Nature’s Nether Regions

Description

A tour of evolution’s most inventive—and essential—creations: animal genitalia

Forget opposable thumbs and canine teeth: the largest anatomical differences between humans and chimps are found below the belt. In Nature’s Nether Regions, ecologist and evolutionary biologist Menno Schilthuizen invites readers to discover the wondrous diversity of animalian reproductive organs. Schilthuizen packs this delightful read with astonishing scientific insights while maintaining an absorbing narrative style reminiscent of Mary Roach and Jerry Coyne. With illustrations throughout and vivid field anecdotes—among them laser surgery on a fruit fly’s privates and a snail orgy—Nature’s Nether Regions is a celebration of life in all shapes and sizes.“Schilthuizen whizzes between geographies and species, learning from apes, slugs, spiders. In the process he invites us on all kinds of interesting adventures, from finding ancient beetle genitals trapped in amber to examining barnacles depositing their sperm with eight-foot-long appendages…. This is a book about heterosexual sex between animals, but Schilthuizen hasn’t closed the case on other kinds of sex driving animal evolution, too. Ever excited, ever open-minded, he pushes towards new frontiers.”
–Tess Taylor, Barnes and Nobles Review

“From the very first page, Menno Schilthuizen makes us both laugh and think about the bewildering genital variation in the animal kingdom. We laugh at the outrageous shapes these organs take, and think about the central issue of this book: how genital anatomy advances male and female procreation. An exhilarating and most informative read!”
—Frans de Waal, author of The Bonobo and the Atheist
 
“A remarkable book… succeeds in finding exactly the right tone…. Schilthuizen’s entertaining work reminds us not to take ‘the mechanics of sexual intercourse’ for granted.'”
—Publishers Weekly
 
“A provocative voyage on the ‘vast ocean of sexual function beyond the quiet backwater that we humans find ourselves in.’”
—Kirkus
 
“The science of genitals is a relatively new field for biologists, who have long overlooked the evolutionary importance of species’ private parts. Biologist Schilthuizen balances the silly and the serious to describe researchers’ latest efforts to understand how ‘evolution has graced the animal kingdom with such a bewildering diversity of reproductive organs.’ Schilthuizen tours some of nature’s weirdest inventions, such as the chicken flea penis, which is ‘actually a profusion of plates, combs, springs, and levers’ and looks like ‘an exploded grandfather clock.’”
—Scientific American

“Rather than furiously flipping through a stack of increasingly obscure science journals, those interested now have an easily digestible text to work with, the charmingly titled, Nature’s Nether Regions, by Dutch evolutionary biologist Menno Schilthuizen. Menno’s book is a deep dive into the science of genitals, one that comes interspersed with a selection of the finest, and most scientifically-accurate, sex jokes.”
—Lex Berko, Vice’s Motherboard
 
“A closer look between the legs (or, in the case of the Australian velvet worm, on the head) to explore what the sex lives of various creatures can teach us about reproduction, diversity and human sexuality…. I actually missed my stop on the train this morning because I was engrossed in the chapter about duck sex.”
—Lindsay Abrams, SalonMENNO SCHILTHUIZEN is a research scientist at the National Museum of Natural History in Leiden, the Netherlands. He has written on ecology and evolution for Science, Natural History, and other publications.

ABOUT THE AUTHOR

 . . . yes and his heart was going like mad and yes I said yes I will Yes.

—James Joyce, Ulysses

Preliminaries

Not too long ago, the Netherlands Natural History Museum was housed in a lofty, cavernous building in the historical center of Leiden. Generations of biology students took their zoology classes there, in its two-tier lecture theater over the monumental staircase. During the less captivating parts on crustacean leg structure or mollusk shell dentition, their gaze would have wandered off to the two features that made this lecture room unforgettable. First, its abundant display of antlers of deer, antelope, and other hoofed animals, hundreds of them, suspended from the walls. Second, the huge painting from 1606 of a beached sperm whale that hung over the lectern. On an otherwise nondescript Dutch beach lies the Leviathan, its beak agape, its limp tongue touching the sand. A smattering of well-dressed seventeenth-century Dutchmen stand around the beast. Prominently located, and closest to the dead whale, stand a gentleman and his lady. With a lewd smile, face turned toward his companion, the gentleman points at the two-meter-long penis of the whale that sticks out obscenely from the corpse. Centuries of smoke-tanned varnish cannot conceal the look of bewilderment in her eyes.

These few square feet of canvas, strategically placed in the painting’s golden ratio, exemplify two things. First, the unassailable fact (supported by millennia of bathroom graffiti, centuries of suggestive postcards, and decades of Internet images) that humans find genitals endlessly fascinating. Their own, but by extension those of other creatures, too. The amazing diversity in shape, size, and function of the reproductive organs of animals has been an eternal source of wonder, making bestsellers of the 1953 book The Sex Life of Wild Animals, the 1980s classroom wall poster Penises of the Animal Kingdom (over twenty thousand copies sold), and the Sundance Channel series Green Porno—short films starring a sanguine Isabella Rossellini enacting the copulation of various animals.

The second point that may be underscored with this seventeenth-century sperm whale penis is the curious observation that the public fascination with genitalia was, until very recently at least, not matched by equally intensive scientific inquiry. The lofty offices down the corridor from this lecture theater housed scores of biologists quietly cataloging the world’s biodiversity. In good classificatory tradition, they would painstakingly draw, measure, photograph, and describe the minutiae of the genitals and distinguishing features of the reproductive organs of any new insect, spider, or millipede they would discover—and yet never stop to wonder how these private parts evolved.

