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Thursday, Dec. 6, 2001

NATURAL SELECTIONS

Female langurs get empowered


Humans are remarkable in many ways. Most of us, for example, have sex in private. Compare that to most other mammals, who will copulate in clear view of their fellows.

Female mammals usually have a well-defined period of time when they are sexually active. In most primates, at ovulation, the skin around the vagina swells and changes color, and the animal's odor and behavior change. Sex occurs during this estrus period and may be prolific (female baboons copulate about 100 times with many different males).

Humans are different. There are no morphological or behavioral changes associated with ovulation (or such changes that do occur are subtle compared to those of primates like baboons, who waddle around with heavily swollen pink hindquarters raised provocatively in the air). In humans, the 28-day cycle of ovulation is concealed from onlookers. There is no specific period when sexual activity occurs -- humans have sex continuously.

Explaining why humans are different in these ways is difficult. One hypothesis, for example, put forward by evolutionary biologists George Williams and Randolph Neese in their book "Why We Get Sick," suggests that if Stone Age women had been conscious of the moment of ovulation (and, therefore, the time they are fertile), they might have linked the pain of childbirth with sex. Childbirth was far riskier in prehistoric times, and many women died. If the link between sex and childbirth was made, women might not have wanted to have sex.

It's an interesting hypothesis, but hard to test. So one way to learn why ovulation is concealed in humans is to look at other animals that also conceal it, and try to understand what's going on with them.

Hanuman langurs are catarrhine primates, a group that includes Old World monkeys, apes and humans. As in humans, the ovarian cycles of Hanuman langurs are not linked to sexual activity; sex will often occur without ovulation. They form predominantly female groups, with one or more males also present, and mixed groups, in which females will copulate with all the males.

However, there is another, darker aspect of Hanuman biology that influences what females do. As among lions and some primate species, infanticide is known to occur. Males can increase their reproductive success by killing the young in a group, forcing females to start the reproductive process all over again.

A study on Hanuman langurs, published this week in the Proceedings of the Royal Society of London, set out to test the hypothesis that concealed ovulation and extended sexuality evolved to confuse paternity among males in multi-male groups. If paternity is unclear, then infanticide loses its selective appeal.

Michael Heistermann and colleagues at the German Primate Centre in Gottingen set about testing the infanticide theory in a group of wild Hanuman langurs in Nepal. Field workers followed females from dawn to dusk, collecting data on mating activities (a total of around 3,000 hours of observations were carried out). They also collected fecal samples from each animal to determine (through progesterone analysis) the timing of ovulation and the lengths of the ovulatory cycle. Finally, the scientists used a form of DNA fingerprinting to determine the fathers of infants born in the birth season following their observations.

The researchers found that Hanuman langurs are sexually receptive for long periods, and during that time, ovulation is concealed. As predicted, this female strategy lead to mixed paternity in the group and, no doubt, considerable confusion about who fathered whom. In the study, DNA analysis revealed that a substantial proportion of infants were fathered by subordinate males -- and one was even fathered by a male from a neighboring group.

Because the females didn't sneak off for quick sex with any particular, favored male, Heistermann and his team think their behavior was merely aimed at confusing the whole paternity issue. What do the females have to gain by this?

They have their children to gain. Infanticide is extremely costly for the female: The time and energy spent on nurturing an embryo, and then an infant, is wasted. But if a female copulates with any and all males that she encounters, the risk of infanticide will drop, say the researchers, because the chance that a given male langur will commit infanticide depends on his mating history with the female.

The results provide the first direct evidence in catarrhine primates that the extended period of sexual receptivity is a female strategy leading to male confusion. In a way, it can even be seen as a means of female empowerment.

Are human females empowered in the same way? It seems likely that the threat of infanticide led to concealed ovulation in humans, too.

"According to investigations of old church documents, there is evidence that the mortality of stepchildren under 15 years old was extremely high," said Thomas Ziegler, a coauthor of the langur study, in an e-mail interview. "Even today, in the United States, the risk of being mistreated by a step-parent is about 40 times higher compared to the risk of mistreatment by a biological parent. There is no doubt that infanticide occurred in early hominids."

Moreover, concealed ovulation in humans is also associated with confused paternity.

"Genetic screening discovered [in 1991] that in European populations up to 10-30 percent of children were fathered by a man other than the official father," said Ziegler.

Hanuman langurs are named after the Hindu monkey god, Hanuman, the strongest and wisest of the monkeys. Hanuman was a lifelong bachelor, a state that might be expected if he was wise enough to see through the confusion strategies of female Hanuman langurs. But in humans the confusion might have led to a wholly different outcome -- the institution of marriage.

"Humans have concealed ovulation to intensify their pair-bonding -- to make it permanent," said Ziegler. "And to keep the protecting male(s) in the proximity, because the male never knows when ovulation will occur."

E-mail Rowan Hooper at rowan@japantimes.co.jp


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