Nature's Nether Regions

by Menno Schilthuizen

  But as dung flies are only the size of dung flies, and what with their scatological tendencies, they adorn only the pages of niche journals like Ethology, Evolution, the Journal of Evolutionary Biology, and Behavioral Ecology and Sociobiology. And have done so in an uninterrupted series of scientific publications produced by Parker and his students for the past forty-five years. One of the things they found out is that a female dung fly possesses one large central sperm chamber, the “bursa copulatrix,” and three smaller “spermathecae,” each one connected to the bursa via a long, narrow duct. Two of these spermathecae lie on the right-hand side of her abdomen, while the third one lies on the left. In 1990, Parker’s former Ph.D. student Paul Ward set up a dung fly lab at the University of Zurich in Switzerland (where the hills are alive with the hum of dung flies). And in the twenty years up until his untimely death in 2010, Ward’s work showed that female dung flies can play these internal bagpipes with amazing finesse.

  In the lab, Ward let female dung flies copulate for twenty minutes with one or two males. Then some of the females were allowed to lay their eggs on nicely measured bits of cowpat in petri dishes, after which Ward checked which larvae were fathered by which males; this was possible because the males had been bred to contain different gene mutations, by which their offspring could be recognized. The other females were killed after mating and then dissected so that Ward could count the number of sperm cells in each of the spermathecae. What he found was that a female prefers to store more sperm from a large male—which Parker had shown to be more attractive to females—than from a smaller male. She also stores large-male sperm preferably in one or both of the spermathecae on the right, rather than spread evenly across all three, as she tends to do with small-male sperm. And Ward also discovered that when it’s time to lay eggs, the female would preferentially squeeze sperm from her right-hand spermathecae, so that the big guy would father most of her babies.

  Female discretion. Internally, a dung fly has three spermathecae for keeping sperm from the males she has mated with. The paired spermathecae are reserved for “sexy” males; the single spermatheca is a backup for sperm of lesser quality.

  Later, when genetic fingerprinting techniques were developed for dung flies, Ward’s team was even able to extract the sperm from the separate spermathecae and show that, indeed, these were from different males in different proportions. That all this sperm positioning was mostly the female’s work, and not influenced by the male, was proven in a cute little experiment done by two collaborators of Ward’s, Barbara Hellriegel and Giorgina Bernasconi. They divided just-mated females into two groups: some were left awake while others were put under anesthesia with carbon dioxide. They found that only the conscious females were able to create separate sperm stores, while the ones under narcosis spread the sperm randomly.

  So the yellow dung fly is the last in a long series of organisms that teach us that females in the animal world have a wide variety of tricks up their sleeves to determine which sperm is going to get access to their eggs. Not only can a female enforce dry copulation on her mate and give him the slip before his apogee, she can also dump or eject his sperm, or use internal valves and locks to keep unwanted sperm away from her eggs. Even when she accepts a male’s sperm, she can store it away in a safe location and decide later whether or not to use it. And the list does not end there. Even after they have fertilized their eggs with a male’s sperm, some females can, as a last resort, deny their embryos the opportunity to come to term. Such drastic measures, used by some female mammals to favor certain males over others, are known as the “Bruce effect.” Rather disappointingly, the term does not refer to a disinclination in women to have their babies fathered by the kind of men who are called Bruce. Instead, it is named after Hilda Bruce, the English zoologist who revealed it in 1959.

  The dramatic phenomenon was discovered quite by accident. Bruce, who was studying the effect of hormone supplements in lab mice, noticed that a pregnant female mouse would sometimes miscarry when she was introduced to a new male, and would instead conceive an entire new litter from this novel mate. Since then, zoologists have found the Bruce effect in many other lab animals, especially rodents, and the cue from the new male that induces the female to give up on her existing pregnancy differs quite a bit. In the woodland vole, Microtus pinetorum, for example, the trigger is in the male odor, but in the field vole, Microtus agrestis, mere physical contact with a strange male can induce abortion. In the meadow vole, Microtus pennsylvanicus, finally, a female would abort and reovulate only once she had actually copulated with a new male.

  For a long time, the Bruce effect was seen only under very unnatural laboratory settings, and many a zoologist wondered aloud whether it was a natural phenomenon at all or just a quirk brought about by the highly artificial conditions in a laboratory. But then, in 2011, it was also discovered in the wild. Zoologist Elia Roberts, who spent many years studying wild troops of geladas (a relative of the baboon) in Ethiopia, found the telltale sign of a natural Bruce effect in her geladas’ feces. By measuring the level of estrogen in the droppings from particular females, she could tell if they were pregnant, and, when a sudden and permanent drop in the estrogen level occurred, that they had aborted. In almost all cases where there was such a premature abortion, this happened immediately after the troop of the female had been taken over by a new alpha male.

  Now, the Bruce effect as we know it is probably an adaptation to the sad reality of infanticide. The males in many of the species in which the phenomenon has been found have the habit of killing any offspring of their mates that wasn’t sired by themselves. In geladas, whenever a new male ousts the resident alpha male, the first task he sets himself is to execute all the juveniles fathered by his predecessor. So if the new male is going to kill her babies anyway, a female can invoke the Bruce effect to save time and energy wasted on a doomed pregnancy.

