Nature's Nether Regions

by Menno Schilthuizen

  Even in humans, penis size does not vary as much as our preoccupation with the subject would suggest, and it is hardly related to other body size indicators—and certainly not to shoe size, despite the popular myth. In 2002, London-based urologists Jyoti Shah and Nimal Christopher published an article entitled “Can Shoe Size Predict Penile Length?” They somehow persuaded more than a hundred of their patients to have their penises measured and to divulge their shoe sizes to them. Shah and Christopher then graphed both against each other and found no relationship whatsoever—relegating the shoe-penis connection to the realm of fables. However, they measured their patients’ members in a flaccid rather than an erect state, arguing that, presumably in view of medical propriety, it was “not feasible” to measure them in their “true physiological length.” Point taken, but this could be a problem, because it is known that the longer a man’s penis in floppy state, the less it will grow in length when it becomes erect. Nor did the researchers record height or weight or any other body size measure besides shoe size. But in one of the more remarkable citizen science projects, the online questionnaire the Definitive Penis Size Survey, Shah and Christopher’s results are borne out: among more than three thousand men who filled in the questionnaire, their shoe sizes said nothing about the lengths of their erect penises. Stature fared a little better in this respect, but the allometry was still negative: men 20 percent taller on average have erections that are only 10 percent longer.

  For as long as biologists have been measuring animals (and that is a long time!), they have found that genitalia, in males as well as in females, tend to be pretty much unaffected by the size of the rest of the body, just as in stag beetles and humans. In a large survey of such animal data, Bill Eberhard, Bernhard Huber, Rafael Lucas Rodriguez, and colleagues found that this was true for virtually all of over 130 species of insects, scorpions, spiders, crustaceans, snails, and mammals. Apparently, males as well as females that are under- or overendowed do not fare well in sexual selection, suggesting that evolution smiles upon a kind of general-purpose, “one-size-fits-all” genitals. This does not seem to be because of any literal mechanical fit between the genitals, since negative allometry turns up in animal species with soft, stretchy genitalia just as much as it does in those with hard, unyielding ones. Instead, Eberhard and his colleagues think the reason may be that male genitalia need to “press all the right buttons” in the female genitals. If his or her genitalia are too large or too small, the relevant knobs do not end up opposite the relevant nerve endings and stretch receptors in the female genitalia. So in sexual selection, individuals that are so well or so poorly endowed in the nether department that they are likely to be a mismatch with many potential partners will not leave many genes in the next generation. Hence, evolution will punish those with extremely small or large genitals, and negative allometry, average-sized genitals, and “one-size-fits-all” will be the result.

  Now, the one-size-fits-all rule applies to animals where the male shoves his entire penis up the female’s vagina. But there are also species where only the tip of the penis is inserted. When that is the case, the bulk of the penis is no longer constrained by the need to fit in the female’s vagina and if, for whatever reason, evolution favors bigger penises, then grow bigger they will. We have seen this with the record-setting barnacles that Darwin discovered (Chapter 3), and in Chapter 8 we will meet slugs that have evolved penises so long that it takes them a whole night to get erect. But even then, limits may apply. Namely, when sexual selection promotes a kind of evolution that the rest of the environment, by way of natural selection, won’t allow.

  The first example of the environment curbing sexual evolution is in so-called poeciliid fish—the family to which the guppy (Poecilia reticulata) belongs, which we came across earlier in this chapter in the context of color and the rare-male effect. Poeciliids are rather exceptional fish. Not only are they among the few kinds of fish in which the males have an actual penis to inseminate the female internally—rather than just dumping their sperm over the eggs as she lays them, which is what most fish do—they also are one of the few exceptions of animals in which penis length is not negatively but positively allometric. In male guppy fish, a body size twice as long translates to a penis—known as a “gonopodium,” in fact an anal fin fashioned by evolution to serve as a sperm squirt—not twice but up to four times as long. Poeciliids may be the exception that proves the one-size-fits-all rule, since during mating males do not insert the entire gonopodium into the female. Instead, they swing it forward and either proudly display it in courtship (where females prefer better-endowed males) or—forgoing courtship—take quick stabs at her vagina from a distance, with only the tip penetrating. Interestingly, when you measure the width of the tip, the only part that actually meshes with the female genitalia, you do find negative allometry. So, clearly, in poeciliid fish, girth does not matter, but length does.

