Nature's Nether Regions

by Menno Schilthuizen

  In the bird world, such marriage of love and convenience is also commonplace. Peachicks fathered by the most attractive males with the longest trains grow faster and survive better, while barn swallow males with the longest tail feathers possess the best genetic tools to fight off infection. But we can’t assume all male ornaments that win over females signify good health and long life. Some sexual selection by female choice is just about being irresistible, as we shall see shortly.

  Feathers and Phalluses

  If anyone knows the value of serendipity, it must be behavioral biologist Nancy Burley of the University of California, Irvine, who can trace much of her career to a botched experiment back in the late 1970s. At the time, Burley, then a young postdoc at the University of Illinois, Urbana, was researching breeding behavior in Australian zebra finches. These birds nest communally, so to be able to recognize individual birds in the large aviary she was going to house them in, she fitted each of her forty experimental birds with a unique combination of seven colored rings on their legs. Then something unexpected happened: five months into her project, some males still had not paired off, and those were invariably the ones without any red or pink bands on their legs. When she took some of those frustrated bachelors and added two red bands to their already overloaded legs, they instantly paired off (and as soon as they became aware of their increased desirability, they began philandering and generally behaving as if they were God’s gift to female zebra finches). Clearly, the plastic rings on males’ legs could boost or break the males’ sex appeal: red and pink rings, and the females would be flocking to them; green and blue, and they would turn away in disgust.

  Now, a lesser researcher might have cursed such an unexpected turn of events, rounded up her finches, and started all over again with neutral-colored bands—after all, an experimenter should not be influencing the behavior of her study subjects. Not so Nancy Burley. She realized that she was actually on to something very interesting. After all, zebra finches normally don’t have brightly colored legs, so the females in her aviary were choosing their mates based on an aesthetic preference that they normally never got to exercise. Intrigued, Burley began experimenting with other artificial ornaments for her male finches. She dyed loose feathers to produce white, red, or green crests, which were then fixed upright on top of the males’ heads with a crown of beads and a generous dollop of glue. And even though crests do not naturally occur in zebra finches or in any of their relatives, the new headgear once again had females swooning—but, as if to underline the whimsicality of “a woman’s reason,” only the white version: the red and green ones left them cold.

  A woman’s reason. Female zebra finches swoon over males with white-crested crowns—even when those crests were glued on by a researcher.

  The surprising finch aesthetics that Burley unveiled are grist to the mill of a version of sexual selection theory known as sensory drive. The idea is that, obviously, animals must choose their sex partners on the basis of what they can gauge of them with their senses. In every species, the working range and resolution of those senses have been optimized for the species’ habitat and way of life, albeit limited by what is “technically” possible in the species in question. Take vision. The zebra finches of Nancy Burley munch seeds and fruit and have multicolor vision to find and distinguish these in the surrounding foliage. Their retinas carry four different kinds of color pigments, with high sensitivities in ultraviolet, blue, green, and red. These sit in cone cells, each of which is wired via neurons to the zebra finch brain. Rather than such four-channel vision, humans have only three color pigments (for blue, green, and red), most monkeys two, and the owl monkey eye can create only monochromatic images; mantis shrimp, on the other hand, have at least seven, including three ultraviolet ones. Other animals forgo vision entirely and instead live in a world of sound or scent, hearing, touch, or more exotic senses, like the platypus’s electroreception.

  In other words, we can view a female animal (for this particular purpose) as a central processing unit with a complex series of input channels. Each of those input channels has different sensitivities, and stimulation within those sensitive ranges will result in a physiological response. One of the peak sensitivities of the zebra finch eye, for example, is an orangey kind of red, so a male with an ornament (either real or artificial) of the right sort of red will stimulate the neurons in her eye, whether she likes it or not. Or rather, sensory drive adepts would argue that stimulation equals liking. Whatever a male can produce during courtship that strikes her eye, caresses her ear, or just generally dazzles her senses will be registered, noted, and, by default, liked.

