piece of rotting meat, up to nine species of the rove beetle Atheta, and five different Nicrophorus burying beetles. All these beetles are, at least to the human eye, very similar. Those Catops species, for example, are all about 3 millimeters (0.1 inch) long, gray, and oval, with pretty much identical legs, antennae, and body proportions. But each species has its own unique penis shape: Catops tristis: lance-shaped. C. nigrita: three-pronged. C. morio: gouge-like. C. westi: forked. C. chrysomeloides: spoon-shaped. It is not hard to imagine why a check for mutual fit of lock and key might be an efficient safeguard against accidentally having it off with the wrong species.

  And as further support for the idea, biologists discovered that male and female genitalia of the same species indeed do mesh perfectly. In the May 27, 1967, issue of Nature, primatologist Jack Fooden of the Field Museum of Natural History in Chicago provided such an example for two monkeys from southern China: the rhesus macaque (Macaca mulatta) and the stump-tailed macaque (Macaca arctoides). The rhesus macaque has a human-like vagina and a blunt, helmet-shaped glans penis. The stump-tailed macaque, on the other hand, has its glans extended into a long, flat, lance-shaped structure of up to 7 centimeters (3 inches) long, supported by a bone inside. At the same time, the vagina of the female of the same species is almost completely obstructed by a thick lump of tissue hanging from the roof. As Fooden writes, the slender penis “is ideally formed for reaching and entering the vaginal opening of the female by passing through the narrow slit. . . . [C]onversely, it appears unlikely that this passage would transmit the short blunt glans penis of Macaca mulatta.” In other words, it would be like the proverbially doomed square peg in a round hole.

  With so much going for it, it’s little wonder that the lock-and-key hypothesis survived for more than a century without anybody seriously questioning it. Another reason may be that, until a few decades ago, the biologists most interested in genitalia were taxonomists, quietly organizing and dissecting, drawing and describing their specimens, and not particularly keen on rigorous tests and experiments. Yet dark clouds did appear on the horizon now and then. Already in the 1920s biologists working on bumblebees (then still called by the slightly more endearing “humblebees”) realized that the multiformity of male “keys” (already showcased above) was answered with just a single “lock” in the females. Despite attempts to find differences, bumblebee researchers had to conclude that the vaginas of these winged balls of fluff all have the same internal shape. More worryingly still, with alarming regularity reports appeared of males of one species of insect found with their keys firmly and cheerfully inserted in other species’ female locks. A butterfly collector in Rotterdam once showed me his drawer full of what he called “flagrante delicto cases”: pinned female butterflies, the male of another species still hanging by its genitals from hers.

  But it was not u
ntil the 1980s, when evolutionary biologists began to pay more than cursory attention to genitalia, that the theory found itself in stormy weather, and it has since then been slowly sinking to the bottom of the scientific sea. So how did such a simple and attractive idea that was quite popular for more than a hundred years all of a sudden fall out of favor? First of all, when you think about it (as some clever people started doing), the theory does not make as much sense as it seems to at first sight: if the prevention of miscegenation had indeed been the evolutionary drive, then wouldn’t placing the crucial barriers at the very end of the sequence of preliminaries be a bit inefficient?

  There was more. I already mentioned that, very early on, researchers found that the differently shaped penises in bumblebee males seem not to be matched by differences in the female vaginas; hence, the whole lock-and-key idea fails in these animals. In fact, with few exceptions, genital differences between species sit in the male parts, and much less in the female ones.

  In a brief aside, I should stress that the apparent absence of female “locks” may be an illusion caused by an issue that will be a recurrent theme in these pages: the worrying ignorance of the ins and outs of female genitalia compared with the well-studied male ones. Zoology has not been spared the same male chauvinism that has made the study of the human male sexual apparatus deemed more acceptable and relevant than parallel studies in females. There is also a practical bias: male genitalia are often sturdy, sticking out, and anatomists find them much easier to access than the soft, folded, invaginated ones of females, especially when we are talking about dried and pinned millimeter-sized insects. Both the sociology of science and the realities of preservation and dissection, therefore, seem to have conspired in our ignorance of female genitalia. So in many animal groups where the female genitalia are said to be “all the same,” this should be interpreted as “nobody has really bothered to look.” We will come back to this at length, also in reference to human genitals.

  With this caveat in mind, even in types of animals where scientists have taken the trouble to dissect and measure the female genitalia with as much abandon as the male ones, the general trend points to genital extravagance more in males than in females. At the same time, reports keep popping up of females unable to keep their fertilization apparatus locked to “wrong” males.

  One particularly telling example of this last problem comes from Ciulfina praying mantids. These small (as mantises go), handsome insects live in forests in Australia’s northeast and are genitally quite special in that some species have male genitals that are the mirror image of those of other species. You’ll have to imagine that the penis of a praying mantis is always a very asymmetric affair. Seen from the rear, it is a twisted arrangement of plates, spokes, and prongs. And as with all asymmetric forms, its mirror image cannot be superimposed on the original. This is called chirality, after the Greek cheir, meaning “hand”: our hands are perfect examples of chiral forms, with your left hand identical and yet completely different in form from your right. (We will come back to chiral genitalia in Chapter 8.) So some Ciulfina species have, let’s say, “right-handed” male genitals whereas others have “left-handed” ones. However, says Greg Holwell of the University of Auckland in New Zealand, who studies these critters, the female genitalia are all symmetric. The result is, as Holwell found out when he mated females of left-handed species with right-handed males and vice versa, that females’ locks can be opened by their own males’ set of keys just as easily as by a set of mirror-image keys. Try that with a real lock, and you’ll understand that this is not something that jibes with a lock-and-key idea.

