Sex on Six Legs Read online

  A Good Year for Sons

  ALTHOUGH on average the number of men and women is roughly equal, the availability of either sex depends on the situation. You will be more likely to find a single man in a bar in Alaska, more apt to meet women at a convention for nurses. As it happens, these concerns about the sex ratio among humans also affected the development of another major theory about sex ratio in nature itself.

  It all started when Bob Trivers, the biologist who worked out the ratios of reproductive individuals expected within ant colonies that I discussed above, was a graduate student at Harvard. Trivers was a teaching assistant for a popular course in primate behavior, and as he relates in his collected papers, he had a mathematics student named Dan Willard who took the course as a way to meet women. The math graduate program at Harvard, as elsewhere, was rather like the aforementioned Alaskan bar in terms of its sex ratio (I assume, without really knowing, that the resemblance stops there), but the primate behavior class of nearly three hundred students was about two-thirds female. Trivers never divulges whether Willard's social hopes were fulfilled, but after a lecture about why the sex ratio is usually 50:50, Willard came up with an idea that the two of them later published as a highly influential paper in Science.

  Like many keen insights, this one seems simple once you hear it. Having offspring is costly, in the sense that it requires energy from the mother to produce eggs or babies. And as pregnant women the world over are acutely aware, the condition of the mother affects the condition of the baby, often for a long time after birth. Even among insects, better-nourished mothers can often produce larger eggs that in turn develop into more robust larvae. Although of course it would be ideal to always be in the best shape possible and produce the highest quality offspring a mother can, the situation doesn't always allow mothers to be in that tiptop condition.

  Trivers and Willard reasoned that the consequences of producing a baby that is of less than optimal condition will differ depending on the sex of that baby. Because males in many animal species compete vigorously for mates, only males of the highest quality are expected to be successful in fertilizing a female. Producing a weakling son is therefore unlikely to yield any reproductive payoff for the mother. On the other hand, if one's son is very successful in combat with other males, he can potentially sire many more offspring than a single female, even one in the best condition. Even a daughter in poor condition, however, will almost certainly find a mate and reproduce. So Trivers and Willard predicted that when circumstances keep the mother from pouring a lot of resources into her offspring, she would be more likely to have daughters than sons, and vice versa for mothers lucky enough to be at the top of their game.

  The mechanism behind such a sex bias is not entirely clear. No one, least of all Trivers and Willard, suggests that animals alter the usual method of chromosomal sex determination. But many more eggs are fertilized than end up implanting in the uterus or developing into offspring, and it is possible that embryos may be selectively retained or discarded depending on the mother's condition. This does not require a conscious decision on the part of the mother, of course, but selection may have favored implantation of a male or female egg only if, say, her hormone levels reflect a particular level of nutrition.

  The Trivers-Willard effect has been demonstrated in a wide range of animals, from deer to fish to birds, and may even operate in humans. A 2008 study of 740 British mothers found that the women were more likely to give birth to a boy if their diets were more nutritious around the time they had conceived. The bias was not huge—56 percent sons among the mothers that ate the most, versus 46 percent sons among the least-nourished women—but it suggests that more than chance may play a role in the sex ratio even in our Western societies. These insights in humans wouldn't have come about if we hadn't had insects, with their wildly variable lives, as test cases.

  Insects do not become pregnant, of course, although some retain the eggs inside or on the mother's body after they are produced. Furthermore, among many insects, large females are favored by natural selection because they can lay more eggs. Good conditions might be expected to cue the production of daughters, rather than sons, to take advantage of the resources necessary to manufacture a robust future mother. Indeed, among many parasitic wasps and flies, the sex ratio is biased toward daughters when the host maggot or caterpillar is large, and toward sons when the host is puny and provides less nourishment for the growing parasites.