  It is at this point that the phallus lumbers onto the scene. Bill Eberhard’s revolutionary idea was that the main role of the penis on the stage of reproduction is not just sperm transfer (that, too), but rather courtship, played out in a theater of sensory drive. Females, Eberhard claimed, employ their senses to exert their preferences over the available phalluses just as they do for other available male ornaments. Occasionally, females do this on sight. In 2013, Brian Mautz and his colleagues used animation software to project life-sized computer-generated nude men on a screen and asked women to rate their attractiveness. These volunteers clearly turned out to have a preference for virtual male models with large penises, especially in combination with tallness or masculine hip-to-shoulder proportions. And in some other vertebrate animals like lizards, mosquito fish, and primates, males actually show off their penises for the femalefolk. For example, in a 1963 paper in Animal Behaviour, researchers Detlev Ploog and Paul MacLean described “display of penile erection” in squirrel monkeys this way: “[A] male approaches a female or another male head on, places one or both hands on its back and thrusts the erect penis towards the face. In doing so it ‘thigh-spreads’ [and] the gaze is directed away from the recipient.” (And they illustrate the behavior with a touching little pen drawing.)

  Primate exhibitionism aside, the evolution of male genitalia through sensory drive mostly proceeds via the female’s tactile senses, thinks Eberhard. And his reasons are quite persuasive. To begin with, there’s the penis’s complexity. We have already seen that the organ possesses all kinds of bits and pieces that seem unnecessary for the mere task of squirting sperm into a female. In fact, if that were really its sole function, says Eberhard, then the penis of many an animal would be akin to a Rube Goldberg machine. (The hilarious inventions of cartoonist Rube Goldberg are composed of immense series of interconnected parts to perform an incredibly simple function—like the nineteen-part pencil sharpener comprising, among other components, a kite, an old shoe, and a live woodpecker.) But nature has no sense of humor, so the constituents of the penis must serve some more meaningful goal. And, simply put, that goal seems to be to tickle the female in as many ways as possible. To begin with a rather convincing example, published by Eberhard himself in 2009: a crane fly with a vibrator on its penis.

  On a cool December morning in 2006, Eberhard, who, next to his position at the Smithsonian Tropical Research Institute in Panama, also works at the University of Costa Rica, found a pair of crane flies (probably a new species of the subgenus Bellardina) having it off on the wall of a house in San Antonio de Escazú. As is usual in these insects, the male was dangling underneath the female. Always eager to expand his catalog of animal intercourse, Eberhard coaxed the female onto a twig and rushed the pair to the lab, where he placed them under a microscope and videotaped the whole affair—not anticipating the surprise they had in store for him. In the November 2009 issue of the International Journal of Tropical Biology, he and crane fly specialist Jon Gelhaus tell their story of sex, flies, and videotape.

  To begin with, the meshing of the pair’s genitalia was rather complex. The male crane fly’s aedeagus (to use Jeannel’s term) is a tightly packed bunch of tubes and plates. Several of these form a cylinder through which, during mating, two appendages of the female’s abdomen, so-called cerci, are inserted. Thus configu
red, the pair that Eberhard had arrested first remained motionless for the better part of fifteen minutes. Then, suddenly, a subtle, repetitive movement began to take place, which, under the microscope, revealed itself as the first confirmed case of “copulatory stridulation” by a male’s genitalia. On the outside of the aedeagus, the male carries a pair of hairy, claw-like things called outer gonostyli. These it moved rhythmically to and fro along the outside of that cylindrical part of his aedeagus encasing the female’s cerci. On closer inspection, the part of the cylinder that the claw scraped across turned out to be covered in small, parallel ridges, perpendicular to the direction of stroking. In other words: a miniature washboard, scraped, in repeated two-second bursts fifteen to thirty times per second, to produce a vibration with a pitch slightly below middle C. The female, her cerci firmly gripped in the washboard itself, must have felt this hum reverberate through her entire genital region.

