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July 7, 1998

What Do Female Bugs Want? Surprise: It's Shape, Not Size

By NATALIE ANGIER

The movie posters for "Godzilla" read: "Size does matter." Hey, wipe the scales from your eyes, you overstuffed iguana! Size is not the point: points are the point. Titillators and claspers are the point. So are hooks, knobs and grooves, cerci, epiprocts and paraprocts. How about something that unfolds blade by blade, like a Swiss Army knife -- or the phallus of a male oriental cockroach? If big is the best you can do, darling 'Zilla, no wonder you've been a box office snore.

Up and down the phylogenetic scale, in all creatures where a female's eggs are fertilized internally, the male's phallus must perform pretty much the same task: penetration and ejaculation. Yet, as comparative biologists have found, the penis and its accessory parts are often far more complex and embellished than utilitarian design would seem to require. The organ of the male cat is stippled with spines, that of some male monkeys is flanged as though with wings, while the human penis has its foreskin and the distinctive bulbed glans beneath.

Among insects, male reproductive organs differ so dramatically from one species to another that entomologists rely on the particulars of the cerci, epiprocts and other bits of arthropod genitalia to distinguish between species that otherwise look alike.

Scientists have long debated the reasons for such ornateness of penile shape, or morphology. By one prevailing theory, male organs are diversely proportioned for much the same reason that keys are: to keep strangers out of the house. In this scenario, the male penis serves as a barrier against cross-copulations between members of two different species, an act that would either be a sterile waste of reproductive energy, or would result in the birth of genetically weak offspring. Thus, the males of a species must all have uniquely shaped keys to match the genital locks of their corresponding females. Charles Darwin himself believed that the evolution of reproductive organs was driven by such practical concerns as the maintenance of species purity.

But now a researcher from Sweden has published results strongly suggesting that here, at least, the great man was wrong. In a detailed study of insect genitalia and its association with insect sexual practices, Goran Arnqvist of the University of Umea offers evidence supporting another theory for the divine absurdity of phallic diversity. His results, which appear in the current issue of the journal Nature, indicate that male reproductive organs are the pelvic equivalent of peacock feathers -- the fruit of sexual selection.

Sexual selection stands with natural selection as a mighty engine of evolutionary change. But while natural selection favors practical traits that help an animal survive in its habitat, like a fur coat to weather winter or a long tongue to pick out ants from an anthill, sexual selection favors traits that, for whatever reason, lend a male an advantage in the harsh competition for access to a female's eggs. The most familiar example of sexual selection in action is the peacock's gorgeous, awkward plumage, which does nothing to help the bird escape a predator, but which does plenty to attract a peahen's eye and persuade her, "Mate with me, not with that drip over there."

As Arnqvist demonstrates in his new report, the hand of sexual selection does not stop at molding the properties necessary for attraction and courtship. Because females of many species mate with multiple partners, he says, it is not enough that a male have the wherewithal to solicit a copulation. He must also possess features that keep his sperm in the race once mating has occurred. And what better way to fight the spermic fight than through modifications of the vehicle that delivers it?

"Charles Darwin saw sexual selection as the force whereby certain males are more attractive to females than are other males, and so they gain more matings, leading to the evolution of things like bright plumage," Arnqvist said in a telephone interview. "The thing that Darwin did not realize, but that has become apparent to us in recent years, is that sexual selection can operate in different way, not just on the level of mating, but on the level of fertilization as well. That's where the variance in genital morphology comes in."

Arnqvist proposes that nearly every fillip, flange and blade somehow plays a role in assuring its owner's fertilization success. He proved his thesis by comparing two groups of closely related insects that differed in their mating systems. One group consisted of species that were polyandrous, in which the female copulates with many males, while the other was of species that were monandrous, in which the female mates only once in her lifetime.

Gathering the right mix of representative insects was a grueling task, not the least difficulty being that monandry is rare among insects, as it is elsewhere in the animal kingdom. "It was a huge amount of work finding good examples," Arnqvist said. "I talked with hundreds of researchers all over the world and read I don't know how many thousands of papers." Eventually, he managed to find species from four different insect orders: mayflies; butterflies and moths; flies and mosquitoes, and beetles.

