Billy Crystal may have been shocked when Meg Ryan so effectively—and amusingly—faked an orgasm in a restaurant during the 1989 movie When Harry Met Sally, but surveys suggest only one-third of women are regularly fully aroused during intercourse. And although poor partner performance, psychological issues, or physiological shortfalls are often cited as the reason, two evolutionary biologists now offer a provocative new explanation. In a paper published today, they argue that female orgasm is an evolutionary holdover from an ancient system, seen in some other mammals, in which intercourse stimulated important hormonal surges that drive ovulation.

Humans and other primates don’t need intercourse to trigger ovulation—they evolved to a point where it happens on its own—but the hormonal changes accompanying intercourse persist and fuel the orgasms that make sex more enjoyable, the biologists hypothesize. And because those hormonal surges no longer confer a biological advantage, orgasms during intercourse may be lost in some women. This explanation "takes away a lot of stigma” of underwhelming sexual relations, says one of the authors, Mihaela Pavlićev, of Cincinnati Children's Hospital in Ohio.

The new work addresses what David Puts, a biological anthropologist at Pennsylvania State University, University Park, calls “one of the most contentious questions in the study of the evolution of human sexuality: whether women's orgasm has an evolutionary function." There are more than a dozen theories about the evolution of orgasms, most proposed decades or more ago. They include arguments that women have orgasms because their reproductive machinery has the same origins as those of men, who need to have orgasms to ejaculate sperm. Others think orgasms are an evolutionary novelty that persists because it helps foster loyal partners. Some have proposed that female orgasms induce physiological changes that increase the chances of conception, but there’s no strong evidence that women who have more have increased fecundity.

Orgasm itself may have no evolutionary function, but it is derived from a key part of the reproductive cycle, Pavlićev and her colleague propose today in the Journal of Experimental Zoology Part B: Molecular and Developmental Evolution . Pavlićev didn't start out studying orgasms. To better understand the evolution of reproduction, she was compiling data on the ovarian cycle in different mammal species. During this cycle, cells destined to become eggs mature, escape from the ovary, and travel down the reproductive tract. She discovered that in some species, environmental factors control egg maturation and subsequent ovulation; in others, such as rabbits, sexual intercourse with a male or even just his presence causes the release of the egg. In either case, a series of changes involving the hormones oxytocin and prolactin are triggered that cause the egg to mature and migrate. In humans and other primates, the ovulatory cycle has become spontaneous, generally on a set schedule that requires neither an environmental trigger nor a male. Pavlićev then realized that women still undergo the same hormonal changes as species with induced ovulation, but during orgasm.

To see whether induced ovulation was the evolutionary predecessor of orgasms—in a similar way that fins were ancestral to limbs—she and Günter Wagner, an evolutionary biologist from Yale University, first needed to see whether induced ovulation predated spontaneous ovulation in evolutionary history. Their literature search showed that environmental- and male-induced ovulation are found in earlier evolving mammals and spontaneous ovulation appears in later species, including our own. They also noticed another change. In earlier mammals, the clitoris, which is so often key to a woman’s orgasm, tends to be part of the vagina—guaranteeing that intercourse stimulated this organ and kick-started ovulation. But in later arising species, particularly primates, the clitoris has moved ever farther away from the vagina, even out of reach of an inserted penis. “A shift in the position of the clitoris is correlated with the loss of intercourse-induced ovulation,” says Martin Cohn, an evolutionary developmental biologist at the University of Florida in Gainesville. “Their hypothesis shifts the focus of the research question from the evolutionary origin of orgasm as an evolutionary novelty, which has long been presumed but not demonstrated, to the evolutionary modification of an ancestral character.”

Pavlićev and Wagner’s theory helps explain why female orgasms during intercourse are relatively rare. “It is new to use [this] innovative, Darwinian approach to understand one of the mysteries of human sexuality—why the male orgasm is warranted, easy-to-reach, and strictly related to reproduction and the female counterpart [is] absolutely not,” says Emmanuele Jannini, an endocrinologist at University of Rome Tor Vergata. The nonnecessity of orgasms for reproduction may also explain why women’s reproductive tracts vary a lot more than men’s—there are fewer constraints, he adds.

Jannini and others point out, however, that this theory needs more confirmation. So far, it deals only with the parallels between the hormonal surges in females during male-induced ovulation and orgasm, but has not looked to see whether there are also parallels in the neurological components of these activities, says Elisabeth Lloyd, a philosopher of science at Indiana University, Bloomington, who was not involved with this work. And because it’s so difficult to assess whether other mammals feel the pleasure associated with orgasms, the work can only ever address the evolution of some of the components of female orgasm, Puts notes.

Others more strongly criticized the new explanation. Two behavioral neuroendocrinologists, Michael Baum from Boston University and Kim Wallen from Emory University in Atlanta, tell Science that Pavlićev and Wagner misinterpret some previously published results and do not have the details about the hormonal changes during ovulation and orgasm correct. “Their hypothesis remains a good hypothesis,” Wallen says. “But I’m not very convinced by the data they marshal.”

Lloyd says the work drives home how much more we need to learn about female sexuality in other organisms. Wagner and Pavlićev concede that more data are needed to firm up their theory, though for now they have no plans to follow up themselves. Cohn predicts others will pick up the baton. “Pavlićev and Wagner have taken a fascinating, creative, and thoughtful approach to a problem that has been investigated by many but resolved by few,” he says. “I suspect that many investigators will be stimulated to further test the hypotheses raised in this paper.”