  But, as research in one poeciliid has revealed, there are limits to how long your gonopodium should get. Males of the mosquito fish Gambusia, a guppy relative that lives in lakes and ponds in the southern United States, have particularly impressive gonopodia that sometimes reach up to a third of their body lengths, and males have a habit of flashing these to interested females. Thus engrossed, however, they may not notice the predatory sunfish taking advantage of the fact that their guard is down and swooping in to snap up the hapless hormone-heavy poeciliids. Unless, that is, the mosquito fish can make a quick last-instance getaway. It is in these desperate escapes that their big members become a liability. As Brian Langerhans discovered in his work at Washington University in St. Louis, when you’re a mosquito fish and you’re trying to swim away quickly, a heavy trailing penis is—quite literally—a drag. Langerhans and his colleagues measured the speed of burst swimming in well-endowed males and found that these were much slower than in poorly endowed ones. Not only that, they discovered that the trade-off between sexual selection on penis length (bigger is better) and natural selection (shorter is safer) had left its mark on natural populations: in ponds with predator fish, gonopodia were 10 to 15 percent smaller than in predator-free ponds.

  Another example of such a trade-off is found in Tidarren spiders. About ten species of these small spiders exist, all living in the Tropics and all characterized by being half-eunuchs. As you will recall, male spiders load their pedipalps with sperm and then usually use both of them to inseminate the female. But Tidarren adolescent males, just after their second-to-last molt, do something rather peculiar. While hanging upside down from their web, they use their legs and one of their pedipalps to push the other pedipalp firmly in between the tangled threads of the web. Then they begin circling around the one pedipalp that soon becomes hopelessly tangled in more and more silken threads and, after a couple of revolutions, is no longer able to spin along with the rest of the spider and snaps off. Unfazed, such a self-mutilated male then sucks the amputated pedipalp dry and continues his one-pedipalp life (the amputated palp never grows back) until, after his final molt, he is ready to mate.

  Tidarren is one of those spiders in which mating is a once-in-a-lifetime opportunity. Their testes produce a single drop of sperm and then wither away. This single drop of sperm is sucked up in Tidarren’s one remaining pedipalp. His one-shot genital apparatus at the ready, he seeks out a female and then copulates with her—only once, for consummation is consumption: the female invariably has him for lunch even before copulation is over. As she begins nibbling away at his body, he rests secure in the knowledge that meanwhile his pedipalp—still firmly attached to her epigyne—is busily pumping his life’s supply of sperm into her.

  The self-semi-emasculation is the outcome of a curious set of evolutionary circumstances. In Tidarren, females have evolved large body size—presumably because bigger females outcompete small ones in terms of egg output—while at the same time males have evolved small bodies. And although the cause for the miniature males is still unclear, the result of
this evolution in opposite directions is that Tidarren males weigh less than 1 percent of a female’s weight! To still be able to fertilize a female, they need very, very large pedipalps—each weighs over one-tenth of the male’s body weight. The problem is, with two such hefty pedipalps hanging in front of your head, it’s almost impossible to move around. Hence, the evolution of the half-eunuch strategy.

  Self-semi-emasculation. Male Tidarren spiders routinely self-amputate one of their pedipalps, the better to move about. They do this by entangling one pedipalp in the silk of their web and then turning around and around until it snaps off. Then they suck the amputated pedipalp dry.