We really have Darwin to blame for this. In his next-greatest book, The Descent of Man, and Selection in Relation to Sex (1871), Darwin explains how secondary sexual characteristics—like colorful bird plumage, the prongs on beetles’ heads, and the antlers of deer—have been shaped not by natural selection (adaptation to the environment) but by sexual selection: adaptation to the preferences of the other sex. He denies the primary sexual characteristics entry to his theory by categorically stating that sexual selection is not concerned with the genitalia or primary sexual organs—which, after all, are merely functional, not fanciful. So the diversity of all those antlers on the walls of the museum lecture room had been a tradition of evolutionary biology since Darwin, but investigating the evolution of the business end of things—of which the centerpiece of that seventeenth-century painting is just one prominent example—hadn’t.

It took until 1979 for evolutionary biology to start paying attention to genitalia. In that year, Jonathan Waage, an entomologist from Brown University, published a short paper in Science on the damselfly penis. He demonstrated that this minuscule penis carried a miniature spoon that, during mating, cleaned out the female’s vagina, scooping out any remaining sperm from previous males. It was an eye-opener as well as a sperm-scooper. For the first time, here was proof that animal genitals are not just mundane sperm-depositing and sperm-receiving organs, but are sites where a sexual selection of sorts goes on. After all, during damselfly evolution, males with the best sperm-scoopers had left more descendants.

The time was ripe for this paper. When I interviewed Waage about those early days, he recalled how, in the years leading up to his sperm-scooper discovery, he had been influenced by the quiet revolution that biology faculties worldwide were undergoing at the time—a sea change brought about by George C. Williams’s book Adaptation and Natural Selection and by Richard Dawkins’s popularization of it, The Selfish Gene. People began to do away with the false notion that evolution works “for the good of the species” (an outdated concept, echoes of which can be heard even today in nature documentaries). Instead, they began viewing evolution correctly, as the effect of a kind of reproductive selfishness, in which it is all about the success of an individual in carrying its genes into the next generation. Evolution does not “care” about the species. And if a sperm-scooper would scupper the chances of competing males, then that is what evolution would favor. Waage was one of the first scientists to start asking the questions that mattered for how evolution works. And since evolution is all about reproduction, no wonder Waage and other modern biologists would sooner or later find themselves closely inspecting genitals.

In that same revolutionary era, other young biologists began asking similar questions. One of them was a certain undergraduate biology student who in the 1960s was earning some extra cash with menial tasks in the depot of Harvard University’s Museum of Comparative Zoology. His job was to top up the alcohol in jars with pickled animals and to organize unsorted spider specimens. Picking up spider identification guides, the student began wondering why spider species are so often distinguished by the way their genitals are formed. Asking around in the museum, he was told that that is just the way it is. The genitals of different species of animals, be they spiders, spittlebugs, or Spanish fly, are often widely different, even if the species are one another’s close relatives and look identical on the outside. Probably, his seniors told him, the genetic differences also accidentally affect the shape of the genitals. Very useful if you want to identify spiders, but probably quite meaningless biologically. The student, unconvinced but not in a position to argue, shelved the question in the back of his mind, graduated, and went on to become a productive and successful tropical biologist at the Smithsonian Institution’s Tropical Research Institute in Panama.

That student’s name was Bill Eberhard. And when, many years later, the issue of Science with Waage’s damselfly penis article landed on his desk, that old conundrum from his undergraduate days let out a little muffled cry from beneath many layers of mental clutter. Perhaps genitalia, in spiders as well as other animals, differ so much because each is a different kind of sperm-scooper? As it happened, Eberhard was about to begin a six-month stint as a visiting scientist at the University of Michigan, which gave him the opportunity to spend some weeks in the library.

There, he pulled off one of those rare feats of biological unification. It is often not realized that the basic source of inspiration in biology, namely the endless diversity of life, is also one of its greatest handicaps. Biologists, much more than, say, chemists or mathematicians, tend to be divided by invisible barriers. Those barriers are held in place by expertise with a particular kind of organism. More often than not, biologists identify themselves as entomologists if they work with insects, or as botanists if plants are their thing. Or even as copepodologists, coleopterologists, or cecidomyiidologists (if their creed be copepods, beetles, or cecidomyiid gnats, respectively). And each organism-based field has its own congresses, professional societies, and journals, further affirming separatism. Contrary to, for example, physicists, to whom a neutron is a neutron is a neutron, biologists are always unsure whether what applies to one kind of organism also applies to another—or, worse, they don’t care about broad applicability at all. As ecologist Stephen Hubbell lamented, if Galileo had been a biologist, he would have spent his whole life documenting the trajectories of different animals thrown off the Leaning Tower of Pisa without ever coming up with gravitational acceleration.

Biology really moves ahead when somebody dares to cut across all those different subfields and look for general patterns. And that is precisely what Eberhard did when he cloistered himself in the University of Michigan library and began pulling books off the shelves on the genitalia of mice and moles, snails and snakes, weevils and whales. Four years later, in 1985, what had started as a little hobby project had turned into the 256-page Harvard University Press classic Sexual Selection and Animal Genitalia. In it, besides dazzling his reader with a sheer endless parade of wondrously shaped animal willies, Eberhard made two points. First, that genitals are bafflingly complex systems, far too complicated for the relatively simple task of depositing and receiving a droplet of sex cells. The male chicken flea, for example, has a “penis” that is actually a profusion of plates, combs, springs, and levers and looks more like an exploded grandfather clock than a syringe—whereas the latter should suffice if the organ’s role were just to squirt sperm into the female. And the second point he made was that no body part in the animal kingdom evolves as fast as genitalia.

