Sperm and Eggs on Six Legs - Sex on Six Legs: Lessons on Life, Love, and Language from the Insect World - Marlene Zuk

Sex on Six Legs: Lessons on Life, Love, and Language from the Insect World - Marlene Zuk (2011)

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 female 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.

Leigh and Paco then performed what is called experimental evolution, by altering the environment of the beetles to see if the hypothesized selection pressure, namely, the risk of sperm competition, had the predicted effect on the beetles' testes size. It is really just artificial selection, the same process used to obtain do mesticated animals or crop plants with desired characteristics. The researchers set up populations of the beetles under different circumstances: monogamy, with a set of randomly chosen males and females paired so that there was no risk of competition among rival males; and multiple mating, with buckets containing ten individuals of each sex so that the males could jockey for access to the females. The offspring from each of the experimental treatments were then placed in the same situation as their parents, and so forth for twenty-one generations, which took about four and a half years, since a dung beetle can get from egg to adult in about eight weeks.

At the end of the experiment, the males in the monogamous treatment had smaller testes than those from the lines in which sexual competition had been allowed to continue. This was clearly a genetic response, not simply a "use it or lose it" effect of the treatment, because the beetles were measured just after they reached sexual maturity but before they had time to mate. Leigh and Paco could also use genetic analysis to determine exactly which males fathered the most offspring, and they found that when given the opportunity to compete, males from the monogamy lines were not as good at fertilizing the females' eggs as males whose ancestors had been allowed to mate in groups. They concluded that sperm competition drives the evolution of testes size and sperm viability in these beetles, just as the theory predicts.

A Funny Thing Happened on the Way to the Egg

AS I mentioned above, many of the early researchers studying sperm competition were men, and without delving too deeply into their motivations, it is safe to say that most of them did not consider the female's side of the equation. Once Eberhard and a few others got things started, however, it became clear that female insects did not simply lie around passively waiting for the sperm to duke it out inside their bodies. One of the best examples of cryptic female choice is found in the humble flour beetle, the same tiny pest that infests the canisters of flour and other grain products in your kitchen. Lurking inside these miniature creatures is a hotbed of reproductive intrigue.

Tatyana Fedina, now at the University of Michigan, performed some extremely clever—if grisly—experiments on the beetles when she was a graduate student at Tufts University to see just how much say the females had over the fate of sperm. Flour beetle males pass sperm to females in a tube that turns inside out once it is in the female's body. The beetles mate with multiple partners, and some males father more offspring than others. But who controls paternity? Is it the males, via sperm competition, or the females, via selective use of sperm?

Fedina took advantage of the rather oblivious nature of male flour beetles when it comes to sexual activity and allowed them to either mate as per usual, or mate with a freshly killed female, something they did quite readily. She also starved some of the males so that they would seem to the females to be of poorer genetic quality than the others, and then compared how many sperm were transferred to the female's reproductive tract. Not surprisingly, the food-deprived beetles were less successful at transferring sperm—but only as long as they were mating with a live female. Males mating with the dead, and hence incapacitated, females showed no difference in their ability to inseminate, regardless of their condition. This means that the female herself must be doing something to influence the father of her offspring, favoring the well-fed and presumably higher-quality males.

Other, perhaps not quite so ruthless, experiments used anesthetized female flour beetles to study the degree to which females can control the movement of sperm inside their bodies. The immobilization of a female's musculature caused changes in the number of sperm inside different parts of her reproductive tract, further supporting the idea that females are more than simply vessels for sperm. A similar experiment was performed using a small moth; when a female moth was mated to two males, the larger individual always fathered most of the offspring, regardless of the order in which the matings took place. Again, this bias seems to be due to the female's actions, because anesthetized females showed no sperm in their sperm storage organs, even though the sperm themselves were just as mobile as ever, suggesting that the female has to actively shuttle sperm into the right place.