  This is probably not an isolated case. Many other species of crane flies, as Eberhard and Gelhaus discovered, have such a file-and-scraper system on the male genitals. Sometimes the file has the same frottoir-like appearance as in the male that Eberhard filmed. In other species, the ridges are replaced by bumps or puckers, probably producing a whole different sensation. And similar devices are found on the male genitals of several families of moths. For some of these, it was already known that the males use them to sing at an ultrasonic pitch to communicate with females from a distance (the sensory drive here being that moths possess ears that can detect the ultrasonic clicks of the bats that chase them). But Eberhard was the first to actually see genital stridulation during mating. In fact, after he separated the couple and “collected them” (the entomologist’s euphemism for dunking an insect in a vial of alcohol), he noted drily, “The male outer gonostyli continued to execute the scraping movements in slow motion as the male expired.”

  And the vibrator-penis of the crane fly is just one highlight of the animal world’s multipage sex-aid catalog. Remember parameres? Those whip-like or drumstick-like appendages of many a beetle penis that Jeannel used to classify his cave beetles? Well, whip and drum is exactly what they do. The penises of beetles, flies, butterflies, moths, and many other insects often carry such accessories (although they are called by different names in different types of insects), and they are used to drum, tap, slap, or stroke the outside of a female’s genital region during sex while the rest of the aedeagus is working on her inside. Susanne Düngelhoef of the University of Bonn in Germany studied the use of parameres in leaf beetles and noted that during mating a female often would reposition a male’s parameres with one of her hind legs. Not forcefully, as if to kick him away, but more gently (“More to the left—yes, that’s it”). The parameres are particularly large and flat in some ladybird beetles, such as the common American spotless ladybird Cycloneda sanguinea. By inspecting a mating pair up close it is possible to see the hairy parameres literally slap the female’s genitals like two miniature Ping-Pong paddles. As all this happens out of view of the female, sensory drive adepts think that it is the triggering of nerve endings in her hindquarters that makes the female pay attention to what the male is “telling” her.

  A crane fly with a singing penis. During mating, the female’s nether regions are stuck through a sleeve on the male’s genitals. These have a washboard-like contraption that produces a vibration with a pitch just below middle C.

  Now, you could argue that since the crane fly vibrator and ladybird parameres stay outside of the female, they don’t really qualify as what Eberhard calls “internal courtship devices.” But parts of the male genitalia that are inserted deep into the female also seem to have a job to titillate her. For example, the penises of many insects but also some mammals have a whip-like extension at the tip. In hoofed mammals, for instance, the urethra leaves the penis on the left-hand side and continues inside a thin, worm-shaped appendage (in rams, this appendage adds another 4 centimeters—1.5 inch—to the length of the penis). In bulls, it has been seen that this so-called urethral process flips forward inside the female upon ejaculation, probably triggering some kind of sensation in the cow. And then there are all the other outlandish adornments such as spines and knobs on the penises of snakes, monkeys, and cats, and multiple sideways-pointing flanges on the rhinoceros phallus (which the men of some indigenous peoples of Borneo emulate by piercing their own penises with a crosswise metal rod, the so-called palang). Not to forget the seemingly rigid but apparently flexible plates of wasp penises, which Eberhard’s wife, the famed entomologist and evolutionary biologist Mary Jane West-Eberhard, has described as capable of “the most fluid and subtly modulated movements I have ever observed in wasps.”

  Speaking of movements: the genital thrusting that to us seems almost synonymous with copulation itself speaks in favor of Eberhard’s hypothesis. After all, familiar as the old in-out may seem, there is no obvious reason why genitals should be moved rhythmically at all for sperm transfer: animals eject all kinds of liquid—venom, urine, feces, slime—without any need for rhythmic movement in the ejecting organ in question. Yet in three-quarters of all species of insects, spiders, and mammals—and also in snakes, millipedes, and roundworms—definite humping goes on. And not only before ejaculation: many species continue to thrust for a long time after the male has ejaculated (in the case of the thick-tailed bush baby, for up to four and a half hours). Even in some insects that mate without any outward motion visible, the penis often moves to and fro or throbs inside the female, which Eberhard calls “cryptic thrusting.” Rather than to make the release of sperm possible, it seems more plausible that these movements are the most efficient way for a male to use his penis as an internal courtship device and make the female sense whatever knobs, ribs, spines, and palangs it is provided with. A male that is able to stimulate the receptors of nerves in his mate’s inner sanctum particularly strongly will leave a lasting impression, increasing his chances to be a preferred suitor.

