Not just another pretty face

Not just another pretty face – naked mole rat

Elizabeth Pennisi

A naked mole rat peeks out of its burrow, and Richard Alexander signals silently to Paul Sherman, who’s crouched in a ditch near the opening. Sherman slams a hoe into the dirt by the mouth of the burrow, hoping to block the animal’s escape back underground. ”Missed,” he mutters under his breath.

A second nose appears. Sherman lunges, this time with forceps inhand. Snap! and he has the critter by the tail–his first naked mole rat. His fellow hunters applaud; the animal hisses and grunts. Down below, other mole rats, alarmed by the vibrations resulting from the scuffle, swiftly plug the tunnel and scatter.

Naked mole rats resemble baby rats and live like moles, but are in fact neither. They’re specialized rodents thought to be distantly related to porcupines, and are found in arid regions of Ethiopia, Somalia, and Kenya, where they’re often as common as field mice in Iowa. Colonies of ten to 300–the average is 75–live in vast subterranean networks of tunnels and chambers, subsisting on roots and tubers. Since mole rats never need surface, most Africans know them only as unseen pests that eat their cultivated yams and undermine roads.

Subterranean life has transformed the naked mole rat into one ofnature’s ugliest and oddest creatures. The ugliness is apparent, but the oddity, slowly revealed to scientists, is the as- tonishing fact that naked mole rats behave more like social insects–termites, ants, wasps, and honeybees–than mam mals. Mole rats are organized in colonies dominated by a queen, which is the only female to reproduce; all the others–male and female– work to protect and provide for her and her babies.

In crossing a behavioral barrier separating invertebrates from their bigger-brained, back-

boned brethren, mole rats have stirred up vigorous debate over why and how such an unexpected social system evolved. Most social behaviorists have assumed that mammals, people included, can’t cooperate to the extent that social insects do. Among insects that establish queen-worker relation- ships (except termites), sisters are more closely related to each other than they are to their mothers. As a result, a female worker passes on more of her genes by helping to raise her sisters than by laying her own eggs. Mole rats follow the same reproductive pattern, although they lack the insects’ close genetic relationship with their sisters. The question is: Why do they display so much team spirit?

Complex insect societies with queen and worker castes have long fascinated Alex- ander, an entomologist who’s a world-renowned expert on crickets and a curator of insects at the University of Michigan’s zoology museum. He felt that the social behavior of ants and bees wasn’t adequately explained by their genetic relationships. A decade ago he published a paper exploring the premise that workers were help- ing the queen because she was forcing them to. If their behavior wasn’t a matter of peculiar genetics, he reasoned, ”then this type of social system could also be found in vertebrates that cared for their young. I hypothesized a mammal.”

Alexander’s theoretical mam- mal would have to live like a termite–in a self-contained environment that was safe, but with risks that enabled workers to act heroically to help pro- tect the queen. Since even the smallest mammal would require more room to live in than a termite, a burrow- dwelling rodent was the most logical candidate. Because it would need access to enough food for the whole colony without having to surface, tropical Africa, where giant tubers are abundant, would be an ideal habitat.

By chance, in 1976 a mammalogist heard Alexander discuss this imaginary creature and told him his description fitted the naked mole rat precisely. ”What the hell is a naked mole rat?” Alexander asked, whereupon he was presented with several pickled specimens and told about the work of Jennifer Jarvis, a biologist at the University of Cape Town in South Africa and the grande dame of mole rat research.

For more than a decade, Jarvis had been studying the creature that Alexander had hypothesized, and by 1971 she had begun to suspect that mole rat behavior closely resembled that of social insects. At first she couldn’t figure out why she never got more than one female per group to breed in the lab, but after collecting an entire colony and watching it closely, she became convinced that this was the mole rat’s normal pattern.

Jarvis found other analogies to social insect behavior in the way mole rat young are reared. The queen gives birth to litters of up to 27 pups, usually at three-month intervals, and for the first four weeks provides milk for them herself, while her subjects bring food to her. After this, worker mole rats take over care of the young, providing them with nutrients from their feces and bits of food. By the age of three months the pups are ready to take their places as workers.