Among most vertebrates, sperm are deposited all at once during ejaculation, which means that the length of copulation probably has little effect on the number of sperm transferred. Many insects, however, transfer sperm in tiny packets, called spermatophores, that often attach to the outside of the female's body, leaving them perilously vulnerable to removal while the sperm are draining into the female's reproductive tract. Other species transfer sperm during the entire mating process, which can take many minutes or even hours. This means that if females control how long coupling lasts, they also control how many offspring a given male is likely to father. For example, female black field crickets in Australia let spermatophores remain attached longer for more attractive males (those singing more energetic songs) than for relatively wimpy males.

To induce females to allow spermatophores to remain attached, males in many different insect groups offer an enticement in the form of food. Several different kinds of male katydids produce not only the spermatophore like those of the crickets discussed above, but a nutritive blob attached to it called a spermatophylax. In some katydids, this structure takes several days to manufacture, and weighs a third or more of the male's body weight, representing a substantial offering. The female eats the spermatophylax, and its protein-rich contents enable her to lay more and larger eggs. The sperm are transferred to the female while she is eating the spermatophylax; when she has finished her meal, she often reaches around, breaks off the sperm-containing structure, and eats that too. The larger the spermatophylax, the longer it takes her to finish it, and therefore the more sperm enter her body.

Because the spermatophylax is so expensive to produce, each one represents a significant chunk of the male's mating effort for his lifetime. As a result, males in some katydid species become rather choosy about just who is entitled to receive one of the delectable morsels. Larger female katydids lay more eggs, which means more offspring sired by a male's sperm. Thus, as might be expected, in Mormon crickets (which are really katydids, not crickets, and which lack any religious affiliation so far as anyone can determine), males spurn small delicate females in favor of plump ones, a practice that may console failed dieters.

Other insects, such as hangingflies and scorpionflies, go out and catch prey items to present to females, who then consume the item while their hind ends are occupied with mating. Acquiring the prey items can be risky, since they are mainly obtained from spider webs, and so in a few species of scorpionfly, males offer specially produced wads of saliva to females instead. As with the katydids, the larger the gift, the longer the female will remain paired with the male. Sometimes, however, a male will simply grab a female and attempt to mate with her without offering one of these so-called nuptial gifts. Females take a dim view of such forceful behavior and generally won't stay coupled for very long with a male arriving sans offering. They also may be able to control the rate at which sperm are delivered into their reproductive tract. A recent study of a scorpionfly native to the Caucasus region in Europe found that while gift-bearing male scorpionflies remained coupled to females only twice as long as males attempting to force copulations, they transferred almost eleven times more sperm.

Females can also eject sperm after mating. Male damselflies and dragonflies, like the scorpionflies, simply grab females and mate with them, often removing the sperm of previous mates using the scoops and spines mentioned earlier. Most scientists studying these insects had assumed that the females had little control over who fathered their offspring, but a recent study by Alex Córdoba-Aguilar from the Institute of Ecology at the Autonomous University of Mexico showed that the females might have the last word. Córdoba-Aguilar noted that in many damselfly species, females had much less sperm in their storage organs than was present in the male's ejaculate. In fact, they seemed to have discarded so much sperm that they lacked sufficient numbers to fertilize all of their eggs. This seemed puzzling, or as he put it, "If females are using such sperm for oviposition, females are bad sperm administrators." He then collected females during different stages of the mating process and measured the volume of sperm present in their reproductive tracts. Then he counted the number of eggs that were laid after the females had mated with one or more males. It seemed that the females were favoring some males' sperm over others by ejecting the less-preferred males' contributions, long after the male himself had departed.

Males do seem to engage in some extreme antics to ensure that their ejaculates are not only placed in the appropriate part of the female's reproductive tract, but will be used by the female in fertilizing her eggs. As part of his ongoing studies of the intricacies of animal genitalia, Eberhard has uncovered some pretty racy stuff. A 2006 paper on spider mating behavior by Eberhard and colleagues Alfredo Peretti and R. Daniel Briceño, published in the ordinarily staid journal Animal Behaviour, contains passages that sound like what would happen if Danielle Steel were an entomologist: "Males squeezed females rhythmically with their enlarged, powerful genitalia throughout copulation." The title of the paper is no less suggestive, containing the words copulatory dialogue, again something one imagines those in the adult film industry to have mastered. In the spider under consideration, a rather modest-looking species called the short-bodied cellar spider, females "sing" during mating by moving their pedipalps, small appendages near the jaws, and making a sound the authors describe as "resembling squeaking leather." (If there is such a thing as spider porn, this is it.) As in many insects and their relatives, females mate with more than one male, and in this case the females seem to regulate paternity according to the ability of the male to be in tune with their wants and desires, if suggesting that spiders possess such things isn't too much of a stretch. The males adjust those rhythmic squeezes according to the sounds produced by the females, and males that were more responsive to females ended up fathering a larger proportion of the offspring.