In his book, Eberhard argued that the reproductive organs of animals are under constant, intensive, and multitarget sexual selection—including the kind revealed by Waage, but certainly not limited to that. This is why they are so complex. This is also why they differ so much from species to species—a phenomenon that taxonomists (that special breed of biologist whose task it is to circumscribe, describe, name, and classify biodiversity) had been happily using throughout the twentieth century as an easy way to differentiate species. Animals’ nether regions are the stages where an evolutionary play is performed that would have made even Darwin blush. An evolutionary play that had been totally ignored by generations of biologists—even though genitalia are probably the best body parts to illustrate the power of evolution.

And yet the evidence had been, quite literally, staring us in the face. Humans and our fellow primates do not shy from Eberhard’s accelerated genital evolution. Forget forebrains, canine teeth, and opposable big toes: the largest anatomical differences between us and our closest relative, the chimpanzee, are found in our nethers. The human vagina is flanked by two pairs of skin folds, the labia minora and the labia majora. The clitoris is a two-winged structure lying along the walls of the vagina, and only the relatively small glans is visible externally, covered by the clitoral foreskin and lying at the point where the labia minora join. The chimpanzee vagina, on the other hand, lacks labia minora, has a larger and downward-pointing glans of the clitoris, and contains specialized tissue that makes the labia and the foreskin of the clitoris swell dramatically during the fertile phase of the menstrual cycle, causing the vagina to bulge out and increasing its operating depth by 50 percent. And on the other side of the sexual divide the differences between these two sister species are no less striking. The human penis is thick and blunt ended, boneless, has a ridge around the smooth glans, and has a foreskin. It has two corpora cavernosa, the sponge-like tissue that swells during erection. The chimp penis, by contrast, is thin and sharply pointed, carries a penis bone (baculum) inside, has no glans, no foreskin, and only one corpus cavernosum. Oh—and it carries lots of tiny tough spines along the sides.

In other words, the exaggerated diversity—biodiversity—in genital shapes that Eberhard had highlighted carries right up to our own species. The evidence for this pattern throughout the animal world is available in large quantities of respectable nineteenth- and twentieth-century tomes on comparative anatomy and systematic zoology, and yet before Eberhard nobody had bothered to explain it.

But this is not a book about Bill Eberhard. Rather, it is about the band of disciples that followed in his footsteps. Hundreds of scientists all over the world, myself included, have been inspired by Eberhard’s book. Together, with our lab experiments, fieldwork, and computer simulations on a wide variety of organisms from primates to pack rats and from sea slugs to sexton beetles, we have nursed to life a brand-new discipline of evolutionary biology: a science of the genitals, if you will. And, as disciples and disciplines are wont, we have increasingly come to dispute the exact workings of genital evolution. Are penises internal courtship devices, as Eberhard would have it? Or are they used to combat rival males on the female’s turf, as Waage showed? Or are male and female genitalia perhaps at loggerheads over who is in charge of fertilization, as people like the English zoologist Tracey Chapman think?

Despite these bones of contention, two things unite these scientists. First, a genuine desire to understand. To reconstruct the tortuous routes by which evolution has graced the animal kingdom with such a bewildering diversity of reproductive organs. And second, that same innate interest in all things sexual that is the reason why you are reading this book and also the reason why I wrote it.

Such fascination with private parts notwithstanding, by devoting an entire book to the field, and by not shying from the more complicated bits, I hope to rise above the giggly press genital researchers have been getting. I am not saying this book will be any less naughty in tone. Still, rather than being a vaudeville of juicy anecdotes fished from the nooks and crannies of animal weirdness, evolution of genitalia has, over the past twenty-five years, matured into a solid science where extreme biodiversity, advanced evolutionary theory, and elegant experimentation come together. My aim is to paint a portrait of this new branch of biology.

From time immemorial, we have taken the mechanics of sexual intercourse for granted. But the nitty-gritty of our own reproduction is anything but default. The evolution of our genitals has steered the evolution of our copulation behavior and vice versa, blessing (or saddling) us with just one of the possible outcomes of countless scenarios of complex evolutionary interactions, involving everything along the continuum between graceful dances and vicious arms races. Realizing this may make us better appreciate humans’ place in the reproductive diversity of life.

Chapter 1

Define Your Terms!

This book is not about sex.

A puzzling statement, perhaps. You could have sworn that the preceding pages were strewn with words and phrases that in everyday parlance would be flagged as decidedly sex related. But then the meaning of biological terms in everyday parlance often is quite divorced from the same terms used by actual biologists. To a biologist—at least during working hours—“sex” does not mean the events leading up to and including the insertion of genitalia into somebody else’s genitalia and/or additional orifices. Instead, it means something like “the exchange of DNA between two individuals.” And exchanging DNA can be done in a multitude of ways, many of which do not involve any activity that the man or woman on the street would consider “sex.”

Take bacteria, for instance. They regularly pick up bits of DNA from other bacteria, which they transfer to their own genetic machinery via finger-like protrusions called pili. They even take up and incorporate into their chromosomes whatever loose strands of DNA take their fancy as they encounter them in their microscopic environment. Such “bacterial sex,” as microbiologists call it, is a far cry from the results one gets when typing “sex” into an Internet search engine. For starters, bacteria use sex—that is, looting the environment for bits of DNA code—not for procreation but to improve their own lot (so do many people on those Internet pages, but that’s another matter). The DNA that bacteria mop up from their environment might contain genes that they can put to good use. To fix gaps in their own DNA, for example, or to feed on foods that their original DNA did not contain the digestive tools for. They don’t do it to reproduce. For that, bacteria simply divide themselves—in the bacterial world, sex and reproduction are two entirely unrelated activities.