  However, the Bruce effect might also signify a more general ability in female animals to terminate pregnancies at will. In many mammals, miscarriages are very common. In humans, it is thought that up to two-thirds of pregnancies abort spontaneously, often without the woman being aware that she was even pregnant. The majority of such abortions are probably due to the female body screening for serious genetic defects in the fetus, but there are more subtle mechanisms. For example, both pig-tailed macaque and human females miscarry more often if their mates have immune systems that are very similar to their own. Again, this is probably a strategy evolved to maximize a baby’s disease-fighting ability—inheriting different immunity tools from both parents is better than inheriting the same set from both—and it is also not clear whether such abortions are triggered by the male or by the fetus. Still, these are intriguing indications that females could summon abortion as a last-resort effort to deny certain males their reproductive chances. (Counterintuitively, the phenomenon is misappropriated by some antiabortionists with the tortuous reasoning that if a woman’s body can abort naturally, we should not do it artificially.)

  To sum up, the female is anything but a passive sperm receptacle that nurtures the life breathed into her eggs by the males that dignify her with their semen. Instead, her body harbors a varied arsenal of ways to peeve her partner. It is a highly sophisticated engine of preference that springs into action upon each coitus. Taking cues from the male and his “courtship device,” it winnows semen, rejects or selects sperm, and works its internal valves and springs like a mail-sorting machine. As we shall see in the next chapter, it is this intimate interaction between male and female genitalia that is the driving force for their unpredictable evolutionary trajectories. But we shall also see that there are limits to what this force can achieve.

  Chapter 5

  A Fickle Sculptor

  Roughly speaking, biologists come in three flavors: field, lab, and theoretical. Those biologists who are happy only when they can don a raincoat, put a pencil and notebook, binoculars, hand lens, and collecting jars in
an old military bag, and walk off into the wild clearly belong to the former kind. Lab biologists find the great outdoors a much too confusing place and prefer to parcel biological processes into nicely contained simple systems in petri dishes. And then there are the theoretical biologists, for whom even a fruit fly in a lab bottle is way too unpredictable. They forsake real life altogether and instead capture it in formulae on paper and strings of computer code.

  Famed sexual selection researcher Andrew Pomiankowski of University College London snugly fits in the latter category, having authored papers with titles like “The Costs of Choice in Sexual Selection” (1987), “Why Have Birds Got Multiple Sexual Ornaments” (1993), and “A Resolution of the Lek Paradox” (1995)—all highly influential but also highly devoid of actual animals or observations. Instead they are chock-full of formulae and computer simulations, with opening sentences like “Let t be a male trait used by females in mate choice and p be the strength of female preference.” Still, even theoretical biologists understand that the market value of their theories increases if they can be applied in the lab and in the field, which is why, since the late 1990s, Pomiankowski has been testing his work willy-nilly on animals in the wild. And that explains why, several years ago as I lived and worked in Borneo, I received an e-mail from him asking me to take him a-hunting for stalk-eyed flies.

  Stalk-eyed flies, or Diopsidae, are among the weirdest insects you can find in the Tropics. Immediately after emerging from the pupa, when the outer casings of their bodies are still soft and pliable, both males and females (but especially males) inflate and extend the struts that their eyes sit on, and these harden into enormously elongated stalks, which they then fly around with for the rest of their lives. It is the culmination of aeons of females preferring males with eyes that stand far apart. In the most extreme cases, such as the species Teleopsis belzebuth from Borneo, the flies have evolved an eyespan that is a whopping two and a half times the length of the body—headgear that is the insect equivalent of the peacock’s tail: cumbersome, extravagant, and very much sexually selected.

  As in peacocks and other pheasant-like birds, mating in stalk-eyed flies takes place in so-called leks (the Swedish word for “game” or “play,” Scandinavia having been the epicenter for sexual selection research for many years). Leks are a kind of love-in where groups of males and females congregate and where the latter choose from among the former and copulate with them. Stalk-eyed fly leks crop up at dusk on the tiny twigs and root hairs that stick out from the eroded banks of streams in tropical forests. So as the sun was setting over Malaysian Borneo one late afternoon in April 2006, I found myself clutching the spongy stems of wild yams and stumbling over loose branches and boulders, while slip-sliding down a steep slope in the company of Pomiankowski and my friend the tropical ecologist Stephen Sutton. We eventually reached the stream and, still a little unsteady, began aiming our headlamps at the muddy rootlets that Andrew had said might contain the fly leks. And so they did: here and there, congregations of the nimble flies revealed themselves, jerkily moving up and down their root hairs with their ridiculously wide eyestalks sticking out on either side, like tightrope artists carrying balancing poles.

  The work of Pomiankowski and his collaborators has shown that each lek is controlled by a single male. Females prefer to alight on root hairs tended by the males with the largest eyespan. Laboratory studies proved that the eyespan a male can attain is genetically determined but that it also says something about the male’s quality as a mate: males can develop large eyespans only if they have coped well with the toils of larval life, and long-eyed males also have larger testes that produce more sperm, and so are able to fertilize more eggs in one copulation.