My, What Big ... Oh, Never Mind

HUMAN sperm cells have an easily recognized tadpole appearance and, while not exactly iconic in society, have their own modest place in kitschy, not to mention downright tasteless, objets d'art. There are neckties with stylized sperm cells, salt and pepper shakers, and of course the inevitable coin bank in the shape of a sperm cell (get it?). At the American Society for Reproductive Medicine's 2008 conference, sperm cell-shaped USB drives were handed out. But such aggrandizement aside, the truth is that human sperm cells have a pretty humdrum appearance compared with those of many insects.

In his original paper, Parker noted that sperm within an ejaculate must compete, not only with sperm from rival males, but with each other, and therefore any attribute making one individual cell better able to succeed should be subject to selection. This variability is particularly important in the insects, because sperm are usually not used to fertilize the egg immediately, as is the case in many other animals, but are stored for a period of weeks, months, or even years before they are used. This means that anything giving a sperm cell longer life or a competitive edge over the long term will be valuable. Indeed, insect sperm morphology is amazingly varied, including some with multiple flagellae, the whiplike organs used to propel the sperm through the medium. Sperm cells are much more variable across species than other kinds of cells, and even more variable than many body parts; one could, at least in theory, use sperm characteristics to distinguish species, the way that beak shape or feather color are used by bird-watchers to determine whether they are seeing a black-headed blue warbler or a white-eyed vireo. This is probably unlikely to catch on as a pastime ("Hey, guess what—I spotted a double-flagellated big head over the weekend!"), but it points to an often unconsidered source of biodiversity.

Some species of the humble fruit fly are the real sperm champions, at least if you think size is what matters. Male Drosophila bifurca look pretty much like any other fruit fly, namely, tiny and brown. But they have sperm cells that are about twenty times the length of the male producing them. To put this into perspective, for a human male six feet tall to achieve a similar feat, he would have to produce sperm cells that could span a sizeable portion of a football field, to carry on with the sports analogies that inevitably seem to accompany discussions of sperm competition. The cells are mostly tail and initially are in tangled coils resembling balls of yarn, so that the males employ what one scientist calls a "peashooter effect" to get the sperm transferred to the female.

Needless to say, manufacturing such behemoths is energetically costly, and a male can't produce nearly as many so-called giant sperm as the ordinary variety. Male D. bifurca therefore "use their sperm with female-like judiciousness," according to Scott Pitnick from the State University of New York at Syracuse. Unlike most species of insects, including other types of Drosophila, D. bifurca males and females mate with roughly similar numbers of partners. The precious cells are produced on demand, with more being manufactured when males are given greater access to females and fewer when mating opportunities are scarce.

The function of the elongated tails is unclear. Some researchers suggest that they may block other males' sperm from getting through the female's reproductive tract. Alternatively, large sperm may have evolved because of selection by females for the more exaggerated forms of the cells, making them what Pitnick and his colleague Gary Miller called "the cellular equivalent of the peacock's tail." Pitnick and Miller took laboratory populations of D. melanogaster, a more commonly used fruit fly than the giant sperm-bearing D. bifurca, and subjected them to artificial selection experiments similar to the ones that Simmons employed with the dung beetles. Here, instead of constraining the number of mates an individual had, Pitnick and Miller selected directly for either increased or decreased sperm length or the length of the females' primary sperm storage organ, the seminal receptacle. Like most insects, female fruit flies have convoluted organs used to keep the sperm until the eggs are fertilized, often many days later.

