Nature's Nether Regions

by Menno Schilthuizen

  We now know much more about onychophorans. We know that they are a separate phylum of animals, equal in rank to the arthropods, and indeed closely related to them (but not to the annelids). We know that there are hundreds of species living in damp places all over the Tropics and the Southern Hemisphere, where they (sometimes in family groups) hunt termites and other prey, which they catch with a sticky substance squirted from nozzles under their mouths. We know that they have a surprising variety of ways of reproducing—some indeed have extended pregnancies after which they give birth to live young, but others lay eggs. And despite their rarity and elusiveness, they have become somewhat of an icon, due to a nonscientific characteristic known as “cuteness.” A commenter to one of the many velvet worm videos on YouTube likened them to “centipedes in romper suits.” Quite.

  But adorability aside, they figure in this chapter for the ways in which males transfer sperm to females. As noted by Adam Sedgwick, who brought three hundred live onychophorans from the Cape to Cambridge and studied them there, “the males deposit spermatofors quite casually all over the body of the female.” He added: “How the spermatozoa pass up the uterus and oviducts, which are always full of embryos . . . I do not know.” In the nearly 130 years that have passed, we have learned a great deal more about onychophoran sex. And it is weirder than Sedgwick could have dreamed.

  Although some velvet worms have orthodox vaginal sex, males in the family Peripatopsidae, to which Sedgwick’s species belonged, produce spermatophores that they, not unlike squid, affix to the female’s skin. Sedgwick was rightly puzzled by how the sperm then reach the eggs, given that they would first need to find their way to the vagina and then struggle through a uterus cluttered with developing embryos. The fact is that they don’t. Instead, the female helps them create a rather drastic shortcut. At the site where the sperm package sticks to her skin, she releases enzymes that dissolve her own skin as well as the spermatophore envelope, which allows the lump of sperm to sink into her body. The sperm cells then begin swimming through the female’s blood. They reach her sperm storage organs either via helpful funnel-like structures or by forcing themselves straight through the wall of these organs.

  But it gets stranger still. In the 1980s, velvet worm specialist Noel Tait of Macquarie University in Sydney discovered a whole menagerie of unknown species, all belonging to entirely new genera, in the forests of New South Wales and Queensland, of which the males all carried curious “head structures” between their antennae. These ranged from flower-like arrangements of bumps to single or multiple erectable teeth and spikes. Only in 1994 did it become clear what the males use these for. On April 27 of that year, Tait found a mating pair of the species Florelliceps stutchburyae in leaf litter in the Nightcap Range, a mountainous area some 130 kilometers south of Brisbane. As Tait described it in the Journal of Zoology, “The male’s head was firmly attached to the genital region between the last pair of [legs] of the female. The two individuals moved about in a coordinated fashion with the female leading.” When he took a closer look at the couple under the microscope, he saw what was happening: the male had a spermatophore stuck on the prong on its head, which he was delivering into the female’s vagina. The female, meanwhile, had her hind claws locked tightly into the skin around his head structure, as if to keep him in position.

  For these male velvet worms, it seems, the crowns on their heads are their genitalia. These are the tools they use to move sperm into the female’s vagina. A further twist came in 2006, when Tait and his collaborators announced that they had found that females of several head-structure species still possess working machinery for transporting sperm from their skin to their eggs via the blood. So Tait now thinks that perhaps the headfirst mating behavior is applied only on virgin females, which still have a vacant uterus, not clogged by developing embryos, whereas mature females, with developing embryos in place, mate with the old through-the-skin method. Whether the males also use their head structure to fix spermatophores on the female’s outside remains to be discovered. Either way, it is clear that velvet worms give a whole new meaning to the term “genitalia.”

  Genitalia on your head. The male Australian velvet worm Florelliceps stutchburyae mates by placing sperm on a crown-like adornment of his head and then pushing his head into the female’s vagina.