  That natural selection for improved mobility is indeed likely to have been the impetus for this bizarre behavior was proven in a 2004 study by Margarita Ramos and colleagues at Tulane University in New Orleans. They placed male Tidarren sisyphoides spiders on a tightly stretched silken thread of a female spider, either just before the males had self-emasculated or just after. They found that males still in possession of both pedipalps scooted along the thread at a speed of less than 3 centimeters (1 inch) per second, whereas half-emasculated males did so at more than 4 centimeters (1.5 inch) per second. Not only that, their endurance was also severely affected by the presence of an extra pedipalp. The researchers used a small paintbrush to chase a male around a piece of paper. If the male still had both pedipalps, he would collapse from exhaustion after about twenty minutes, whereas males that had self-amputated one pedipalp persevered for more than half an hour before giving up.

  The bizarre self-inflicted genital mutilation of male Tidarren spiders clearly means that its pedipalp has evolved to a size that is just about as large as the demands of a functioning spider will allow. Any larger and it would be too heavy and unwieldy for a Tidarren male to drag himself into his nuptial-cum-deathbed—that is, a female’s arms.

  Pedipalp-amputated spiders, gonopodium-encumbered poeciliid fish, and all animals that have one-size-fits-all genitalia demonstrate the limits to what sexual selection by cryptic female choice can do. And perhaps the hitting of these limits is what we see when we chart those jerky evolutionary pathways of genitalia in fossil beetles and throughout the family trees of damselflies and other animals. Perhaps once such a limit is hit, sexual selection is lame for a while and has to wait for a new mutation to appear so that genital evolution can dart off in a different direction.

  Does this mean that our picture of genital evolution is now complete? With sexual selection in the driver’s seat, steering the evolution of animals’ genitals along a winding road curbed by the limits of natural selection, it may seem that we have a satisfactory outline and that the rest is just details. But when all seems crisp and clear and yet you’re only halfway through a book, a plot twist lies around the corner. As we shall see in the next few chapters, genital evolution is not only about male courtship, female control, and their limitations. Prepare for sexual persuasion to turn nasty.

  Chapter 6

  Bateman Returns

  Entomologist Jonathan Waage of Brown University did for the penis what the Swiss army did for the penknife. In a two-page article that appeared in the journal Science of March 2, 1979, Waage revealed how a male ebony jewelwing damselfly (Calopteryx maculata) will use his penis to scoop out any sperm of previous males from the female’s genitals before using it to deposit his own. The penis as a sperm-scooper. The compact publication is seen by today’s researchers as the foundation stone of the whole field of genital evolution, and it makes its appearance in many a biology textbook. But at the time, it created little more than a tiny ripple.

  “I do not recall more than a few articles that showed up here and there in newspapers. No interviews,” says Waage. Still, the news did manage to make it across the Atlantic. I was only thirteen at the time, but I do remember reading about it, probably in Kijk, the Dutch high school science and technology monthly that I used to devour the moment it landed in our mailbox.

  What I read, thumbing the pages of Kijk excitedly, was that Waage had tried to figure out what happens in a female damselfly’s sperm storage organs when she mates with more than one male in short succession (which damselflies usually do). Are the sperm of the second male simply mixed with the first? To tackle this question, he began by catching female jewelwings—easily recognized by the white spot on their wings—at the bank of the Palmer River, a small stream just across the border in Massachusetts. Each time he caught a female, he carefully tied a length of nylon fishing line to her abdomen and, the female thus tethered, gently moved her into the territory of a male, which promptly elicited a copulation.

  You may recall from the previous chapter that damselflies mate in an unusually cumbersome and acrobatic way. This is because damselflies and dragonflies are the only insects in which the male’s penis (at the base of the long, wispy abdomen) is not attached to the testes (sitting at the tip)—a similarly disconnected affair as in spiders, which are not insects, of course. To deal with this sexual handicap, a male, after grabbing a female in the neck with the pinchers at the end of his abdomen, needs to transfer the droplet of sperm that his testes produce to a temporary sperm container next to the penis. He does this by doubling over the entire abdomen, basically to inseminate himself. Then the female throws her abdomen forward to meet his penis, thus forming the romantic heart-shaped “mating wheel.” In this position they fly or hang around for a variable length of time—a couple of minutes in the ebony jewelwing, but up to several hours in other species.

