Nature's Nether Regions Read online

  Blushing is the most peculiar and most human of all expressions.

  —Charles Darwin, The Expression of the Emotions in Man and Animals

  Afterplay

  When Jonathan Waage published his groundbreaking 1979 Science article in which he described the damselfly penis gizmo, he received some laudatory media coverage. But one headline—he thinks it was in the National Enquirer—blasted, “University Egghead Wastes Taxpayers’ Money Studying Dragonfly Sex.” Thirty-five years of genitalia research since Waage’s landmark piece have not lessened the aim that certain media will take at its practitioners. In March 2013, the news network CNS derided the study on duck genitalia by Patricia Brennan and colleagues (Chapter 6) under a similar heading, leading to a two-week media mini-cyclone in the United States (outrage on Fox News; defense from National Geographic and Slate) that was quickly dubbed “Duckpenisgate.”

  It is easy to see why genitalia research is such an easy target (a sitting duck, almost) for those who wish to ridicule basic scientific research. Studying the finer details of the private parts of some inconsequential animal can effortlessly be cast in terms of frivolity beyond words. The reasoning would be a very effective double whammy of the following form: “Not only does nobody in the world, besides perhaps Patricia Brennan and her deviant colleagues at Yale, care about the exact shape of the genitals of the ruddy duck, but it also serves no practical purpose whatsoever—so public money should not be wasted on it!” No wonder 90 percent of the people polled by Fox News agreed with the latter conclusion.

  Some arguments can in fact be brought to bear against the notion that genitalia research has no application. At several places in this book, we have seen cases of human and livestock fertility problems that can be understood—and sometimes solved—only with a good command of the evolution of the genitalia involved. In Chapter 4, for example, we saw that artificial insemination in domestic animals is improved if the shape of the syringe used resembles that of the penis of the respective species; Eberhard wrote a paper in the journal Medical Hypotheses arguing that the same might be true for humans.

  The fact that that paper has been completely ignored by the medical literature (it has been cited exactly zero times since it was published in 1991) is symptomatic of the medical tradition of viewing human reproduction as a mundane bodily function, where both sexes are cooperating “for the good of the species,” and fertility problems are seen simply as defects in that function. It should now be clear that reproduction in any species is the outcome of a never-ending evolutionary tango, a dance marathon that conserves elements of both battle and ballet. And, as we have seen, gynecological and urological problems in humans, such as preeclampsia (Chapter 7), spontaneous abortion (Chapter 4), seminal allergy (Chapter 7), and pregnancy in noncommunicating uterine horns (Chapter 6), which physicians often tend to take for granted as unavoidable “errors,” can all be understood, and possibly better addressed, if we know the forces involved in genital evolution.

  Yet potential practical applications should never be given by genital researchers as the sole justification for their work. Like art, music, and sports, basic science exists to provide a form of entertainment for the rest of humankind. Evolutionary biologists do the hard, painstaking labor to find out and make sense of all the details required to tell true stories about the world we live in. Nature documentaries on TV, for example, are watched by hundreds of millions of people worldwide. They marvel at and are entertained by what they learn. What is often forgotten is that it is not the presenters who, panting their way through steamy tropical jungles and along precipitous cliffs, have discovered all the biological facts that they are dishing out to the viewer. Every minute in such a documentary is based on years of work by some anonymous biologist doing fundamental scientific research sometime, somewhere.

  By feeding (while at the same time being fed by) the deep-rooted human fascination with sex, genital researchers should have no problems getting the rest of the world to take them seriously. But therein also lies their weakness. For that deep-rooted fascination with sex is a curious beast. Since our genitals take up a strategic position in multiple strands of human emotion, we have always had a tumultuous relationship with our private parts. They pique our interest in a very urgent way, but they also are the seat of power and vulnerability in both men and women. It may well be that the curious mix of modesty and lewdness that results is an evolved aspect of human behavior that, in some ways, we share with our closest relatives. (Apes seem to know the special meaning of genitals, too. I have always been struck by Frans de Waal’s observation that when two up-and-coming chimpanzee males in a colony staged a coup against the incumbent alpha male, they did not throttle him or bash in his head, but instead chose emasculation.)