In 1979 Alexander decided to see for himself just how social mole rats were. He proposed a joint field trip to Sherman, a professor of animal behavior at Cornell who’d spent years studying the social structure of Belding’s ground squirrels in the Sierra Nevada. Sherman had heard of Jarvis’s research on mole rats, and he, too, wanted to observe their unique behavior first hand. As soon as they reached Cape Town, Alexander and Sherman went to Jarvis’s office, where, upon seeing her laboratory colony, Sherman momentarily lost his scientific reserve. ”I don’t know when I’ve had such an adrenaline rush,” he says. ”Here before me was the missing link between vertebrate and invertebrate social systems.”

Alexander and Sherman im- mediately realized that the mole rat could turn the study of social behavior upside down. Here was proof that a species didn’t have to have the bee’s special genetic makeup to have a hierarchical, queen-dominated social system. Here, to, was evidence that even mam- mals, in the right circumstances, readily and permanently gave up breeding–or at least seemed to.

Today, after studying the mole rat for five years, they’re beginning to see that a colo- ny’s apparent harmony is only part of the mole rat’s story. It’s now clear that, along with the cooperativeness and altruism, selfishness and subtle competition also exist. This discovery whets an even deeper curiosity. Their findings, says Alexander, ”could lead, I hope–I think–to a whole new kind of comparison between human social systems [in which virtually everyone reproduces] and those animal social systems with queens and workers.”

Because of their harmony and efficiency, beehives and anthills have often been cited as pinnacles of cooperative social behavior, more sophisticated in this regard than any vertebrate society, with the possible exception of man’s. These ”pinnacles” may have been reached by insects and not mammals because insects have had more time to evolve, or because mammals are inherently more selfish. But the discovery of the naked mole rat’s insectlike behavior challenges those notions; at least this mammal seems to be following the same evolutionary track as social insects. A philosopher might wonder whether hu mans are on the same trail, but Alexander won’t carry his the- sis that far.

During Alexander and Sher- man’s visit to Africa, Jarvis joined them on a field trip to Kenya. Capturing mole rats was harder than the Americans had expected. They could sometimes see a mole rat’s feet as it frantically kicked out dirt from within an eight-inch mound, but the faintest disturbance sent the animals scattering down their burrow. And Alexander and Sherman soon learned that a single burrow system could be more than a mile long. When frightened, the mole rats forsook the narrow tunnels a few inches below the surface for wider throughways about 15 inches down. Most of the animals kept right on going to their capacious, hollowed-out nest chambers two feet underground, but en route some of the larger ones paused in the throughways, heads cocked, moist nostrils quivering. Although mole rats are nearly blind, their eyes can sense air currents that indicate a tunnel has been broken into. They can detect low-frequency vibrations, such as footsteps above, and can sort through the faintest odors wafting down passageways to determine whether an intruder is near. Only when there was no longer any hint of unusual activity did these mole rats re- sume their business.

Alexander and Sherman’s first day of hunting yielded just one animal, so they hired a local mole-catcher, Anthony Simon Ndalinga Chondo. He needed goats to pay his in-laws for his new wife, and agreed to catch mole rats to earn enough to buy them. Even with Chondo’s expert help, Jarvis says, ”it was hit and miss, but very exciting. You’re bent for hours catching them, and the work is very hot, dirty, and hard.” Alexander says mole rat hunting is the hardest work he has ever done.

After two weeks, the Americans headed home with 108 mole rats, including at least one breeding queen. ”It took a while to get them settled in the labs,” Sherman says, ”and each time we tried a new food we were afraid we were poisoning them.” Fortunately, mole rats thrive on yams, carrots, bananas, apples, corn-on-the- cob, dog biscuits–even dough made from moistened baby cereal and served in blobs that look like unbaked drop cookies.