For most larger organisms, like ourselves, sex is a usual component of reproduction. We carry double sets of all our genes—one set inherited from Mom, one from Dad—produce eggs and sperm that contain single sets of those genes, and combine sperm with eggs to produce children with reconstituted double sets of genes. But there are many different ways in which organisms can make sure that eggs and sperm meet, and copulation is just one of them. Fixed on their reefs as they are, corals, for example, cannot consort with one another and thus are left with no option but to release their eggs and sperm into the waters and hope for the best—that is, fortuitous chance encounters between them. And the birch trees that line the streets of many a northern country pump billions of pollen into the air each spring, of which a very small fraction is wind-carried to the stamens of female catkins. Only a few hay fever sufferers realize that they are sneezing themselves through clouds of birch ejaculate.

Okay, you might say, so sex is perhaps a bit unconventional in such obscure things like microorganisms and corals, but surely most of the more familiar animals “have sex” to mix their DNA with that of their partner and produce babies, right? Sorry, no. Not necessarily. Pseudoscorpions, for example, don’t. In these animals, which look like miniature scorpions but without the sting, males simply leave tiny stalked sperm-filled balloons scattered throughout their neighborhood. Females encounter these surprises and, if they feel so inclined, position their genital openings over them, squat down a little, and absorb them. And many species of springtail and salamander perform similarly impersonal sex. In fact, biologists think that this is the original system, and that genitalia evolved later to make the transfer of such sperm packages more efficient. What we, from our myopic human-centered perspective, consider “sex” is just one of the many ways that organisms have evolved to combine packaged DNA from one individual with that of another.

Another general misconception is that, in nature at least, sex and reproduction are synonymous. But they are not. We have just seen that bacteria have sex (that is, they mix foreign DNA with their own) but don’t necessarily reproduce in the process. Conversely, there are lots of organisms that reproduce without sex. Bacteria, but also many plants, some parasitic wasps, stick and other insects, some lizards, as well as tiny aquatic creatures called bdelloid rotifers, to name but a few, almost always eschew sex. They consist entirely of females that simply give birth to cloned daughters that are genetically identical copies of themselves. No males, no exchange of DNA via sperm and eggs, and certainly no hanky-panky.

In fact, now that we are on the subject, biologists are still puzzled as to why there should be sex at all. Cloning yourself, as the animals in the previous paragraph do, is four times as efficient as sexual reproduction. First, you don’t need to share your genes with those of a male (a twofold advantage); second, all your children can have babies, rather than only the female half (another twofold advantage). The fact that sex is so pervasive in nature means that there must be an enormous benefit to having sex over cloning yourself. And, no, in biology “the joy of sex” does not qualify as an advantage. Instead, you may be surprised to learn that biologists think that sexual reproduction evolved either as a way of outsmarting parasites or as a way to purge your DNA of harmful mutations.

The parasite theory goes as follows. Let’s, for the sake of argument, imagine that humans were a clonal species. That Eve, so to speak, had never lain with her male companion but instead begot genetically identical daughters who then gave birth to clonally reproduced granddaughters and so on, until the whole world was populated by identical copies of Eve.

Enter a killer parasite. In a sexual species, such a deadly parasite—a virus, for example—would normally not be able to spread very far, because soon it would encounter individuals that were genetically so different from its first victims that it would need to mutate to overcome their immune systems. But in a clonal species, everybody is genetically identical, has the exact same weak spots, and is thus equally susceptible to the new parasite, which would spread like wildfire and kill off all clonal Eves in no time.

The benefits of clonal reproduction could thus be lost in one disastrous sweep of parasitic infection. A sexually reproducing animal or plant, on the other hand, does not run this risk, because all its offspring are genetically different (being random recombinations of the genes of both parents), so that even if a particularly mean parasite strikes, there would always be some offspring that are more resistant than others.

So there you have it: to stay one step ahead of fast-evolving parasites, the members of a species have to use sex to keep reshuffling their genes all the time. Since this is akin to getting nowhere fast, the parasite hypothesis is also known as the “Red Queen” hypothesis, after the Red Queen in Lewis Carroll’s Through the Looking-Glass, who tells Alice, “Now, here, you see, it takes all the running you can do, to keep in the same place.”

Attractive as the parasite hypothesis may be, there is another popular (well, popular among evolutionary biologists) explanation for the benefits of sex: that it is a clever way to get rid of accumulated errors in your DNA. Each time DNA is copied—to produce a sperm or egg cell, for example, or during cloning—there is a small chance that one or a few letters in the DNA code will be misread by the copying machinery (which is only chemical, after all) and misincorporated into the copy. Occasionally, this leads to a T where first there was an A, or a C is accidentally replaced by a G, or perhaps an A is unintentionally doubled to AA or skipped altogether.

These “spelling errors” are sometimes harmless or even beneficial, but more often they will be flies in the genetic ointment. In a celibate organism that reproduces solely by copying itself, there is no way to prevent such harmful mutations from accumulating from one generation to the next, like making photocopies of photocopies of photocopies, which eventually leads to illegible text. Each daughter inherits the exact genome of her mother, flaws and all, and adds new ones of her own. Over many generations, lots of those little errors will have piled up in her descendants, and overall their genetic health will deteriorate.

Now, sex can prevent this. Of course, during the production of eggs and sperm such errors are also made and are inherited by sexually created offspring. But since the genetic shuffling during the production of eggs and sperm is a chance process, as is the combination of sperm and eggs to produce new organisms, some offspring will inherit lots of errors, and some none at all. This means that if the ones with fewer inherited DNA mistakes are slightly “fitter,” they will be the ones surviving, thus purging each litter of the worst genetic flaws.