  At the end of this first chapter, we are left with the sobering thought that in sex, all our certainties should be reconsidered. Even if the immediate reason for a male and a female to have sex may be attraction, hormones, and the innate urge to procreate, the ultimate cause is an unlikely sequence of evolutionary events involving genetic variation to evade parasites, peacekeeping among warring organelles, and the hostile environment out of the sea. The tools they use to accomplish all this, the organs subsumed under the term “genitalia,” even if we adhere strictly to Eberhard’s definitions, can be anything from a penis to a zombie tentacle and from a vulva to an upper lip.

  Yet it is precisely those genitalia that evolution seems to have singled out to display its greatest virtuosity. Next we will see that taxonomists, not evolutionary biologists, were the ones with front-row seats to this evolution tour de force.

  Chapter 2

  Darwin’s Peep Show

  I have now traversed the dusty paths crisscrossing the Jardin des Plantes and the buildings of the Muséum National d’Histoire Naturelle. I have leafed through Les Statues du Jardin des Plantes in the museum bookshop and scanned the numbered, colored dots on the plans at the entrance of the famous Parisian park. Arrows point to the grandiose statues of the great French naturalists Lamarck and Buffon, and the book provides directions to at least twenty-five other busts in the gardens. But the one I am after, of entomologist René Jeannel, remains elusive.

  For the third time, I cross rue Buffon and wander among the haphazardly placed nineteenth- and early twentieth-century buildings, in various states of disrepair, that form the small village of zoological and geological laboratories of the museum. The security guard, in his cabin at the main gate, who has already been ogling me suspiciously, says he has no recollection of a statue anywhere nearby. But then a second security guard who ambles in overhears my question and relieves my two-hour-long foray with the words: “Ah, a statue? Yes, there is a statue at the end of this cul-de-sac, in the corner, behind that blue truck!”

  Indeed there is. The truck obscures from view an ill-tended corner of the grounds of the entomology department, where building rubble, a garden shed, and parked cars vie for space. Among them, barely rising above weeds and saplings, and with several wooden pallets propped up against it, stands the bust of a solemn mustachioed gentleman, a gift from the Romanian government on the passing of Dr. René Jeannel (1879–1965), “for his magnificent oeuvre in entomology, biospeleology, zoogeography, and evolution.”

  Judging from photographs, Jeannel in real life looked more kindly and well coiffed than the wild-eyed, ominous effigy that the Romanian artist, probably steeped in socialist realism and portraying revolutionary heroes, had produced. Notwithstanding representational inaccuracies, the bust and its subject deserve more exposure than they get in their forgotten corner of the Paris museum grounds. For Jeannel, who was indeed a great entomologist, was also one of the founding fathers of the study of genitalia.

  The son of a medical officer in the French army, Jeannel was destined to follow in his father’s footsteps. But his medical career had already been nipped in the bud when, during his studies in Toulouse, at the foot of the Pyrenees, Jeannel took up caving and began exploring the many limestone caves in the south of France. Initially as a hobby but soon more and more seriously, he studied the bizarre life-forms adapted to the dark, damp, cool, and nutrient-poor conditions deep inside those ancient caves. During those excursions, Jeannel discovered two unknown cave beetles in the Grotte d’Oxibar, which an entomological authority published for him and named Bathyscia Jeanneli and Aphaenops Jeanneli. By then, any residual medical asp
irations were doomed, much to his father’s regret: René was going to be a full-time naturalist.

  In 1905 Jeannel teamed up with another young spelunker, the Romanian biologist Émile Racovitza, and together they embarked on a lifelong collaboration in biospeleology: the study of the evolution of “troglobites,” those bizarre organisms that have adapted to the demands of cave life and can no longer survive aboveground. The two must have almost grown into troglodytes themselves, spending more time in those underground echoing vaults than in the human world, for in the first seventeen years of their collaboration alone they jointly explored a staggering fourteen hundred caves in southern Europe and North Africa. They published descriptions of the caves and the animals living there, and in passing discovered some of the finest examples of Paleolithic cave art. Later, when Racovitza was invited by the government of his home country to found a biospeleological institute in Cluj, Jeannel joined him there as deputy director (hence the Romanian statue) until he landed a job at the Paris museum in 1927, accepting a chair in entomology and eventually becoming the museum’s director.