After thirty or more generations of the selection treatment, flies from the different groups were mated to each other, and the relative success of the different types of males at fathering offspring was calculated. The newly created long-sperm males were much better than the short or normal length sperm males at fertilizing eggs of the females with longer seminal receptacles. When females had short seminal receptacles, sperm length didn't matter. Pitnick and Miller concluded that the giant-sized sperm evolved because the female reproductive tract selectively biases paternity in favor of males with longer sperm. What caused the female's seminal receptacle to become longer—and why D. bifurca is the fly equivalent of a bird of paradise, while other species are the drab sperm sparrows of the Drosophila world—isn't clear.

Complicating the story is the finding that among at least some other insects, such as the dung beetles, shorter sperm seem to do better than longer sperm. Male dung beetles in better condition, with better nutrition as larvae, produce shorter sperm. And fathers that sired sons producing short sperm also had daughters with larger sperm storage organs. At least with regard to sperm, size may matter, but it isn't always better to be big.

A Caste of Thousands

AMONG virtually all butterfly species and some other insect groups, two types of sperm, sometimes called castes, as in the worker and queen castes of social insects, are produced: eusperm, which has a DNA-carrying nucleus and is capable of fertilization, and parasperm, which is smaller and has no genetic material. Some scientists have suggested that the different sperm morphs have different functions, with only a tiny minority of sperm actually able to reach the egg. The other sperm cells act as blockers of rivals or helpers of the real champs (for example, they make it easier for the fertilizing sperm to move through the female reproductive tract) but are themselves sacrificing their own chances for survival. Some years ago it was suggested that similar divisions of labor occurred in human sperm cells, and the nonfertilizing sperm were dubbed kamikaze sperm, for obvious reasons.

It is a colorful theory, but the evidence, at least as it pertains to humans, is weak at best. In mammals, many sperm that appear nonfunctional didn't get that way through a plan; they represent errors in manufacturing. And the evidence about what is retained versus rejected by women's reproductive tracts comes from a very few studies of what is exuded after sex, using samples provided by a group of volunteers who may or may not represent the general population.

Insects, though, are another story as far as sacrificial sperm goes. In butterflies, the theory that seems to have the most support is that the nonnucleated sperm cells are cheaper to produce and, hence, may act as "filler," allowing the male to swamp out other ejaculates with quantity if not quality. The more likely a butterfly species is to experience sperm competition, the longer the eusperm. But the same function does not seem to occur in the other insects with two kinds of sperm, and until recently the role of these odd self-sacrificing cells was a mystery.

Some recent work by Luke Holman and Rhonda Snook at the University of Sheffield in the United Kingdom suggests that looking at the situation from a female perspective may help explain the evolution of this obviously masculine trait. They used yet another species of Drosophila, D. pseudoobscura, which also has the two sperm types, to see whether female flies might be the ones controlling the situation. Indeed, many of the sperm are actually killed by the chemicals or cells present in the female's reproductive tract, and the DNA-containing eusperm seem to be particularly sensitive. When males produced more of the parasperm, the eusperm were protected from the spermicidal activity. The parasperm appeared to be acting as shields for their more fertile brothers. A few authors actually refer to the parasperm as soldier sperm, but I think that presumes that they are fighting each other, when as Holman and Snook point out, the female seems to be playing an active role in their demise.

Why should the female reproductive tract be such an unwelcoming environment for sperm? Holman and Snook speculate that one possibility is that females are using their own reproductive organs as a screening device, making the sperm from various males run (or swim) a gauntlet of tests before being allowed to fertilize the eggs. In other words, cryptic female choice could explain the evolution of a seemingly nonfunctional cell type. The criteria that the females might use to distinguish among suitors are not well understood. It may be that, as with the exceptionally long tails of the giant sperm in D. bifurca, parasperm are a kind of secondary sexual trait, like the peacock tail.

An answer to the question of why sperm are so variable, as well as how likely it is for females to sort through sperm in their reproductive tracts and the function of all those chemicals in the semen, will likely require examining the situation from the sides of both males and females. The fierce activity that occurs inside a female after copulation does, however, provide a possible insight into that sex difference in postcoital behavior. With all that commotion going on in there, who could sleep?