Nature's Nether Regions

by Menno Schilthuizen

  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.