Sex on Six Legs Read online

  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 he
lpers 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.