Arnqvist then worked with detailed illustrations of the male genitalia of his exemplary species. That information, at least, was comparatively easy to find, thanks to the historic importance of male genitals to standard insect taxonomy research. Using a new and rigorous method for assessing structural complexity called geometric morphometrics, he then gauged the genital complexity of his various species at 19 different contrast points. He asked how different those traits were from one species to the next. He also measured and analyzed other body parts, like wings and legs.

Arnqvist reasoned that if the lock-and-key hypothesis of genital morphology was true, then there should be more variation in genital shapes among the monandrous group of species than among the polygamous ones: if a female only has one shot at mating, and if it is essential that she finds just the right species key for that event, then the pressure would be on to vary the phallic details in no uncertain terms between two closely related species.

If, on the other hand, sexual selection is what drives genital diversity, then the variety would be greatest among those species where the females philander, and the males must perpetually evolve new and improved genital ploys to prevail in the post-mating contest.

The results were startlingly clear-cut. In his group of polyandrous species, the genitals of the males were more than twice as divergent as they were among related species where females mate only once. For 18 out of 19 of the contrast points, he said, the male genitals of the polyandrous group displayed greater variability than they did in the monandrous group. At the same time, the other, nonsexual body parts he analyzed showed little or no variability between a closely related pair of, say, moths or fruit flies. Hence the variability of the insects in the polyandrous group was specific, focused on the region where the force of sexual selection might be expected to work with greatest monomania -- viz., below the belt.

But what are all these parts and bits doing to give a male a reproductive leg up, as it were? In a few examples, the function of a genital detail is easy to see. The male damselfly, has little brushes at the end of his penis that can scrape out from a female's genital tract any contending sperm that got there first. Other insects have hooks on their phalluses that clasp a struggling female into position until the job is through. The spines of a cat's penis are thought to act as titillators, which help accelerate ovulation by stimulating the female's vaginal tract.

For most genital structures, though, the purpose can only be guessed at. Some components may convey promotional information about the male's merits -- his size, health and vigor. Still others may have arisen arbitrarily, the consequence of female taste for novelty.

"There doesn't always have to be a reason for female choice, but once it starts, once this component of male genitalia has been preferred over that one, it can have a runaway effect on evolution," said Darryl T. Gwynne of the University of Toronto in Mississauga, who wrote an editorial that accompanies the new report.

Arnqvist's report offers the most rigorous evidence yet that sexual selection explains the evolution of genital diversity in insects, but other researchers think they see a similar mechanism at work in an order closer to our hearts: the primates. Most famously, they have noted that the testes of a chimpanzee are much larger than those of the gorilla, even though a male gorilla has maybe five times the body mass of a chimpanzee. That discrepancy is thought to arise because female chimpanzees are promiscuous, while female gorillas tend to mate solely with the silverback male in whose harem they live. Thus, chimpanzee testicles must be large to generate abundant quantities of competitive sperm. The male gorilla has relatively less need for big testicles, and more need for big body size, to give him the chance of fighting other males and assuming haremship in the first place.

Neither are humans immune to the competitive squeeze. Writing in the journal Human Nature, Raven Rowanchilde of the department of sociology at the University of Toronto, has speculated that sexual selection explains the variety of penile modifications and accouterments seen among different human societies. She proposes that the men of many cultures alter their penises, in sometimes painful fashion, to augment their appeal as mates.

In Australia and New Guinea, a number of traditional peoples practice subincision, in which a cut is made to the underside of the penis that makes the organ look wider without, apparently, affecting its capacity to perform. According to anthropologists who study these groups, the women consider intercourse with a subincised man to be superior to sex with a non-incised partner.

In 20 cultures of Southeast Asia, men ritually insert objects like bells, balls, pins, rings, or marbles made of ground shells under the skin of the genitals. The To Saloe-maoge women of Sulawesi may even demand to know the number of penile marbles a man possesses before they will consider a proposal of marriage. The Dyak men of Borneo use a palang, a smooth bar with rounded ends made of bone or metal, to transect the head of the phallus; Dyak women, according to anthropologists, say that sex without a palang is like rice, "but with it, it tastes like rice spiced with salt." At which a squeamish Western fellow might be tempted to sigh, "Whatever happened to candlelight and romance?"



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