  Finally, the sex ratio in some insect species can fluctuate wildly, even over the course of a very short time. A Polynesian butterfly had only 1 percent males in 2001, due to an infection by bacteria that selectively kill male embryos. But just 5 years later, researchers found a nearly 50:50 sex ratio on some of the islands where the butterfly occurs, even though the bacteria were still present. Selection apparently acted to reduce the male-killing ability of the bacteria, probably because producing males was enormously advantageous in the highly female-biased populations.

  See what you miss if you assume that Jerry Seinfeld makes a good bee?

  Chapter 5

  Sperm and Eggs on Six Legs

  DO YOU suffer from fertilization myopia? Just when you thought you'd heard of all the latest trends in maladies, from attention deficit disorder to cyberchondria (looking up dire diagnoses online at the first sign of a sniffle, in case you didn't know), here comes a new condition to worry about. Luckily, although many of us do, in fact, show signs of fertilization myopia, it can be cured without a single infomercial-shilled medication. All that's needed is a better understanding of insect sex, which might also help us understand sex in other creatures along the way.

  Fertilization myopia is a term coined by Bill Eberhard, a biologist who works in Panama and Costa Rica on a wide variety of spiders and insects. For the last twenty years or so, Bill has been intrigued—some might say obsessed—by animal genitalia and the finer details of insect mating. Despite what you might think given this predilection, he is a gracious and genial man and is married with children. He just happens to have an abiding curiosity about the natural world and an unwillingness to accept the conventional wisdom regarding mating behavior.

  Until quite recently, that conventional wisdom held that once a male and female mated, from an evolutionary perspective, it was all over. Sperm had been transferred, and now all that remained was to wait for the offspring to appear and carry on their parents' genes. Fertilization was the goal, and we didn't look beyond it. Even in humans, people assumed that the exciting part was the lead-up to sex: the partner choice, the foreplay, the act itself. The aftermath was just an ignominious anticlimax (so to speak) of damp sheets and flaccid organs. Pregnancy may or may not result, but there was nothing anyone could do to influence its likelihood once the deed was done. Arguments about how he wanted to roll over and sleep while she was still wide awake and needing to cuddle notwithstanding, postcoital activity just didn't get a lot of press.

  In insects, however, and maybe in many other animals as well, fertilization is far from the end of the mating story. Many insect females, from butterflies to beetles, mate with more than one male in succession before they lay their eggs. This fact had been well known among biologists, but it wasn't until 1970, when Geoff Parker at the University of Liverpool wrote a landmark paper about what he called "sperm competition," that the consequences of such multiple mating began to be fully considered. Parker pointed out that while male competition for females is more commonly associated with the more flamboyant battles between bull elk or elephant seals, it could still occur after copulation has occurred. The males just continue to vie for the prize of siring offspring via the one-celled messengers of themselves they leave as a consequence of mating: their sperm.

  The process would, Parker recognized, lead to different kinds of selection on males. On the one hand, male attributes that allowed their sperm to win at fertilization by circumventing the efforts of other males' sperm would be favored by selection; on the other, males that could prevent a fem
ale from mating with another male in the first place would do well because they would avoid the whole problem from the start. Insects are ideal candidates in which to observe such postmating activity because the females of most species mate with more than one male, often in rapid succession, and because in many insects females have specialized organs that serve as holding tanks, keeping the sperm in reserve until it is used to fertilize the eggs hours, days, or even weeks later.

  The idea of sperm competition appealed to biologists, most of whom, at least at the time of Parker's insight, were male. Numerous mathematical models about the conditions under which a given male's sperm might be favored were developed, and the details of sperm structure in various species—which turn out to vary enormously, as I will explain later—were examined. But other scientists, including Bill Eberhard, pointed out that this emphasis on male competition missed the other half of the equation: the female. After all, it was the female that did the multiple mating that allowed sperm from more than one male to be in the same place at more or less the same time, and it was the female's body in which all the action occurred. Not to mention that the female too has a stake in which male sires her offspring.

