(WOMENSENEWS)--Charles Darwin's famous theory of natural selection--which he began to develop in the 1830s--may still be widely accepted as an explanation for how species are related and what causes them to change over time. Biologists, however, are beginning to pick apart another of his evolutionary premises--sexual-selection theory--and say it deserves to be rethought and perhaps discarded altogether.

The key idea of sexual-selection theory is based on the idea that females' way of choosing mates can influence male traits and that this selection process can explain a great deal of sexual behavior. Darwin formulated sexual-selection theory in part to explain questions raised by elaborate and bizarre sex behavior. For instance, why do peacocks brandish their plumage when such bright displays could attract predators? Darwin's answer: Evolution of showy male traits is justified when those traits increase the chances of carrying genes forward, even if the feathers eventually attract a fox rather than a pea hen.

But while sexual-selection theory justifies some mating behaviors it by no means explains all of them, says Joan Roughgarden, a professor of biological science at Stanford University, Stanford, Calif. The evidence for diversity of sex, gender expression and sexuality in nature are extensive, she says. Continuing to overlook the flaws in Darwin's sexual-selection theory, she continues, will eventually undercut and endanger confidence in the rest of Darwin's work, which has stood up to extensive scrutiny.

By ignoring the abundant challenges to Darwin's sexual-selection theory in nature, overlooked is evidence that sexual behavior often doesn't match gender and that many species exhibit flexible sexual expression.

Male-Female 'Binary' Is Challenged

"The biggest mistake in biology today," said Roughgarden, "is extending the idea of the gametic binary to both behavior and life history." (Gametic binary is the premise that there are only two sexes, male and female, and by extension just two genders, masculine and feminine.)

However, many plant and animal species make both eggs and sperm during their lifetimes, making the idea of distinct "male" and "female" bodies untenable. In fact, says Robert Warner, professor of marine ecology at the University of California at Santa Barbara, many animals and plants function as both sexes at the same time, and some, like the hamlet fish, can change sex as conditions change, in a matter of minutes.

In addition, nature produces societies with up to three male and two female genders. For example, there are three types of male bluegill sunfish, all different in size and appearance. A "controller male" attracts females to a territory, an "end-runner" male curtails the controller's monopoly by intercepting and fertilizing eggs, and a "feminine male" helps facilitate mating. All fertilize some eggs and their multi-gendered society continues.

"Gender is surprisingly labile and is not solely determined by the gametes a creature happens to produce," said Warner. It is more useful to think of sex as tactical: in other words, sexual expression can vary depending on factors such as an animal's parents, environment and social circumstances, he says. "There is incredible diversity of sexual expression out there," said Warner, "and while it is predictable, it is not as simple as Darwin might have imagined."

Gender Does Not Dictate Sexual Behavior

Patricia Adair Gowaty is an ecologist at the University of Georgia, Athens, who argues that it is almost impossible to draw definitive conclusions about mate selection from existing studies. "We need research that asks the same questions of males and females in the same species," she said. "Do females approach males and can males be choosy too?"

Yes, and yes, she found.

She conducted two kinds of experiments, the results of which she presented earlier this year. In one, she placed one male and one female fruit fly in a vial and noted who went toward whom. Standard sexual-selection theory predicts that males are the ardent ones. Her results defied this however. She observed that females were often as interested in the males as the males were in the females.

"In the second set of experiments," she said, "we placed either flies or mice in a three-armed arena so that choosers could get a look-smell-hear of the two opposite-sex individuals. Again, standard sexual-selection theory predicted that female choosers would be picky and male choosers would be indiscriminate. But we found that in both flies and mice there were no differences in choosy or indiscriminate behavior by sex," she said.

Gender, which originates in the gonads, does not equal sexuality, which is a product of the brain, says David Crews of the University of Texas at Austin. The study of gonadal sex influences, but does not explain, sexuality, he says. Sexuality emerges from a different process, resulting from genes, but also hormones, physiological conditions such as the health of the pregnant mother, maternal care during infancy and accumulation of life experience.

Broader Role of Sexual Intercourse

Roughgarden says that sexual intercourse has social roles--managing power, negotiating for resources--as well as a reproductive one. She proposes a new theory she terms "social inclusionary selection." This concept encompasses Darwin's idea that female choice can influence male traits, and that sexual selection does exist. However, it reaches beyond his theory by incorporating the enormous diversity in how sex, gender and sexuality are expressed.

There are many examples of same-sex sexual activity in animals, including humans, which Darwin noted but did not explain. Paul L. Vasey's studies in the past few years of Japanese macaque monkeys at the University of Lethbridge in Canada suggest that animals may sometimes choose mates that don't have reproductive value, i.e., whom they can't impregnate or become pregnant by.

While Darwin posited that males compete among themselves for access to female mates, Vasey observed that both males and females compete to have sex with other female macaques. He set up tests that ruled out functional explanations for their homosexual behavior such as easing social tension or attracting male mates. Instead, the activity appears to be for sexual reward. Female macaques masturbate by mounting each other, in this way cooperating for pleasure. They almost never masturbate in any other context.

Although challenges to sexual selection theory are widely documented, the flaws are rarely included in biology classes, nature programming or zoos. Instead a contradiction is perpetuated: on the one hand females are choosy about mates so that they can select the best genes; on the other, broad genetic diversity ensures a species' long-term survival.

Roughgarden asserts that this contradiction suggests females seek either elite or diverse genes. Nature points to more wide-ranging conduct. Educators should teach the broader reality of sexual behavior, she says. "It's about time criticism of sexual-selection theory was carried forward by women scientists."

Kathleen Nelson is a freelance journalist in New York City.

Copyright 2003 Women's eNews