  Not surprising, then, that by drawing our attention to the origins, workings, and evolution of our and other species’ reproductive organs, genital researchers get both the gain and the pain from this double-edged sword. Communicating the science involved is easy, because people instantly prick up their ears, but curiosity can quickly turn to embarrassment. When in 2013 Scientific American reported, via its Facebook page, on Brian Mautz’s study on attractiveness of penis size in men (see Chapter 3), Facebook removed the (computer-generated) images for being too explicit.

  At the same time, genitalia research itself is not free from entrenched notions about genitals and sex. Throughout this book, I have pointed to an ongoing debate between two camps of genital researchers. One camp, headed by Bill Eberhard, emphasizes the importance of cryptic female choice (CFC) for the evolution of genitalia. Other researchers, like Göran Arnqvist, think that sexually antagonistic coevolution (SAC) has been the driving force for the biodiversity of genitals. The differences are subtle. If CFC holds sway, then genitalia evolve mostly because females pick the best males from among the available suitors. Even if these males play vicious tricks to manipulate the female, in the end it is the female who “selectively cooperates,” as Eberhard puts it, to provide her offspring with the best genes she can find. The SAC camp, on the other hand, sees genital evolution as going off down a vortex of male-female conflict over who has the final say in fertilization—with both parties suffering.

  It is hard to decide which camp is right. The only way to obtain hard evidence would be by comparing, under natural circumstances, the exact numbers of children and grandchildren and great-grandchildren—in other words, the total reproductive success—of females that mate with different types of males. If these numbers go down when females mate with many males, then that would be evidence for SAC; if they go up, CFC would have the best cards. But nobody “has ever come even close to producing reasonable data on this score,” according to Eberhard.

  Meanwhile, both camps accuse each other of falling victim to old, nonscientific, patriarchal stereotypes about sex roles. CFC adept Eberhard speaks of “cultural blinders” that unconsciously persuade SAC folk that sexual interactions are still more about males being active and females being passive. The SAC camp, on the other hand, points out that CFC people are too much penis-focused and often ignore the gynecology of their favorite species.

  The charge of penis staring and vagina neglect should certainly be taken to heart by the whole field of genital science. Partly for practical reasons (in insects, for example, the penis is usually made from chitin and retains its shape even in dried and pinned specimens, whereas the soft and pliable female genitals shrivel), penises have been favored and vaginas shunned. But there must also be a cultural bias, as we have seen from the struggle to get the human clitoris properly described, compared with the penis, which never had any trouble claiming a chapter for itself in the textbooks. As feminist evolutionary biologist Patricia Adair Gowaty has written, female genitalia, throughout biology, have suffered from being viewed as “more common than elaborate, more utilitarian than bizarre.” Yet, more often than not, whenever people have overcome the practical and cultural obstacles to ta
ke a good look at female genitalia (think of the ducks and rove beetles of Chapter 6), they appear to be just as peculiar and multiform as the male ones. In fact, in many types of animals (spiders, clown and featherwing beetles, sand flies, and moths, to name but a few) the female genitals are used for species identification just as the male ones are.

  Despite such shortcomings and biases, studying the evolution of genitalia has provided us with deep insights and spectacular panoramas on the history of life. When Bill Eberhard, as a young student, began flipping through arachnological monographs, what ignited his interest was that no other body part has been diversified by evolution as much as the organs directly involved in reproduction. The fact that genitalia are the acme of biodiversity in many kinds of organisms seems almost like a law of nature. But let us not forget the tenuous and contingent routes that have led to it.

