Naked and not: two species of mole rats run complex societies underground.

On his first trip into Namibia, Chris Faulkes woke up in his tent with a peculiar kink in his back. The ground beneath him had been flat enough when he went to sleep. Yet the next morning, "there was a whopping great lump," he says. A mound of dirt had arisen under Faulkes. He'd inadvertently found--or been found by--Damaraland mole rats, the very creatures he'd come to study. With one of the oddest social systems yet found in mammals, these sub-Saharan rodents spend their lives in networks of underground tunnels that they continually excavate.

These mole rats and a better-known species called naked mole rats survive in land that goes months without rain. When rain finally comes, the animals go into a frenzy of digging to expand their tunnels before the ground bakes again.

With the mole rats' extreme social system, individuals labor for the sake of the colony. Since the early 1980s, mole rats have been used as models of social organization.

The wrinkled, hairless rodent known as the naked mole rat has achieved celebrity status even outside science. In Faulkes' office at Queen Mary College of the University of London stands a cardboard cutout of the Disney-cartoon character of the naked mole rat Rufus. Even the Wall Street Journal has run a page-one story on naked mole rat charms. The subhead read: "What Is Whiskered and Ugly and Has Little Squinty Eyes?--No, Not Your Former Spouse...."

The Damaraland mole rat that woke Faulkes doesn't have a popular following, but it offers a valuable comparison with the naked mole rats' social behavior. Although the Damaraland's basic biology resembles the naked mole rat's, its social structure has some twists. What's more, recent research has revealed a cast that includes couch potatoes.

Says Nigel Bennett, one of Faulkes' colleagues on the Namibia expedition, "I hope people will realize the haired mole rats are just as interesting as the naked ones, if not more so."

GOOD OLD DAYS No scientist knew much about the biology of mole rats in the 1960s, when Jennifer Jarvis of the University of Cape Town in South Africa began studying the evasive, underground rodents. The family she studied contains several dozen species in sub-Saharan Africa that are neither moles nor rats, but are more closely related to guinea pigs and porcupines.

To find mole rats, a researcher looks for hills of dirt and guesses where to dig to strike a tunnel. When the shovel slices through a passageway, researchers fit it with a tube trap rigged so that a door will snap down and capture any mole rat that ventures inside.

Many times, the mole rats detect the breach, says Jarvis. In those instances, instead of trotting into the trap, the mole rats wall off the violated tunnel. That means even more digging for the scientists, often in 40[degrees]C heat and full sun.

Jarvis collects captured mole rats aboveground in tubs until she's retrieved a whole colony. To protect the captives from temperature swings, Jarvis shades the tubs during the day and tucks the animals in at night with carpet backing and hot-water bottles.

When Jarvis first brought a colony of naked mole rats back to her lab, she struggled to find suitable burrows. First, she filled a glass-sided box with soil. "They dug a marvelous burrow system" she says. "The next day, they dug again--and it collapsed." Now, she knows that soil soft enough for easy digging is a rare stimulus for mole rats to embark on urban renewal. "The colony goes crazy," she says.

So, she made her lab colony a plaster of paris home riddled with tunnels that wouldn't collapse. Soon though, the mole rats "looked like tiny white ghosts with beady eyes," she says. Finally, she settled on mole rat runs custom-built from plastic tubing.

Bringing the animals into the lab provided other challenges, which Jarvis would later recognize as clues for one of her major research contributions. She remembers lamenting that she wasn't catching any reproductive females. Also, "I was very distressed to find [the captives] fighting all the time," she says.

"Finally, the penny dropped," says Jarvis. Corresponding with Richard D. Alexander of the University of Michigan in Ann Arbor, she realized that a naked mole rat colony has only one reproductive female at a time. And as befits a queen, she's almost always the last one to get caught in the trap.

If a group of mole rats lacks a queen, the subordinate females struggle to win her place. "There were sometimes vicious fights for over a year," Jarvis says. Contenders often kill each other, until one female manages to dominate the rest. "Then peace reigns," she adds.