Scientists are still debating which of these two theories is more likely to explain the benefits of sex. What is beyond doubt, though, is that such benefits must exist. Without them, all creation would simply be cloning itself, and there would be no genders, no sperm, no eggs, no mating, no genitals, and certainly no popular science books about them. So it is important to keep in mind that sex, familiar and unavoidable as it may seem to us, is not the default way of reproducing in nature. It is Reproduction 2.0, a surprisingly complicated way that has evolved to avoid the encumbrances of straightforward cloning.

Whence She and He?

And there are more aspects about sex that seem to go without saying but, upon closer scrutiny, beg for an explanation. Take males and females. What is that all about? Nothing in the menu for sexual reproduction specifies that for the mixing of DNA two different kinds of individuals are required. Think about it: if there were only one gender and everybody could mate with everybody else, then finding a mate would be twice as easy while still keeping the genetic benefits of sex. What could possibly be the point of imposing a rule that says there must be two genders and you are allowed to reproduce only if you mix your genes with those of the other gender?

Nature is not bureaucratic, so there must be a good reason for such a strange decree. Not surprisingly, biologists disagree over what that reason may have been back in the deep recesses of the prehistory of life. They have come up with several theories, but the one with the best cards argues that separate sexes evolved to prevent war between organelles. I realize you must be frowning now. War? Organelles? Let me elaborate.

All organisms beyond the complexity of bacteria carry so-called organelles in their cells. These are tiny contraptions that perform important functions. An example is the green chloroplasts that sit in plant cells and that house the chlorophyll and the rest of the photosynthesis machinery. Although they seem to be purpose-built micromachines, such organelles are actually the stripped-down descendants of free-living bacteria that, at some time in the distant evolutionary past, invaded the cells of other organisms and began a joint venture with them. They still retain some independence: they have their own DNA and divide themselves.

And in this organelle independence lies the problem. During sex, one sex cell of one organism fuses with one sex cell of another organism. If both contribute their organelles to the daughter cell that is produced by this fusion, it will be populated by two types of organelles: one type from one parent and another, with probably slightly different organellar DNA, from the other parent. Since both types of organelles play the same role in the cell, evolution will favor those types that are best at competing against the intracellular rivals. This may mean that organelles would evolve to draw a lot of resources from their host cell to be able to divide more quickly than the organelles that they share the cell with, or even produce toxic substances to kill their rivals.

Having the inside of its cells turned into an organelle battlefield cannot be good for the host, so if sexual reproduction started off with the fusion of identical sex cells, sooner or later evolution came up with an improved system. In that system, some organisms made very small sex cells, which carried zero or very few organelles, and others made much larger sex cells with lots of organelles. When two small sex cells fused, they would not have enough organelles to start life. When two big sex cells fused, their organelles would engage in a war of attrition over cell domination. But when a small and a large sex cell fused, the organelles from the big partner would immediately swamp the few contributed by the small partner, and the rest of the life of the new organism would not be plagued by any more organelle warfare.

The evolutionary result of this cellular peace process was a system for sexual reproduction with two different kinds of organisms: one kind (“male”) always producing small sex cells (“sperm”) that contribute DNA to the offspring but no organelles, and another kind (“female”) delivering large sex cells (“eggs”) with DNA plus lots of organelles. It’s a sobering thought that the whole system of separate males and females and the ensuing war of the sexes may have come about as a necessary complication to prevent an even more disastrous microscopic war inside our cells. In fact, as the closing chapter of this book will show, males and females do not even need to be in separate bodies. Hermaphrodite animals are male and female at the same time, equipped with masculine as well as feminine machineries, fertilize each other and yet, despite this equality, live even more bizarre sex lives than “regular” animals.

What Is Primary Anyway?

Ask any medical doctor what primary and secondary sexual characteristics are, and she will roll down a wall chart with a man and a woman in full frontal nudity and deftly point out the geography of both on the human body. Penis and scrotum with testicles in the man, and vagina in the woman are the primary sexual characteristics—at least as far as is visible without the aid of a scalpel or a speculum. Secondary sexual characteristics are lots of additional differences between men and women, scattered all over the body and ranging from breasts, hips, and stature to hair-loss patterns, jawlines, and fat deposition arrangement on the buttocks. It seems crisp and clear-cut: Primary are all those features that are directly involved in making babies. Secondary are all the other ways in which males and females—for various reasons—tend to differ.

The eighteenth-century Scottish surgeon John Hunter, who first coined the terms “primary” and “secondary” sex differences, did not have any qualms about the distinction either. But Charles Darwin, writing almost a century later, did. In The Descent of Man, and Selection in Relation to Sex, published in 1871, Darwin mused about the fact that when one tries to generalize across all animals, it becomes problematic to draw a clear line between primary and secondary: “[Secondary sexual characteristics] are not directly connected with the act of reproduction; for instance, in the male possessing certain organs of sense or locomotion, of which the female is quite destitute, or in having them more highly developed, in order that he may readily find or reach her; or again, in the male having special organs of prehension so as to hold her securely.” So far no problems there. But then he went on to say that “[t]hese latter organs of infinitely diversified kinds graduate into, and in some cases can hardly be distinguished from, those which are commonly ranked as primary.”

To understand Darwin’s predicament, imagine the drumstick-like appendages on either side of the penis of the ladybird beetle (ladybug) Cycloneda sanguinea that it uses to tap the female during mating. Or the bright turquoise testicles of male l’Hoest monkeys. The ladybird penis and the mammal scrotum are supposedly primary sexual characteristics, but they have properties that seem unnecessary for transferring sperm. Unless we carry the distinction to its logical conclusion, Darwin wrote, and consider only the ovaries and testicles primary, “it is scarcely possible to decide . . . which ought to be called primary and which secondary.”

