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Tracking the monogamous mouse

THE BALTIMORE SUN

Berkeley, Calif.--Two scientists have identified a species of monogamous mouse, the female of which produces a chemical in its urine that induces the male to take care of their babies.

University of California ecologist David Ribble and David Gubernick, assistant professor of psychology at the University of Wisconsin, also discovered that, after being weaned from their mothers, virgin female California mice (Peromyscus californicus) roam into new territory to find a mate, while virgin males stay near the place where they were born to wait for a female to find them.

After a female selects a mate, it waits, sometimes for several months, before going into estrus to mate, perhaps to ascertain the suitability of the male and its territory for raising offspring.

Scientists have long suspected that the California mouse, which ranges from Northern California to Baja California, was monogamous since it was first studied 40 years ago. "It's extremely rare in mammals as a whole," said Mr. Ribble. Although monogamy is common in bird species -- perhaps as high as 60 to 70 percent -- the best estimates are that only about 3 to 10 percent of mammals mate exclusively with one of their own species.

But this year Mr. Ribble, a doctoral student who does his research at Cal's Museum of Vertebrate Zoology, finished experiments using a technique new to field biology -- genetic fingerprinting -- to demonstrate the exclusive relationships between male and female California mice.

The data backed up field observations he made in 1987. At that time he dusted female California mice living in the canyons of the Hastings Natural History Reservation in Monterey County with different fluorescent pigments to see how many other male mice would pick up the same pigment. He found that each adult male picked up only one pigment -- the color of the female with whom it was living.

To obtain the DNA necessary for the genetic testing, he anesthetized trapped mice and snipped off a tiny tip of their tails. He chose the procedure after noticing that many wild mice were missing their tail tips, perhaps from encounters with predators. He couldn't take blood samples, because the red blood cells don't have nuclei, where DNA is located. In testing 98 offspring from 27 families, he found that their DNA matched the DNA of their parents.

"It turns out they're as monogamous as they can be," said Mr. Ribble.

From his observations during the field studies, he also found that males spend as much time caring for the baby mice -- known as "pups" -- as females do.

By putting tiny plastic collars with radio transmitters around the necks of several male and female mice, he tracked their position for several days before removing the collars. He found that they spent equal amounts of time in the nest. Because pups cannot regulate their body temperature, the adults must attend them to keep them warm for survival.

This behavior was also observed in a Wisconsin laboratory, where Dr. Gubernick began his studies of 600 California mice several years ago with 1,000 hours of time-lapse video recordings. He found that both parents care for the pups: They build nests, carry the young, huddle over the pups to keep them warm and lick them to keep them clean and stimulate blood flow.

Only two behaviors differ between males and females. Although males lick the pups longer than do females, the mothers lick the pups' anogenital area. They do so to stimulate urination by the pups, which can't urinate on their own.

In addition, the mothers drink pups' urine to recover the water provided to the young in the milk. This behavior has also been noticed in rats and is a method for the female to maintain its body's water balance. "It reduces the time the mother has to leave the young and go foraging," said Dr. Gubernick.

When looking at what kept the parents parental, Dr. Gubernick stumbled across the physiological basis for male parenting. Although he found that females needed their pups to act parental, pups did not induce a male to be parental. "It was the presence of the mother that was important to keep the males parental," he said. After exposing males to other female mouse urine and distilled water, Dr. Gubernick determined that it was only a volatile chemical signal from the urine of the male's mate that induced it to take care of the pups.

"We're trying to identify the chemical now," he said, also noting that some changes may be occurring in the brain during parenting. The medial preoptic area, which affects maternal behavior in rats, is larger in virgin males than in virgin females, but the same in mice that are parents.

Dr. Gubernick has also probed the mice's monogamous relationship by investigating the maintenance of pair bonding, mate fidelity and mate choice. He offered females in their second estrus another male. They preferred their mates. When two virgin females were put in a cage with a male and female that had already bonded, the male would not mate with the virgin females.

"How the individual responds to the other individual makes a lot of sense in pair-bonded species," said Dr. Gubernick, who pointed to studies done on humans. "There's a bunch of information gathered by people who have determined that the relationship between a husband and wife affects the way males and females respond to their kids."

Although it's very clear in the laboratory that males spend as much time caring for the pups as do the females, Mr. Ribble and Dr. Gubernick haven't been able to draw firm conclusions about parenting behavior in the wild.

Once, they stuck a fiberoptic probe into a nest in the wild to try to record the parental behaviors. "Unfortunately, the probe resembled a snake, and the parents were obviously upset," chuckled Mr. Ribble.

This past summer, Mr. Ribble and Dr. Gubernick did more field studies at the Hastings reserve to watch adult mice take care of their young. Conclusions have not yet been drawn from the data.

Among other things, they had been hoping to determine if another unusual laboratory behavior also occurs in the field: that weaned offspring help raise their younger sisters and brothers. Immediately after a female gives birth, it mates again and produces another litter a month later. But the first litter stays in the nest for another month before leaving to establish its own nests. During this time, the older siblings appear to baby-sit the pups.

As to why the California mouse has such a complex social system, Mr. Ribble offered a complex answer: The mouse, which weighs 40 grams, is about twice the size of normal field mice. And, usually, in mammals, "the bigger you are, the smaller the litter size," he said. "The reason is, metabolism: There's less energy available to produce pups."

Although four pups can share enough body heat to maintain their body temperature to keep themselves alive, two pups -- the number produced by the California mouse -- cannot. Thus, a male contributes to the growth of the pups by helping maintain their body heat while the female leaves the nest to eat.

Another interesting characteristic of California male mice has prompted Dr. Gubernick to use them as a model for male parenting in humans. When they're parenting, male mice have elevated levels of prolactin, a hormone found in males and females that increases in females when they're producing milk.

This phenomenon is not limited to the California mouse. A study of a primate species found that common marmoset fathers, which have parenting responsibilities and carry the young, also have elevated levels of prolactin.

To find out if human males undergo similar hormonal changes when their wives are pregnant and give birth, Dr. Gubernick is now following 25 couples who are participating in Lamaze classes from six weeks before the birth of a child to four weeks after. He anticipates analyzing the data early next year.

"If we find something, it will have important implications for paternal bonding," he said.

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