  So Eberhard and others suggested that females could influence the likelihood that a given male actually fathered her offspring, even after he had done the deed. This biasing of paternity after copulation is called cryptic female choice, a term originated by Randy Thornhill at the University of New Mexico. It is cryptic because it takes place out of view, inside the female's reproductive tract. Eberhard went further and pointed out that among insects and spiders at least, we should see that females control much of what happens in reproduction, and that we should stop focusing so short sightedly on that moment when sperm meets egg. In true infomercial fashion, we should wait, because there is more. Much, much more. The musician Björk said, "Football is a fertility festival. Eleven sperm trying to get into the egg. I feel sorry for the goalkeeper." One could, of course, take this the other way and point out that in fertility, both the goalkeeper and the players, not to mention the playing field itself, have a great deal to do with the outcome of the game. It isn't enough to just throw the team onto the field and wait for a goal.

  Chemical Genitalia and an Embarrassment of Riches

  MY GOOD friend and colleague Leigh Simmons claims that you don't understand life unless you have studied dung flies, preferably by actually coming into close contact with the substance that the flies call home. "Buckets of dung," he says cheerfully. "You need to really get your hands in it." Despite the numerous other likes and dislikes we share, I have never been convinced about this one enthusiasm, but I will concede that an understanding of sex in dung flies is crucial to an appreciation of what can happen after sex but before the production of offspring.

  As the name suggests, dung flies use cow or other animal droppings as a nursery in which to raise their young, and during summer, the female flies of one well-studied species, the yellow dung fly, seek out the freshly produced pats in meadows all over northern Europe. Once they arrive, they are immediately pounced upon by the males, which have been performing surveillance flights on the dung. As Leigh puts it in his book Sperm Competition and Its Evolutionary Consequences in the Insects, "On capturing a female, males will begin to copulate immediately. Struggles for the possession of females are intense. Searching males will pounce upon copulating pairs, with the result that large balls of golden flies can be seen tumbling about the dung surface while the object of their desire is pushed and pulled in all directions; sometimes females are drowned in the dung surface or otherwise injured to the extent that they can no longer fly. When the density of males on and around pats is high, a male capturing an incoming female will carry her in flight to the surrounding grass to copulate before returning her to the dung to lay her eggs. During oviposition [egg-laying] the male remains mounted upon the female and pairs separate only after a clutch of eggs is laid."

  Aside from making it clear that my friend is a man who truly loves his subjects of study, this lyrical description points out several crucial aspects of dung fly romance, and hints at why thinking outside the fertilization box will be illuminating. First, why would the males bother to take the females away from the melee before mating with them? Second, why bother staying while the female lays her eggs, which occurs after the male has deposited his sperm? And finally, why should mating take over half an hour, a seemingly excessively long time for the simple act of sperm meeting egg?

  The first person to try to answer these questions was Geoff Parker, who in addition to being an evolutionary theorist is something of a dung fly devotee himself. He and others established that the males' behavior helps their sperm to compete with the sperm of any other males with whom the female mates. The last male to mate with a female typically fertilizes most of her eggs, particularly if he can stay engaged with her for at least 30 minutes and displace the sperm of her previous mates. This means that time spent hanging around the female or sequestering her from other males is time well spent, even if the male isn't actively engaged in transferring sperm.

  After Parker's pioneering work, biologists threw themselves into an examination of the fate of sperm after mating, and hence into a scrutiny of the male organs themselves. There is nothing like a view of the genitalia of insects to convince you that the male equipment in human beings is rather dull and pedestrian in its appearance. In contrast, male damselflies have penis equivalents that boast a terrifying array of spikes, scoops, and hooks. The humble chicken flea has genitals bristling with strange knobs, kinks, and coils that Eberhard calls "one of the marvels of organic engineering," citing its "morphological exuberance." We never see these organs because the insects themselves are so small and their private parts are often held inside the body until they are needed, but similar well-cloaked monstrosities lurk in most insects.