  Somewhere in the deep folds of time, sex arose as a means to outrun fast-evolving viruses or help fix errors in the genetic code. Then a bacterium crawled into a primordial cell. To counter combat among cohabiting bacteria, separate male and female sexes, producing different sex cells (eggs and sperm), appeared. Rather than scattering these sex cells randomly in the currents, some organisms began packaging them in spermatophores and evolved genital organs to hand these to one another, setting the stage for sexual selection to wave its magic wand of cryptic female choice, Fisherian selection, and sexual conflict, and giving us the bewildering array of form and function that we see today.

  But there is more. The proteins that form the mating plugs of Chapter 7 are possibly the same ones initially used to build the casings of the spermatophores in the ancestors of these animals, perhaps even before genitalia evolved. Likewise, the cell-penetrating qualities of spermatozoa came in handy in those animals where traumatic insemination evolved, when it became necessary for sperm cells to penetrate more than just the outer layer of an egg cell. The fact that hermaphrodites produce female hormones as well as male ones preadapts them for the hormonal manipulation of their mates, as Joris Koene pointed out to us in Chapter 8. And, finally, there may be a finer line between the sperm dumping of Chapter 3 and the sperm scooping of Chapter 6. A male, during copulation, may be able to trigger the reflex that makes a female dump a previous male’s sperm, blurring the distinction between sperm dumping and scooping.

  Such contingencies and predestinations form a loose straitjacket for genital evolution. Loose because, as we saw in Chapter 4, within certain confines genital evolution is such a dynamic process that it can go off in all kinds of unpredictable directions, leading to great multiformity. At the same time, environment plays a much bigger role than just curbing the size of the genitals of mosquito fish and Tidarren spiders. I am writing this section while on vacation in Crete. Unlike most vacationers, I have spent some time looking at copulating beetles on roadside flowers. While the copulas of some species seem oblivious to the outside world and stay firmly locked together as I pick them up and put them under my hand lens, others separate and fly off instantly when disturbed. Perhaps the former kind are locked together by spines on the penis, and perhaps these could evolve because these beetles are toxic or for some other reason have fewer predators and hence are less vulnerable when caught in flagrante delicto. I would not be surprised if such evolutionary communications exist between a species’ genitals and the niche it lives in.

  Conversely, genital evolution may also be the driving force for the origin of new species. If it is true that male genitalia are constantly evolving to adapt to female genitalia and vice versa, then this dual adaptation could cause such splitting, so-called speciation events. In the substance-injecting seed beetles that we met in Chapter 7, for example, different species have different degrees of penis spininess and the vaginas are correspondingly thicker skinned, such that females of species in which the males have particularly spiny penises have more heavily armor-plated vaginas. Such mutual adaptations do not just happen in seed beetles that already belong to separate species; the same process also takes place in separate populations of the same species—for example, in the seed beetle Callosobruchus maculatus. Males of an Indian C. maculatus that mate with an African female are not very successful in the sperm competition with males from the female’s native population, and vice versa. Such mutual male-female adaptation taking place in each population separately could give rise to barriers to effective crossbreeding between populations, which can sometimes cause these populations to evolve into separate species.

  But that’s seed beetles. In the Preliminaries, I pointed out that there are striking differences between the genitalia of ourselves and our closest relative, the chimpanzee. And while I would not imply that the evolution of genitalia is the wedge driven between us and our primate brethren, it certainly has played its part in paving the evolutionary paths that these species have traveled over the past few millions of years. Throughout this book, we have seen tantalizing glimpses of that: penises that may have lost their spininess but have evolved shapes that help displace sperm, and female orgasms that select or reject semen from males, which, in turn, may be subtly modifying female physiology or even hampering other males’ semen.

  What I haven’t discussed—genital researchers haven’t even begun scratching the surface of it—is the possibility of homosexuality also playing its part in genital evolution. In mammals, including humans, this is likely to be relevant. For example, the glans of the clitoris in bonobos is larger and more forward pointing, an anatomical feature that some primatologists have linked with the fact that homosexual copulations among females (as well as among males) play an important social role in those apes. We have also come across the theory (in Chapter 6) that homosexuality in male bedbugs helps a male to sire offspring by proxy, via the male mate who then goes on to mate with females—if you can still follow. With homosexuality rife in the animal kingdom, it is likely that other ways exist in which same-sex mating may have an impact on genital evolution—none of which has yet been investigated by biologists.