But their housing requirements aren’t as easy to satisfy. At their respective labs, the sci- entists pieced together sections of two-inch glass or Plexiglas tubing to make loops and mazes for the animals. In Africa, mole rats dig out chambers for sleeping and widen dead ends for communal toilets, where the animals urinate and defecate, and then roll around to saturate themselves with the tribal smell. To provide facilities in the lab, Alexander and Sherman placed shoebox-sized containers at tube junctions and tunnel ends. They added food chambers, where the animals could come to find the rations that served as substitutes for serendipitous tubers.

The 35-foot-long plastic burrows run along tabletops and shelvesinside rooms where temperature and humidity are precisely regulated. Although Alexander’s mole rat habitat is maintained under normal room lights, Sherman uses only dim red bulbs, because he thinks bright illumination may distort mole rat behavior. The walls of both labs are extra thick, and the floors are suspended to reduce vibrations, but even a door closing elsewhere in the building can rattle the sensitive creatures. There’s one other chronic problem: as a result of persistent gnawing, about one animal per month manages to chew through the plastic elbow joints, which are replaced as soon as a tiny hole is detected.

By studying the mole rat in the transparent burrows, scientists can appreciate the ingenuity of the animal’s design. Its wrinkled body is soft, and its pink skin loose, allowing it to squirm easily through tight spots. Its squat back legs are bowed and its feet are pronated for running in rounded tunnels. Its heels and long, padded toes are edged with stiff hairs, which makes its feet seem several sizes too big, albeit efficient for sweeping dirt. The mole rat, which can waddle along at 2.5 m.p.h., is one of the few animals–the pocket gopher is another–that can run as fast backward as forward, and it shows little preference for moving in either direction.

The mole rat is also one of the few mammals (and the only rodent) that has lost its fur. This rids it of hiding places for parasites–no small consideration for creatures that live in such close quarters. Nakedness also facilitates the transfer of heat to and from the body. The 80 degrees to 85 degrees temperature and high humidity in mole rat burrows make it unnecessary to conserve body heat as other mammals must. To get warm, the mole rat can huddle with nestmates or go to tunnels near the sun-baked surface; to cool off, it can descend to deeper burrows. With a metabolic rate less than half that of other rodents, it lives six times or more as long as those its size. Nineteen of Jarvis’s original colony are at least 13 years old.

The mole rat’s two pairs of long, slightly curved, and extremelysharp incisors are powered by large jaw muscles that allow it to dig readily through hard ground or chomp tough roots–or bend metal forceps or pierce fingernails. Should a tooth break off, it will regrow in a few days.

As the mole rats scurry along their thoroughfares– walls polished smooth by the constant passage of their bodies, floors grooved by heavy traffic and periodic tidying up by ”janitors”–the creatures’ behavior often recalls scenes from Charlie Chaplin’s Modern Times. A mole rat janitor kicking away refuse in a tunnel will lie down abruptly to nap or lick itself. Another mole rat stops suddenly in the busiest throughway to grind and sharpen its teeth, and then wipe them clean with its long, dexterous fingers. Those lined up behind the stationary mole rats plow into each other and, once traffic begins to flow again, resume their activity without even seeming to notice they’ve been in a pile-up.

At feeding time in the lab, the tunnels are jammed like city streets at rush hour, the en- trances to food chambers grid locked; the animals’ chirps are like cab drivers’ impatient honks. More often, the passageways resemble rural roads on a Sunday morning: a few stragglers are up and about, while most huddle in the nest. Except for the queen, which patrols the tunnels five times or more an hour, mole rats spend almost two-thirds of their lives sleeping or hanging out together.

Since 1980, Alexander, Sher- man, and their students have added many thousands of hours of observation to those already logged by Jarvis and her team. Since nearly all knowledge about mole rats is fresh, almost any experiment can be revealing. At Michigan, graduate students Stanton Braude and Selma Isil have been studying digging behavior and division of labor in mole rat colonies. To monitor their colony’s reactions, Sherman and research assistant Eileen Lacey have plugged tunnels with dirt or Styrofoam, put rootlike obstructions, sand, and nesting material into the burrows, and dropped in live or fake snakes and unfamiliar mole rats. Another of Sherman’s researchers, Hudson Reeve, is studying the breeding female’s role in regulating colony activity.