  As we saw in Chapter 3, when we talked about the sexual selection by females of males with exaggerated adornments, this amply explains why eyespan should keep increasing in a stalk-eyed fly species. Males with longer eyestalks get to mate more often and thus sire more offspring, and those offspring inherit not only the genes for long eyestalks from their fathers, but also, from their mothers, the genes that make females like long eyestalks—leading to the species snowballing evolutionarily into ever greater stalk length. But there are complications, and these are the ones that Pomiankowski has been tackling in his computer models. For example, why do some species have longer eyestalks than others? And what happens when eyestalk evolution finds itself in the dead-end alley where all males have the longest possible eyestalks and all the females have maximum preference for this, an evolutionary gridlock known as the “lek paradox”?

  What Pomiankowski, together with his colleague Yoh Iwasa from Japan’s Kyushu University, was able to work out is that such sexual selection is not a one-way street. In the evolutionary history of any stalk-eyed fly species, there may come a point where all males have the maximum attainable eyespan—any longer and they will no longer be able to fly or their eyes will simply snap off—and all females find this as thrilling as their tiny fly brains are capable of. But once this state of affairs is reached, the benefit of choosing disappears, since all males have become the same. This means that evaluating and choosing males—the whole business of lekking—has now become a waste of time and energy for the females. The result is that mutations that make females less choosy will suddenly confer an advantage, and, as Pomiankowski and Iwasa witnessed on their computer screens, such a population could actually start evolving to have shorter and shorter eyespan. In fact, they found that once they simulated several genes for male eyespan and for female preferences, a population would never stabilize and would continue to bounce around the edges of eyespan and eyespan preference space for the rest of its evolutionary life.

  In this evolutionary restlessness lie the greatest differences between natural and sexual selection. Natural selection, where a species adapts to, say, soil type or temperature, has a single optimum. Soil and temperature tend to stay more or less the same over long periods of time and do not change in response to organisms that adapt to them. There are no feedback loops, so over many generations a species will inch closer and closer to the best fit. But sexual selection is completely different. There is no single optimum that the species is evolving toward. Instead, the male half of the species is adapting to the female half and vice versa. The fact that both genders are tracking a moving target is already enough to guarantee perpetual evolutionary motion, and the combining, mixing, and redistribution of male- and female-adapted genes in each generation adds another layer of complexity. So sexual selection is the acme of evolutionary dynamism—and therefore much more complex and hard to predict than natural selection.

  Pomiankowski’s number crunching to figure out the evolutionary tango of male and female stalk-eyed flies is just one example of a process in sexual evolution so complex and hard to predict that we need computer simulations to understand it. Another example is a phenomenon called the “rare-male effect.” In fish and insects, and probably in a variety of other animals, too, females sometimes prefer to mate with the most “unusual” males.

  Take guppies. As anybody who has ever kept these popular aquarium fish knows, guppy males come in an amazing range of genetically determined color patterns, made up of blotches and stripes of yellow, red, and black as well as patches of golden, green, or purple metallic sheen. And although in an aquarium you may find many different color forms in the same tank, in the Central American streams that are the native home of these fish, male color patterns are to some degree partitioned by watershed. In Trinidad, for example, the La Selva River houses a type of male prosaically called M7, which sports bright gold vertical bars on the base of the tail, a black spot at the base of the tailfin, and orange rims on the top and bottom of the tailfin. The M1 males from the nearby Guanapo River, on the other hand, have a white dorsal fin, a black bar on the tail base, and orange spots on the bases of the fins.

  In an experiment carried out at the University of California, Riverside, researchers showed groups of M1 or M
7 males to virgin female guppies from the Guanapo River. They set up guppy peep shows by dividing their fish tanks into male and female compartments with glass walls, so that the females could see (and be courted by) males, but could not actually mate with them. Then they took individual females out of the tanks and placed each of them with one M7 male and one M1 male and left these trios to sort out their sexual preferences in privacy for twenty-four hours, after which the female was removed and placed in her own aquarium to give birth to her young. Since the color patterns are genetically based, the researchers could easily see how many of each female’s fry had been fathered by the M7 male and how many by the other. The result was that females that had previously been around M7s were about three times less likely to have their eggs fertilized by these males than females who had never seen an M7 before. Familiarity had bred contempt.

  This rare-male effect, where females seem to prefer to mate with the new kid in town, is not unique to guppies. It has also been reported in many kinds of insects, where females prefer to mate with males with, for example, uncommonly white eyes (banana flies) or peculiar styles of courtship (crickets). But it is not entirely clear why females should so love a stranger. It might simply be the kind of sensory drive that we saw in Chapter 3: a female’s nervous system will fire up more eagerly when it is suddenly confronted with new signals it has not yet been numbed by. But perhaps more often it is a mate choice strategy that has evolved to prevent inbreeding: too much mating with relatives is dangerous for the offspring’s genetic health, so a preference for males that look as if they are not from around the neighborhood may be an advantage.