  Despite these managerial posts, Jeannel was primarily a hardworking taxonomist who would closet himself into his office for days on end whenever he was working on a problem. By 1911, which saw the appearance of his 641-page, 657-illustration doctoral thesis on a band of cave beetles called Leptodirini, he had already published more than thirty papers. And during the rest of his working life he added another five hundred scientific publications to this total, together amounting to more than twenty thousand published pages, mostly on cave insects and all illustrated by his own deft hand.

  The cave beetles that Jeannel studied are very old: derived from an aboveground ancestor that must have lived in the Mediterranean tens of millions of years ago, they colonized the many isolated caverns as these were gouged out by groundwater and subterranean rivers, and have had ample time to adapt to the unique cave environments. Pale, with long, spindly legs and ditto antennae that make up for the loss of eyes and wings, as well as bloated abdomens that house extended guts for extracting all the nutrients they can from what little food enters the caves, they all pretty much look alike. And yet, as Jeannel and his colleagues discovered, there are thousands of different species, many of which occur only in a single cave system, evolved in isolation from relatives living in the cave system next door. With their external appearance so constrained by the requirements of their environment, the fact that these are all different species is not nearly as apparent in their outward form as it is in their internal organs—in their genitalia, to be precise.

  Like many beetles, a leptodirin cave beetle has a penis with, on either side, a whip-like “paramere” with a couple of bristles at the end. The penis itself is hollow and contains a soft, crumpled-up sac that, during mating, is blown up and extrudes via two flaps at the bottom. When fully inflated, the internal sac turns out not to be as soft as it appeared at first: it is studded with rows of tough teeth, larger spines, and sometimes a few extremely long and sharp spikes. Jeannel did not (as we will do in Chapter 7) stop to wonder about the function of this entire rather vicious-looking contraption. Instead, for each species of leptodirin, he meticulously described the shapes of the parameres and the arrangements of the bristles at their top, the shape and curvature of the penis, and especially the exact way the internal sac was adorned with rows of variously sized and shaped spines. In so doing, he revealed that hundreds of variations on this theme exist, corresponding to just as many different species. Not only that, he also discovered that the way the male genitalia are constructed holds the key to species’ classification, and he was the first to group species into families based on how their penis looked.

  The beetle penis became Jeannel’s bread and butter. Aware of its potential, he invariably assigned projects to his students that involved dissecting, describing, and categorizing the penises of beetles and other insects, and was puzzled when, in one case, this brought a female student to tears. She told him that he could not possibly expect such a thing of a lady. In what must have been an effort of empathy, Jeannel defused the situation by pointing out that he was not actually asking her to study penises; instead he preferred to use the word “aedeagus” (from the Greek ta aidoia, “the genitals”), since “penis,” “phallus,” and “prepuce” are terms usually reserved for vertebrates like ourselves.

  A Plethora of Parts

  In the early twentieth century, recognizing and identifying animal species by their aedeagus was still something of a novelty among taxonomists, and Jeannel was certainly a trendsetter in his time. Where one of Jeannel’s predecessors, the vertebrate paleontologist Cuvier, had as his adage “Show me your teeth and I will tell you who you are,” Jeannel’s might well have been “Show me your willy. . . .” Toward the end of his career, in 1955, he devoted his entire 155-page memoir L’Édéage (the Frenchified version of the word) to the insights the aedeagus had given him. Today, however, biologists routinely use male and female genitalia as a quick and easy way of distinguishing species that often are very similar otherwise. Or ones that are so variable in color or size that the shape of the reproductive organs is the only reliable indicator of a species.