  In some cases, after a male had released her, Waage let a second male step in and mate with his female-on-a-leash; in some cases not. Either way, when the last (or only) copulation was over, he would invariably end the affair in a rather unceremonious way: by dunking the female in ethanol. Back in the lab, after dissecting the sperm storage organs of the dead females, he found that, whether they had mated once or twice, they always carried the same amount of sperm. Puzzled, he went back to the stream bank and repeated his first experiments, this time always allowing the females to mate with two different males, but killing the females before completion of the final coitus. Again, he dissected the females’ abdomens, and found that most of the females held no sperm at all or only very little—which meant that, somehow, they had lost all the sperm after their first copulation.

  Scoop your rival. In damselflies, the male grabs the female in her neck and she then flips her vagina forward to meet his genitals. In some species, the male uses the scoop on his penis (A) to remove sperm from previous males from the female’s vagina (B) before injecting his own sperm (C).

  Once again, Waage returned to the Palmer River and collected pairs of the damselflies at different stages throughout the mating, which he killed in copula and then carefully dissected under his microscope in an attempt to figure out what was going on inside a pair’s genital organs. This finally clinched it for him: in couples killed early in the copulation, Waage saw that the male still held all his sperm in his sperm store, but his penis was firmly inserted in the female’s vagina, and large masses of sperm (presumably from the female’s ex-boyfriend) clung to the backward-pointing bristles on the penis and the scoop-like horns on either side. In couples arrested in the very final stage, however, the male’s sperm store was empty, but the female’s sperm storage organs were once again filled (with her incumbent lover’s sperm). So it turned out that to a male Calopteryx maculata, copulation is about removing rival sperm just as much as about depositing his own. This also explained why the shape of the damselfly mating wheel passes through two stages. In the first part of copulation, the male’s abdomen is held in a concave shape and is seen to undulate constantly, but in the last few seconds it changes to a convex shape. What Waage’s study had shown was that the first stage is devoted to vigorous cleaning out of any previous sperm from the female’s genitals, and the second stage to filling her up with the male’s own.

  Waage’s article in Science was a seminal publica
tion (pardon the pun). It kick-started more research on damselfly sex, and a worldwide community of researchers has since confirmed that what happens in the ebony jewelwing is common practice in most other damselflies and probably also in their bulkier relatives, the dragonflies. It is now known how sense organs on the penis register the presence of foreign sperm in the female’s genitals and how the flaps, hooks, and microscopic spines and teeth on the penis trap the clump of sperm while the muscles of the penis move it up and down to pump, scoop, and scour out sperm of a predecessor.

  More important, Waage’s paper, published six years before Eberhard’s first book, marked the start of the current wave of serious, wide-ranging research on genitalia in all kinds of animals. Waage had shown, in spectacular fashion, that damselflies adhere to a very literal interpretation of what Geoff Parker (of dung fly fame) had termed “sperm competition.” Parker, in a famous 1970 article, had suggested that a male insect, rather than just persuading a female to choose his sperm over that of his competitors, may up his chances by targeting that competing sperm directly. And indeed, Waage’s damselflies did exactly that, using their penises as true shovels to purge their mates’ vaginas of any rival spermatozoa. Hence, we might expect that the wave of ensuing genital research that began after Waage’s publication was driven by the notion that scuppering the reproductive efforts of one’s rivals might be a very important force in the evolution of male genital organs. And that the road lay open to examine all genital form in this light.

  But this did not happen—or at least, not immediately. Waage himself continued working on damselfly sex throughout the 1980s, but eventually moved into administrative positions, spending less and less time on his scientific work. And although he fathered a band of damselfly sexologists who followed in his footsteps, in the meantime Bill Eberhard’s first book was published, which stole the spotlight. The growing community of animal genital researchers turned to cryptic female choice, overlooking the importance of sperm competition. And yet, if we take a closer look at the way male and female genitalia interact in different species of damselflies, we get a peek into a world that does not seem to be ruled entirely by cryptic female choice, but rather by a kind of evolutionary loggerheads over what he wants and what she wants.