  What these elaborate structures do, more similar to the function of antlers on elk or the curving horns of bighorn sheep than to the genitals of many other animals, is fight with other males. The battles, however, take place while one opponent is completely absent, and the scoops and spines serve to remove a prior mate's sperm from the female's reproductive tract so that it can be replaced with the current male's ejaculate. Exactly what kinds of tools are needed depend on whether the rival's sperm is to be scooped out, poisoned, or merely drowned by a larger number of sperm. In some species, a male tamps down the sperm from previous matings, rendering it less accessible, before overlaying it with his own.

  Sperm competition can also occur via the sperm itself and the chemicals that accompany it in the semen. Although they occur in many, perhaps all, insects, these chemicals have been best studied in the fruit fly Drosophila, which produces substances accompanying sperm that can kill the sperm of previous mates. These accessory proteins, as they are called, also influence the female's sexual behavior, sometimes rendering her less receptive to future matings, sometimes decreasing her overall life span but increasing the number of eggs she lays that are sired by her latest mate. Eberhard and his colleague Carlos Cordero call these seminal products chemical genitalia, because they can be seen as extensions of the more conventional physical reproductive organs. We are only just beginning to understand their complexity; Tracey Chapman from the University of East Anglia in the United Kingdom, in an article titled "The Soup in My Fly," referred to the bewildering diversity of seminal proteins as "an embarrassment of riches," surely the first time this phrase has been used in the context of sperm. At least 133 different substances have been identified, with doubtless more to follow. Whether each has a different function remains to be seen.

  All else being equal, the more sperm that are present in an ejaculate, the more likely the male is to win at sperm competition, simply by overwhelming the prior male's efforts. In the Pieridae, a family of butterflies that includes the familiar cabbage white butterfly, ejaculates are significantly larger than in a family in which females are less likely to mate with multiple males, the
ironically named (at least in this context) Satyridae. In insects, as in humans, sperm are produced in the testes, though insects generally lack external testicles housing the male organs. The larger the testes, the more sperm a male insect can produce, and you would therefore expect that sperm competition would cause the testes of species more likely to mate with multiple partners to evolve to a larger size than those in comparable but more monogamous species. That's exactly what was done by dissecting and weighing the testes in different types of Satyrids, and as expected, the greater the likelihood of females mating with many different males, the larger the testes relative to the size of the body.

  Recently, sperm competition was actually experimentally shown to influence the evolution of testes size, not just indirectly via comparisons of species, in some elegant work by my friend Leigh Simmons and Paco Garcia-González, a Spanish scientist working in Leigh's laboratory at the University of Western Australia. Leigh has continued in the manure-inspired vein begun with the dung flies by performing pioneering research on dung beetles, those indefatigable insects that tidy up the world's ecosystems by removing the droppings of large mammals and using them to provide an all-purpose larder and nursery for the offspring. Many types of dung beetles occur all over the world, and in some species the males possess large horns used in combat with other members of their sex to gain access to underground tunnels excavated by females. Larger horns make it easier to win fights, but as with many insects, the sexual competition is not over after the physical battle is won. Some males sneak into the burrows of the winners and mate with the females behind the resident's back, as it were, and the only recourse of the former winner is to mate more frequently with the female.

  One of the many obliging characteristics of dung beetles from the perspective of the scientists who study them is the ease of obtaining the raw material, so to speak. Leigh and Paco simply turn up at a local dairy farm and ask the farmer's permission to rummage around in the droppings left in the pasture, permission that is virtually always granted, albeit not without some quizzical looks. It is always difficult under such circumstances to decide exactly how much one should explain about the reason behind the request, striking a delicate balance between Too Much Information ("Here, let me tell you all about the evolution of male genitalia in beetles!") and sinister-seeming reticence ("Oh, nothing special, really. I'm doing a project on, um, sex."). From long experience, Leigh has figured out how to make such requests without alarming the farmers, and he and Paco duly brought back about a thousand beetles to his laboratory.