  Still, this argumentation—the absence of female locks—could be seen as only circumstantial evidence against the lock-and-key hypothesis. After all, it is possible that genitalia do not work like a traditional lock and key but rather like one of those modern electronic key cards: no mechanical mesh but an imperceptible exchange of sensory signals, something that need not be visible in the female genitals’ shapes.

  No, the more damning verdict against the genital locksmith came in the third chapter of Bill Eberhard’s Sexual Selection and Animal Genitalia. Rather than looking for proof (or the lack thereof) of a tight fit—either mechanical or sensory—between male and female genitals, his approach was, let’s look for situations where we would not expect the lock-and-key system to evolve. What do we see there? Such situations would be species that simply never run the risk of encountering an amorous member of a closely related species, and therefore would have no use for any specialized locks or keys. The leptodirin cave beetles that Jeannel studied, for example. Each cave has its own species of beetle that never ventures outside of it, and hence never, ever meets any members of the related species in the neighboring cave. Or think of island archipelagos, where each island often has its own endemic species that lives only there and nowhere else, to be replaced by a related, but different, species on the next island. And then there are parasites, which live and mate only on or in a particular host; to them, their host is their island, and they never meet the closely related brethren that are specialized on other hosts.

  Eberhard trawled the scientific literature and came up with dozens of such cases: the Oryzomys mice of the Galápagos Islands, the checkerspot Atlantea butterflies of the West Indies, Meropathus water beetles of the sub-Atlantic islands, and also the lice that live in pocket gophers’ fur, the feather lice of crows, the pinworms in the intestines of humans and other primates . . . all groups of multiple species each inhabiting its own “island” and never meeting another species of the same group. And yet, all showed genital differences between species just as great as between species that do actually run a risk of mating with the wrong species. In the light of the lock-and-key hypothesis, this does not make sense. It would be as silly as the castaway sailor on an uninhabited island who locks and bolts his hut whenever he goes coconut collecting.

  Since Eberhard’s book, such evidence against the lock-and-key hypothesis has been accumulating. By now, it seems an open-and-shut case. Clearly, as we will see in the next chapter, we must look for other explanations for the genital extravagance that appears to be commonplace in nature. Still, I have to leave you with a paradoxical truth: the demise of the lock-and-key theory does not mean that there are no animals that are barred from mating with related species because of nonmatching genitals. We already hinted at this with the rhesus and stump-tailed macaques, but there are more.

  A good example of a true lock-and-key situation was published in 2012 by evolutionary biologists Yoshitaka Kamimura and Hiroyuki Mitsumoto of Keio University in Japan. They studied Drosophila santomea and D. yakuba, two species of banana fly from the small African volcanic island of São Tomé. Males of the species D. yakuba carry two sharp spines on the base of the penis, which during copulation fit exactly in two reinforced pockets on the female’s vagina. The other species, D. santomea, lacks both these spines, as well as the pockets. As a result, a mating between a male D. yakuba and a female D. santomea is no fun for either party: the female, lacking any protective armor on her vagina, is wounded by the spines on the male’s penis. He, conversely, is not happy either, because the spine/pocket mismatch causes his penis to be misaligned, with the result that, when he ejaculates, his sperm does not enter the female’s vagina, but instead is spilled on her behind. The physics at that spatial scale being what it is, the drop of semen dries instantly, gluing the pair (whose enthusiasm for each other was already rapidly dropping) firmly to each other. This then leads to a half-hour struggle during which male and female kick each other vigorously until they finally break loose.

  Other such cases of lock-and-key mismatch in the genitals do exist. Still, these are not to be taken as evidence for the lock-and-key hypothesis. The point is, in none of these cases is it likely that avoiding crossbreeding was the cause for lock-and-key-like pairs of genitals to evolve. More likely, the inability to mate with other species was simply an unfortunate side effect
of genital shape differences evolved for very different reasons. And those reasons are—as we shall see in the next chapter—much more titillating than locks and keys.

  Chapter 3

  An Internal Courtship Device

  In a small room in the attic of my home I have created my own explorer’s den. Nestled among the roof beams is a jumble of wooden and rattan furniture, a shelf with shells, giant rainforest seeds, and other souvenirs from my field trips, and the obligatory stuffed caiman suspended from the ceiling. I also have some Indonesian teak bookcases crammed with natural history field guides. Sitting at my Burmese secretaire, I flip through two of these tomes that I have just pulled off the shelf. The first is A Field Guide to the Birds of West Malaysia and Singapore by Allen Jeyarajasingam. It once got soaked in a tropical thunderstorm, so some of the magnificent plates by artist Alan Pearson stick together, but fortunately Plate 63 is still in pristine condition. It depicts twelve species of flycatchers, all crisply drawn as pairs of a colorful male flanked by a drab female. The males are easy to identify: each species (sparrow-sized, with a short, strong beak planted in a tuft of springy bristles) has its own unique plumage combination of air force blue, amber, off-white, and sooty black. Most of the females, on the other hand, are a nondescript shade of brown. The second book lying open on my desk is an atlas to the grasshoppers and crickets of the Netherlands. Though the males of many European grasshoppers look quite similar, they sing very different songs to attract females; pages 113 to 115 carry a key to the orthopteran hit parade and tucked in the back of the book is a CD with which the grasshopper enthusiast can learn to recognize species by ear.