In 1981, Jarvis compared such goings-on to the communal behavior of ants, bees, termites, and the like. Naked mole rats, she said, were the first mammals shown like those insects, to, live in groups that include several generations of workers sharing the tasks of the colony but to have only a single or very few dominant females bearing young. Among the mole rats, both male and female workers dig burrows and collect food.

Borrowing a word from entomologists, Jarvis argued that naked mole rats are eusocial. They've outstripped the rest of mammals and taken their social organization to another level.

In 1982, she finally found queens in the wild. Just how a naked mole rat queen dominates her subjects is still not entirely clear. The queen spends more time than the other adults do patrolling the tunnels. When she meets a mole rat coming toward her, she typically climbs over it, while other colony members pass each other side by side. The queen also rams certain colony members, nose to nose, as if to assert her authority more strongly. "She seems to know who needs shoving," says Jarvis.

Whatever its mechanism, her domineering behavior works. Among naked mole rats, only the queen and the several males she chooses as mates reproduce. "The colony's very aware of her," says Jarvis. "When she's pregnant, both males and females develop teats." Only the queen nurses, but the other colony members undergo hormonal changes and tend the pups.

NOTES FROM UNDERGROUND Bennett says that he got interested in Damaraland mole rats when he came to South Africa in the early 1980s to do graduate work with Jarvis. The two researchers set up the first major field study of the species and brought a colony into his lab.

"I actually thought the animals looked quite handsome," remembers Bennett, who is now at the University of Pretoria in South Africa. They're huskier than the naked mole rats, and their brown or black fur sets off a white blaze on their heads. Also, he says, "they have a very strong smell that is slightly fruity."

Damaraland mole rats turned out to resemble naked mole rats in many ways. Both block off the ends of their tunnels with dirt and survive without regular fresh-air exchange.

Both species dig with their oversize, paired front teeth. They actually bite their way through the ground. The upper and lower incisors emerge through skin above and below their mouths. Mole rats can close their mouths behind the teeth, keeping dirt out of their mouths during excavation.

The teeth continue growing throughout a mole rat's lifetime, and the animals sharpen them by grinding the top and bottom pairs against each other, often as they're dropping off to sleep.

Such equipment permits prodigious digging. From the size of molehills in the wild, Bennett and Jarvis calculated that within the 2 months after a rain, a colony of 16 mole rats had chewed 700 meters of new tunnels and pushed 2.6 metric tons of soil out of their burrows.

The animals tunnel as a way of looking for food without leaving the burrow. Mole rats eat the tubers and roots where arid-land plants store moisture and nutrients. Damaraland mole rats bring chunks back to store in chambers in the burrow system.

Mole rats are also adapted to underground dining. Without regular sun exposure or abundant vitamin D, they use physiological tricks to manage their calcium balance efficiently. Their diet presents the mole rats with a lot of fibrous material that's not easy to digest. Cows cope via an extra stomach where microbes break down the slurry of plant material before it works its way onward in digestion. Mole rats rely on microbial assistance, too, but their microbial richness lies beyond the stomach in a section of their gut called the cecum.

That organ is less efficient than the stomach at absorbing nutrients. Mole rats get around this difficulty by putting their food through their digestive systems more than once.

A defecating mole rat often bends down to fill its mouth, and weaning naked mole rat pups beg adults for a share. When the queen is too pregnant to bend over well, she, too, demands donations from the rest of the colony.

"It sounds strange to us, but it obviously sounds delectable to them," says Jarvis.

The burrow systems also have bathroom chambers, which get walled off after long service.

OEDIPUS RAT Despite the similarities between the naked and Damaraland mole rats, there are differences. For example, naked mole rats give some 18 vocalizations, variations of "squeaking and grunting and twittering," Jarvis says. The Damaraland variety does make "birdlike chirps" but isn't very vocal, says Bennett.

The two species "exhibit totally different reproductive strategies" says Bennett. This may reflect the seemingly independent origin of the extreme colony structure within the two species.

Several family trees based on DNA suggest that the naked mole rat lineage arises from an ancient branch at the base of the family tree. The Damaraland mole rat lineage sprouts higher in the tree, Faulkes says. On the intermediate branches, there are a variety of solitary species and ones that are social but not eusocial.