In the end, Darwin avoided this gray area (probably much to the relief of his Victorian contemporaries; see Chapter 3) by staying well away from the genitals, stating that his book would chiefly be concerned with “sexual differences quite unconnected with the primary reproductive organs.” He then duly proceeded to investigate the evolution of all kinds of body decoration, ornaments, and armature that male animals are adorned with but females aren’t. Still, he did give us a way out of the difficulty of deciding between primary and secondary: by pointing out the distinction between evolution by natural selection and evolution by sexual selection.

Rhinoceros beetle horns, crustacean claws, deer antlers and prongs, stag beetle jaws, cricket and grasshopper song, bird plumage, and a whole range of other animal traits that distinctly differ between males and females are due to an evolutionary process that Darwin called sexual selection (or, in the title of his book, “selection in relation to sex”). In many ways, the discovery of this process was every bit as revolutionary as his discovery of evolution by natural selection, the focus of his more famous book, On the Origin of Species. We will return to Darwin and the theory of sexual selection in a later chapter, but for now let us focus on the fundamental difference between these two kinds of selection.

Evolution by natural selection needs four things to take place. First, there has to be variation between different individuals of the same species—say, in the numbers and sizes of fawn and maroon patches on a partridge’s back. Second, this variation must be heritable; the offspring of a partridge with particularly large fawn patches on its back must also get relatively large fawn patches. Third, more offspring are produced than can survive. This is usually the case—a partridge lays up to twenty eggs; if all the chicks grew up, within a few decades we’d be knee-deep in partridges. The fact that partridges usually are much thinner on the ground means that most chicks do not survive into adulthood—they die of disease and are eaten by birds of prey. And the fourth condition is that death is not random—if the birds with more fawn on their backs are slightly less likely to be noticed by passing hawks in the dry grass in which they live, then the more fawn-colored partridges will have a slightly lower chance of dying than the more maroon ones. If all four of these conditions are fulfilled, then the stage is set for evolution by natural selection: a maroon species of partridge will, through natural selection by foraging birds of prey, and over many bird generations, evolve into a fawn species. It’s a law of nature.

Sexual selection is different. Here, the great selector is not some extraneous entity like hungry birds, or parasites, or the weather. It is the other sex of the same species. If the environment, including partridge-eating hawks, did not favor one color over the other, the species would still evolve if partridge females preferred to mate with fawn-backed males rather than with maroon-backed ones (or even vice versa). Fawn-backed males would mate earlier or more often, with more different females and be able to father more chicks than maroon-backed ones, and sexual selection would be ongoing. Both sexual selection and natural selection boil down to the same thing—more of your genes in the next generation’s gene pool—but they work by different means.

Having clearly demarcated sexual from natural selection, Darwin then returned to the problem of deciding which sexual characteristics are primary and which are secondary by making only one kind of selection responsible for each. Primary sexual organs, he said, are those that are maintained by natural selection. A male partridge needs organs to produce sperm and a thingy to squirt his sperm into the female. Similarly, females need the machinery to produce eggs and the plumbing to receive, store, and transport sperm. All these characteristics have been shaped by natural selection imposed by the bare necessities of life: individuals lacking any of these traits simply did not leave any offspring. But if partridge males have bright fawn backs, or red wattles under their eyes, or strange tufts of feathers on their necks, whereas females don’t, then those secondary sexual characteristics are likely to have evolved through sexual selection, the result of the greater success that thus adorned ancestral males had over plain ones in the sexual strife over females.

Eminent biologist and philosopher Michael Ghiselin of the California Academy of Sciences in San Francisco has delved a bit deeper into the definitions of the terms we use when speaking of sexual characteristics—or sexual “characters,” as biologists prefer to call them. I mentioned the human scrotum as well as the blue scrotum of other mammals as sexual characters. As Ghiselin has rightly pointed out, use of the term “character” is unforgivably sloppy. If having a scrotum is already a character, then having a blue scrotum cannot be a different character. Instead, Ghiselin thinks, it would be better to speak of “parts” on the one hand and their “attributes” or “properties” on the other. A scrotum is a part, but its color, whether naturel, bright blue, or bright pink as in the rhesus macaque, is an attribute of that part.

In this book, we will see that combining Ghiselin’s reasoning with Darwin’s is the best recipe for dealing with the confusing categories of primary and secondary sexual characters. Genitalia are primary sexual characters: penises and vulvas and their multiform equivalents throughout the animal kingdom are “primary” because they are necessary “parts” that have evolved by natural selection. But most of their attributes—whether a penis is straight, coiled, two pronged, spined, double, or spatulate, for example—are the result of sexual selection and thus are secondary characters. In other words, most primary sexual characters are primarily secondary in character!

How to Be a Private Part

You probably realize by now that any distinction between primary and secondary sexual characteristics is a semantic morass. You will not encounter these terms anymore in this book. Instead, I will speak of genitals, genitalia, or genital organs. We may be jumping from the frying pan into the fire, though, because these terms still require definition. Fortunately Bill Eberhard, whom we already encountered in the Preliminaries, and who will grace these pages with recurrent appearances, has given us such a definition. Male genitalia, Eberhard said, are “all male structures that are inserted in the female or that hold her near her gonopore during sperm transfer.” “Gonopore” is just a fancy word for vagina (which itself is a fancy word for a whole lot of other terms), and “near” is admittedly a little vague, but for the moment we have a good way to describe the territory of this book, as far as the male is concerned.