  It is telling that songbirds, which do not have penises and mate simply by a fleeting “cloacal kiss” (the pressing against each other of the male and female genital openings), copulate for just a few seconds without any rhythmic movements. Except, that is, the buffalo weaver, the only songbird that does have a kind of penis—a rod 1.5 centimeters (0.6 inch) long in front of its cloaca—which it rubs against the female’s cloaca for up to half an hour before it, with quivering wings and clenched feet, climaxes.

  Of course, for internal courtship to work, the female needs to have the appropriate wiring in her genitalia to register these subtle shapes and movements. Sadly, the study of vaginal sense organs is still in its infancy. But where people have looked, they mostly have found evidence for very delicate sensitivities in the female nether regions. In damselflies, for example, the inner walls of the vagina carry a plate on either side, each of which is covered with dozens of separate sense organs. And cockroaches belie their reputation as crude vermin in the intricate arrangement of so-called campaniform sensilla in the female genitals—tiny organs that can register subtle buckling and bending of the chitin that her vulva is supported by. But of course the best-known (though still, as we shall see, understudied) female genitalia are those of humans. A woman’s vaginal walls are uniformly innervated with two kinds of nerves (large and small) all along their length, and the furrow between the foreskin and the glans of the clitoris is even more richly endowed with a variety of microscopic organs that sense fine touch, pressure, and vibration and carry such exotic names as Meissner’s corpuscles, Pacinian corpuscles, Krause’s end-bulbs, Ruffini’s corpuscles, and mucocutaneous corpuscles. All prone to be exploited sensorially by a moving, complicatedly shaped male organ.

  So there we have it. Assuming that the shape, size, and adornment of a phallus are to a large extent heritable (and where this has been studied, they tend to be), sexual selection by female choice will be a powerful force by which the evolution of genitalia is pushed around. But hang on: throughout this se
ction you may have sensed a nagging feeling that something doesn’t quite add up. Because isn’t there a crucial difference between courtship and copulation in the sense that during regular courtship rituals a female can still reject a male, whereas once she has allowed a male to insert his penis into her, isn’t it sort of too late to think, “Hmm, maybe I won’t let this particular male fertilize my eggs”? Well, prepare to have another of your certainties about sex squashed.

  Love’s Labor Lost

  Scientific research papers are usually not particularly riveting reading material. The Materials and Methods section is often the least appealing, easily skipped in pursuit of more enticing bits. But it is in the “M&M” (as scientists call it) that, hidden under dull jargon and cloaked in the passive voice, the jewels of original scientific research lie. Condensed beyond recognition into terse, matter-of-fact sentences are days, months, sometimes years of hard, enjoyable, or exhilarating (but often also mind-numbingly dull) labor, moments of despair and jubilation, false starts, near give-ups, luminous ideas, and innovative inventiveness. And not infrequently a generous helping of courage.

  The M&M sections of the two articles that Robin Baker and Mark Bellis published in the November 1993 issue of the journal Animal Behaviour describe some of the most courageous biological experiments of all time. Not courageous in the way that clambering up tropical cliff faces in search of rare animals or plants is courageous—Baker and Bellis never left their offices. Instead, courageous because they dared ask their closest colleagues and students to become sexual guinea pigs for them. In dry, to-the-point tone, the M&M section describes what they did: “[W]hole ejaculates were collected in condoms during copulation or masturbation. Subjects were provided with a ‘kit’ containing instructions and all necessary equipment, including a mixture of lubricated (non-spermicidal) and non-lubricated condoms. Ejaculate collection and fixation and the counting of sperm followed the double-blind protocol.” It states furthermore: “[C]ounts of sperm [were made] of ‘flowbacks’ (the mixture of seminal fluids, sperm, female secretions and female tissue that flows back out of the vagina after copulation).”