Naked mole rats breed readily enough with close kin. Although their preference is to outbreed, Faulkes says, "a daughter might kill her mother and mate with her father and take over the colony."

In contrast, observations plus genetic work indicate that Damaraland mole rats don't often mate with close kin. When a Damaraland mole rat queen dies, a daughter does not step into her paw prints, and the colony breaks up.

Even in an operating colony, a Damaraland mole rat now and then tunnels off in search of a new living situation. It may meet up with a like-minded mole rat of the opposite sex for possible colony formation or move into another established colony.

Genetic studies support the scientists' view of such underground hookups. Naked mole rat colonies, without an incest taboo, may end up highly related. When Cornell University researchers Kern Reeve and Paul Sherman checked relatedness of naked mole rats in wild colonies, they found that members had the same version of some 80 percent of their genes. However, Damaraland mole rats in a natural colony match only about half of their genes. That's about normal in a mammal family, Fanlkes says.

The high relatedness of naked mole rats makes the animals' extreme social structure seem less bizarre, says Bennett. Most of the offspring drudge away their lives raising their mother's latest litter. If those nannies are closely related to the pups, plenty of shared genes get passed along.

Yet for years at a time, a Damaraland mole rat colony functions much like a naked mole rat colony, despite the Damaralands' lower relatedness. "For mammals, you don't have to be super related for eusociality to evolve," Faulkes concludes. The costs of going it alone just have to be super high.

Faulkes, Bennett, and Jarvis hypothesize that a lone mole rat couldn't survive the punishing climate with its erratic rain and patchy food. When rain does come, mole rats have only a short time to drive their tunnels into new territory and find food or, if necessary, a mate. A solitary animal stands less of a chance of digging a lucky tunnel than does a bunch of animals.

The researchers contend that it's no coincidence that the two mole rat species living in some of the world's toughest habitats have the most extreme social system.

LAZYBONES One of the puzzles of the mole rats' hivelike colonies has been what technical papers politely call "infrequent workers". In conversation, though, Michael Scantlebury, one of Bennett's colleagues at the University of Pretoria, has been known to say "lazy."

Some of the subordinates in a Damaraland colony seem to simply hang around and eat food that other colony members have found. Making up 35 percent of the group, these loafers do only 5 percent of the work. Understandably, they get fat on such easy living.

Infrequent workers had previously been studied in the lab, but only recently have Scantlebury, Bennett, and their colleagues obtained data from the wild.

Again, the researchers collected all the mole rats from each studied colony. Scantlebury then injected these animals with a substance used for monitoring energy expenditure. He released the mole rats back into their home burrows and, a few days later, recaptured them for measurement.

This was not an easy experiment, says Scantlebury. Outdoors, mole rats evaded the traps easily and often. On one bad-data day, he failed to recapture any of the members of a colony. As hours ticked toward the deadline for getting usable data, "I dug the biggest hole of my life," he says.

Finally, a little flick in the sand tipped him off. Poking at the motion, he found a 3-m-long snake that had slid into the borrow, eaten all the experimental subjects, and bulged up so much that it got stuck in the mole rat tunnel.

Still, Scantlebury and his colleagues managed to get metabolic measurements from nearly 40 animals in seven or eight colonies during a dry period and after rain. In the April 6 Nature, the team reports that during the dry period, the fattest group of mole rats showed extremely low metabolic activity after its return to the burrow.

But during the wet period, all the mole rats got more active, and the difference was larger in the fat animals than in the others.

The freeloading lifestyle may pay off in the long term for the colony. When rains finally permit digging, says Scantlebury, the animals that are well provisioned with fat reserves could be the ones that strike off digging to find new sources of food and, perhaps, to cross tunnels with a potential mate.

A class of couch potatoes doesn't necessarily make a society less sophisticated. Bennett, with perhaps an undertone of irony, calls the supersocial mole rats "the pinnacle of social evolution in the mammals." Even if the Damaraland mole rats never become Disney stars, they offer scientists a new look at high society.