As for female genitalia, Eberhard stated: “I will consider as genitalia those parts of the female reproductive tract that make direct contact with male genitalia or male products (sperm, spermatophores) during or immediately after copulation.” Again, there’s some space for multiple interpretations there (what’s “immediately after”?), but for our purpose Eberhard’s definition of female genitalia will do fine. So, in a nutshell, in this book I will deal with the male machinery that transfers ejaculate to the female, and those female parts that receive and store it. (That also means I won’t say very much about ovaries and testes, the organs that produce the sperm and eggs.)

It is important to realize that, thus defined, genitalia are organs that are present only in a limited set of animals, namely those that do internal fertilization. The myriad of waterborne creatures that simply shed their sperm and eggs into the waves do not have genitalia (and won’t feature in this book). Again, we, from our human standpoint, are easily fooled into thinking that those “broadcast spawners” are the odd ones out. But in fact, it is we and all other landlubber animals that are really the weirdos here.

After all, animals evolved in the sea. For hundreds of millions of years, all the major evolutionary acts in the play of life had already been played out against a marine backdrop before, in the final act, a few twigs of that great evolutionary tree began spreading out on land: some plants, of course, fungi, some arthropods, snails, a couple of kinds of worm, vertebrates. The rest of life stayed safely in the briny womb of the sea. And how right they were to do so: marine organisms live in an environment that is extremely friendly to their sex cells. The saline solution chemically cushions their sperm and eggs; it is wet and has the same concentration of salts as do these cells themselves, so many marine animals can safely fertilize one another from a (great) distance by releasing into the currents their sperm, and often also their eggs, and trust that these will reach one another.

The situation faced by sex cells as they left the bodies of those first colonists on land, on the other hand, must have been like a Normandy beach on D-day. Spawning on land is out of the question: sperm and eggs will dry and shrivel and die in a matter of seconds. Even freshwater is deadly: unlike most cells, sperm cells cannot regulate the concentration of their salts, and as was first discovered by Dutch scientist Antoni van Leeuwenhoek in 1678, a sperm cell, when dropped in freshwater, will automatically imbibe so much water that it explodes in a matter of seconds. (This, incidentally, should lay to rest all those urban legends about women getting pregnant from previous guests’ sperm clinging to the rims of hotel bathtubs.)

No wonder, then, that land and freshwater animals (and, admittedly, some marine animals—but for different reasons) have had to evolve ways to protect sperm during their trip from male body to egg. A fail-safe way is, of course, never to allow the egg to leave the body of the female, and to inject the sperm directly into the female body. And that is precisely what copulation and genitalia achieve.

Still, biodiversity being what it is, lots of animals that engage in what can only be called copulation choose not to use their penises to insert the sperm or their vaginas to receive it. Instead, they use parts of their body originally intended for a different purpose. Take rhodacarids, tiny soil-dwelling predatory mites. A male rhodacarid uses his jaws, not his penis, to transfer his sperm to his mate, which she may then absorb not with her vagina but through a pore on the base of one of her legs. For all intents and purposes, the male jaw and the female hip pore are their genitalia.

And mites are not alone in forgoing conventional sex organs in favor of a substitute. Before courting a female, a male spider fashions a special tiny sperm web, then “masturbates” into it and sucks up the sperm in his elaborate, fountain-pen-filler pedipalps—stubby arms on both sides of the head with hollow “boxing gloves” at the end. Then, pedipalps loaded, he wanders off in search of a female to woo and donate his sperm to. Although the sperm is produced by a pore in his abdomen, the business ends of his sex act (so, his genitals) are in his pedipalps. (Next time you watch a Spider-Man movie, imagine a more realistic substance shooting from those gloves.)

Using such replacement genitalia occurs quite a lot in spiders, mites, crustaceans, millipedes, dragonflies, and damselflies, and several other kinds of animals. Frankly, we don’t really understand why or how this came about. Many of those still retain their original genitalia but have stopped using them as such, promoting other body parts to that position. And to end this chapter with a bang, I will give you two stories of animals that have taken substitute genitalia to new heights: cephalopods—the group of mollusks that includes octopi, squid, and cuttlefish—and velvet worms.

Story 1: Calamari Coition

In June 2012, one of those strange-but-true news items rippled across the world to be grossed out at briefly and then forgotten: “Woman, 63, Becomes PREGNANT in the Mouth with Baby Squid After Eating Calamari” was one of many similar headlines in the newspapers. What had happened?

Immediately after eating a mouthful of parboiled squid at a South Korean seafood restaurant, a customer had been rushed to the doctor with “severe pain in her oral cavity.” There, twelve squid sperm packages, or spermatophores, were found embedded in her tongue, inner cheek, and gums. Apparently, as a posthumous attempt at cephalopod-human hybridization, the (male) squid that she had eaten had ejaculated a bunch of his spermatophores into her.

The medical experts studying this case (and newspaper readers across the world) were stunned, but to somebody familiar with squid reproduction, it came as less of a surprise. José Eduardo Marian of the University of São Paolo in Brazil is one such expert, and as he writes in a 2012 paper in the journal Zoomorphology, there are in fact at least sixteen similar cases in the medical literature, most from Korea and Japan, where eating raw or blanched squid is common. To Marian, that a dead male squid can still ejaculate and have his sperm packages lodge themselves into a person’s mouth is not unexpected, given that these spermatophores, as he writes, “function autonomously and extra-corporeally.”