  Bumblebees are a good example. Watching the large, furry insects in their jolly colorful outfits heave themselves from flower to flower, you might think that, insect field guide in hand, one could easily determine the name of a species by a quick scan of its conspicuous black, yellow, and red pattern. Unfortunately, the reality is more frustrating. In Kashmir, for example, some thirty species of the genus Bombus exist, each of which seems to own roughly the same wardrobe of woolly black with variable yellow, orange, and red cross-band patterns. As a result, the color of a cashmere bumblebee says near to nothing about its identity. Experts who are in the know can discern the subtle species-specific differences in the shape of the jaws and the antennae, and in the pattern of pits and wrinkles on the surface of the head. Still, the only fail-safe way of identifying many of these species is to get your hands on a drone, extract his penis, and compare its shape with pictures of the characteristically shaped penises of all thirty species. And it’s the same with the twenty-four species that occur in Britain, or the thirty-five or so North American bumblebees.

  I hope that with these entomological examples, I have not given you the impression that this genital pinnacle of biodiversity is something specific to tiny creepy-crawlies. In fact, the pattern is pervasive throughout the whole animal kingdom, right up to and including mammals. Take, for example, the eighteen species of elephant shrews. These insect-eating animals, which live in all kinds of habitats across the African continent, range from mouse-sized to opossum-sized. Apart from their somewhat long legs, their extended noses, and their sometimes colorful or checkered fur, elephant shrews resemble true shrews, with which they were classified in the past. DNA studies, however, have revealed that elephant shrews are actually members of the Afrotheria, an ancient group of predominantly African mammals that also includes aardvarks, elephants, manatees, tenrecs, and hyraxes, among others.

  In addition to the funny trunk-like nozzle that their noses have evolved into, elephant shrews have peculiar genitalia. Females lack a vagina as such (instead, the womb opens directly to the outside world) and are, besides primates and bats, the only mammals that menstruate. And the males have their testicles as well as most of their penis hidden inside their bellies. The elephant shrew penis is unusual in other ways, too. It is extremely long—about half the animal’s body length—running along the inner wall of the belly all the way from his hindquarters until near the breastbone. There it makes a sharp U-turn and emerges from the belly pointing downward and backward—although in erection, muscles in the skin direct it forward again, so that the shaft of the penis becomes, when seen from the side, Z-shaped.

  Show me your willy. Animal species that are near identical externally often have very different genitalia. In this picture, five—very similar-looking�
�Catops beetle species are shown, together with their respective—very different—penises. In life, the penises are hidden in their abdomens and not visible on the outside.

  If we were to follow an elephant shrew’s penis from its base to where it emerges from his furry belly, we would see that all elephant shrews follow the same basic design. But it is when we reach the tip of the penis that all hell breaks loose. Peter Woodall, whose in-depth study of the elephant shrew’s penis tip (don’t laugh) appeared in the November 1995 issue of the Journal of Zoology, explains that the golden-rumped elephant shrew, from Kenya, has a row of spines on the tip, which ends spoon-shaped; the Southeast African four-toed elephant shrew has a sharp tip with two sideways-pointing “ears,” like a medieval ranseur; and the South African short-eared elephant shrew has a collar near the end and a puffed-up tip; whereas all species that belong to the genus Elephantulus have a nub at the end of the penis tip that can be heart-, dish-, boomerang-, or flower-shaped, depending on the species.

  I could go on like this, but I won’t—at least not yet. You will have to take my word for it that we find this pattern in almost any kind of animal we turn to—to such an extent that it is almost a law of nature: of all the organs that an animal is provided with, the greatest differences between species are not in their brains or beaks, or in their kidneys or guts, but in their genitals. This applies to cave beetles, bumblebees, and elephant shrews, as well as to velvet worms, land slugs, water and rove beetles, small ermine moths, daddy longlegs spiders, banana and hover flies, egg parasitoid wasps, aquatic annelid worms, hoofed mammals, sharks and rays, primates, guppy fish, damselflies, land planarians, nematode worms, trombidiform mites, and harvestmen. To name but a few.