Nature's Nether Regions

by Menno Schilthuizen

  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 dr
y 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.