Squid spermatophores are intricately constructed flask-like things of less than a millimeter (0.04 inch) ranging up to tens of centimeters (about 10 inches) long, the latter being found only in giant squid. Composed of several layers of membranes (some of which are tightly coiled and under tension), a bag of sperm, sticky material, and, in certain species, abrasive spikes, they are nothing less than spring-loaded sperm grenades. All the male does is ejaculate them and then deposit them in or on the body of the female. Once there, either triggered by the sea water or by the friction of leaving the male’s penis, the spermatophores self-ejaculate—yes, the ejaculate can ejaculate! The outer membrane bursts, the spring unleashes itself, the abrasive spikes cut a hole, and the sticky cement helps to secure the payload to the female’s skin. Or to a diner’s oral epithelium, for that matter. In fact, as Marian points out, much of what is known of the way squid spermatophores function is thanks to the steady supply of samples embedded in human tissue collected by Japanese and Korean emergency rooms.

The point is: the female squid does not have a vagina as such. Depending on the species, the male may deposit his spermatophores around her mouth, on her back, her arms, or inside her mantle—the rubbery mitten-shaped covering of a squid or cuttlefish that we humans cut up in rings, deep-fry, and eat as calamari. From there, when the eggs are laid, the sperm find their way to them on their own, although the females of some species store sperm in special pockets around the places where the spermatophores are normally stuck.

And not only do squid females lack a vagina, squid males lack a penis. Or rather, they do have a penis, but they don’t use it as one. Let me elaborate. Most squid eaten in restaurants around the world belong to species in which the males have only a very short penis, too short to reach out of the mantle opening underneath the squid’s “neck.” So how do they manage to place spermatophores so precisely on, for example, the rim around a female’s mouth? For this, they normally use one of their eight arms, one called the hectocotylus, which is specially adapted for handling spermatophores. (It often has a special groove and folds, and lacks suckers along part of it.)

A spring-loaded sperm grenade. The sperm package of squid can self- detonate, which causes the sperm payload to be propelled and stuck to the body of the female.

During mating, when male and female squid are locked head-to-head, arms grappling in bliss, the male reaches with his hectocotylus inside his own mantle and produces the spermatophores, which his penis has just released, and places these in or on the female. So, in fact, and according to Eberhard’s definition, the hectocotylus—not the penis—is the actual genital organ, since it is what delivers the sperm to the female.

In one special group of cephalopods called argonauts, the hectocotylus even takes on a life of its own. Argonauts, or paper nautiluses, are mysterious octopi that live virtually unstudied lives in the open ocean. From what little we do know about them, it is clear that the seven species of argonauts are in many ways among the strangest of cephalopods. To begin with, the females—translucent, purplish, and bluish spotted—are octopus-sized, but the males are tiny: usually just 1 or 2 centimeters (0.4–0.8 inch) long. Also, the females have two webbed arms that are so large that the great Linnaeus, who named the first argonaut species, Argonauta argo, thought they held them up above the water surface as sails (hence the name, after the mythical ship Argo and its sailors). Not so: the female uses these arms to fashion a paper-thin shell that is the spitting image of the kind of shells that were once produced by the extinct ammonites. And herein lies yet another argonaut oddity: in contrast to all other mollusks, the argonaut shell is not attached to the body. Instead, the female lays her eggs in it, keeps it buoyant with bubbles of air, and guards it until her babies have matured.

But before eggs are laid, copulation needs to take place. And argonauts’ copulatory habits are unorthodox even for a cephalopod. A male argonaut has a very large hectocotylus, to which it attaches his spermatophore. That, as we have seen, is nothing out of the ordinary in the cephalopod world. But the male argonaut mates only once in his entire life. He has no choice, because during mating he detaches his entire hectocotylus, which then autonomically wiggles its way into the female’s mantle cavity and stays there until she lays her eggs. Sometimes, a female hosts several of such live hectocotyli, from multiple sexual encounters. In fact, the argonaut hectocotylus is so strange looking, with a head and a tail, that the French zoologist Georges Cuvier in 1829 mistook it for a parasitic worm and gave it the scientific name Hectocotyle octopodis. Although later scientists discovered its true nature, the name stuck, and hectocotylus is now the name used for the male sexual arm—in effect, his genitalia—in all cephalopods. And it is likely that that customer at the South Korean seafood restaurant had already swallowed her squid’s hectocotylus before her mouth was impregnated by his spermatophores.

Story 2: Blue Velvet

Back in 1883, one hundred pounds sterling was a lot of money, especially when spent on a grayish worm-like creature living out in the South African Cape. And yet that is what the British Royal Society paid zoologist Mr. Adam Sedgwick to seek out the animal, then known as Peripatus, and bring it back to England for study of its reproduction. They had good reason to want to study these creatures. Since their discovery in the 1820s, the mysterious Onychophora, or velvet worms, as we now call them, had fired the imagination of zoologists. With their thin, soft, knobbly skin of chitin and their system of tubes to transport oxygen through the body, they resembled insects and their relatives, but their numerous stubby legs and the rings that divide their 2-to-10-centimeter-long (1-to-4-inch-long) bodies made them look more like annelid worms. Even more fascinating was the fact that the females give birth to live young, which they gestate for more than a year in something that suspiciously resembled the uterus of mammals, placenta and all.

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.

US

Additional information

Dimensions	0.6800 × 5.5000 × 8.4000 in
Imprint	Penguin Books
ISBN-13	09780143127062
ISBN-10	0143127063
Author	Menno Schilthuizen
Audience	General / adult
BISAC	NAT001000, SCI056000
Subjects	human body book, wildlife, science books, nature books, physiology, science gifts, nature lover gifts, gifts for animal lovers, animal book, NAT001000, science book, natural history, animal lover gifts, science gifts for adults, science books for adults, anatomy book, anatomy and physiology, biology gifts, biology book, anatomy books, biology books, SCI056000, environment, anthropology, animal, nature, psychology, cats, science, education, health, biology, school, parenting, Animals, Dogs, Sociology, Food, animal books, pets, human body, reference, anatomy