  There is a vast ocean of sexual function beyond the quiet backwater that we humans find ourselves in, and much of what exists in other animals is extremely foreign to us: we would not be very happy if we were to live the sex lives of seed beetles, sea slugs, or cellar spiders. But what I hope to have shown is that humans do fit in. The ways in which the shapes and functions of our genitals have been molded by evolution merge seamlessly with the rest of the continuum, making us an integral part of nature. With all the animals we share this world with, we are descendants of an unbroken line of ancestors who, like that seventeenth-century couple inspecting a sperm whale penis, all agreed on the irresistible lure of sex.

  Acknowledgments

  I wrote this book partly at home, partly while traveling in different parts of the world. At home, I want to thank my partner, Rachel Esner, and my children, Fenna and Jan, for accommodating me and my writing-enhanced pensive moods at the kitchen table in Leiden, Amsterdam, Paris, and Kota Kinabalu—and Rachel for allowing me to muse on genitalia even more than I normally do. Abroad, unbeknownst to them, the staff of the following places helped nurse this book to life. In London, the Dana Centre, the Imperial College canteens, the Victoria and Albert Museum restaurant, and Mrs. Sue Crayson’s bed-and-breakfast. In the Azores, the Lince Hotel in Ponta Delgada. In Crete, the Marin Hotel and Morosini café in Iráklion (overlooking the city’s bustling lek), and in Doulianá, Filippa’s House. The whole of Chapter 6 was written in Ben Bankson’s apartment in Brooklyn, New York, and much of Chapters 1 and 2 in the apartment rented from Annette Ciré in Berlin.

  Then there are the many scientists (and the occasional artist and art historian), some of them friends, others colleagues, yet others fully unacquainted to me, who all freely donated smaller and larger bits of their time, offered advice and information, and in many cases hospitably allowed me into their labs, offices, and homes. In alphabetical order, those were: Gerd Alberti, Göran Arnqvist, Lisa Becking, Tim Bir
khead, Oskar Brattström, Maria Fernanda Cardoso, Satoshi Chiba, Bill Eberhard, Coby Feijen, Hans Feijen, Claudia Gack, John Grahame, Martin Haase, Peter van Helsdingen, Kasper Hendriks, Rolf Hoekstra, Michael Jennions, Kazuki Kimura, Joris Koene, Hanna Kokko, Bram Kuijper, Michael Lang, Martine Maan, Patricia Mainardi, Brian Mautz, Thibaut de Meulemeester, Peter Michalik, Jeremy Miller, Kees Moeliker, Nobuaki Nagata, Virginie Orgogozo, Antonella di Palma, Rich Palmer, Michel Perreau, Michal Polak, Andrew Pomiankowski, Richard Preece, “Theo” Michael Schmitt, Angela Schmitz-Ornés, Stephen Sutton, Gabriele Uhl, Jonathan Waage, and Paul Watson.

  Several friends have given advice and intellectual as well as mental support, especially, and in many, many ways, my partner Rachel Esner, but also Frank van Rooij (both proofread large parts of the draft), Jeroen Roelfsema, Janine Kourakos, Lydian ter Brugge, and Abigail Solomon Godeau. I would also like to acknowledge my colleagues at Naturalis Biodiversity Center, especially Kris de Greef and all the members of the focus group Character Evolution, my genitalia students Flor Rhebergen, Ruben Vijverberg, Thijmen Breeschoten, Paulien de Jong, Tamara Hoogenboom, Rick van Beek, and Melanie Meijer zu Schlochtern, and also my directors Jan van Tol, Koos Biesmeijer, Erik Smets, and Edwin van Huis, whose flexibility has allowed me to divert part of my time to this book project.