One of Jarvis’s students, Brandon Broll, thinks the queen maintains her dominance by means of odors and chemicals in her urine (which her subjects then smear themselves with when they visit the communal toilet), as well as by taking advantage of her greater size to bully her subjects.

More arduous research is under way in Kenya, where British behavioral ecologist Robert Brett, of the Zoological Society of London, has spent two years tracking 14 colonies of mole rats through their burrows by means of radio collars. He has also dug miles of ditches to trace tunnels. The colonies he has studied often have several nests, and its members appear to move from one to another with the seasons. In the wet months, from March through May and November and December, mole rats eat carrot-sized roots. During dry seasons, they eat tubers, which can weigh as much as 100 pounds. They leave enough root behind so the tuber will grow back the next year.

Both Brett and Jarvis have discovered that mole rats work hardest and most cooperatively while exploring fresh territory for food. In early morning and late afternoon during the rainy seasons, when the soil is softest, many will work together, digging long tunnels. They organize themselves into a chain of dirt carriers that shuttle between a digger at one end and a kicker at the other. Mole Rat No. 1 digs by bracing itself against the tunnel floor, arching its back and breaking hard soil between its teeth. Skin flaps close off the throat; nostrils and eyelids are shut to keep dirt out. As No. 1 chomps and scratches its way in shoulder-deep, it uses its paws to whisk loosened soil back to Mole Rat No. 2, the carrier, which gathers dirt under its belly, crouches and pushes the pile backward with its feet to Mole Rat No. 3, the kicker. While positioned face down in a shaft leading to the surface, No. 3 flicks the dirt out the opening with its hind legs. Still another mole rat clambers over No. 2 to drag the next pile backward. As the tunnel length- ens, more carriers join this conveyer belt. Should the tunnelers come upon a tuber, they break up into smaller groups and excavate numerous short branch tunnels, seeking other tubers.

The smallest and youngest mole rats of both sexes are the colony’s janitors. They quickly chew off any rootlets that pierce tunnel walls. They tidy floors by kicking loose droppings back to the toilet. They’re also the food carriers: they forage for tubers, and when they find one, they chew off bite-sized pieces that they transport back to where older members of the colony are lounging. The younger they are the harder they work.

The animals’ roles change as they mature. Larger and older mole rats work less but tackle riskier jobs, such as digging into unfamiliar territory. The biggest seem to serve as the colony’s SWAT team, Sherman says. Almost always, a few of them are crouched in the nest like sentinels, facing outward to check the tunnels for threats. In the lab, Alexander and Susan Finger, a re- search assistant, have watched a strong pair ambush a snake. The mole rats attacked it from opposite sides and bit it repeatedly along its length, leaving it lacerated and dying.

Should tunneling mole rats break through into a neighboring colony, battle cries muster all members of both colonies, with the SWAT teams in the lead. Impassioned hisses and grunts spur on warriors from each side. They pair off, gaping mouth to gaping mouth, each hoping to drag the other into its territory for execution. Mole rats seem adept at twisting their heads to avoid being bit- ten, but Sherman has watched one kill another by driving its teeth through the foe’s skull.

Only one other situation seems to arouse such violence: a fight for succession to the throne. Sherman and Lacey twice have robbed a colony of its queen. In one instance, the resulting combat led to nine gory deaths during the 16 months it took another female to become dominant. In the other case, years have passed and no one has taken charge. Once queenless, the members of this colony adopted an every-mole-rat-for-itself attitude. No one sweeps or carries food. Lacking an order of precedence, the animals sometimes crowd nest entrances until all are stuck. They take a long time to untangle themselves because no one seems to want to make the first move. But such behavior may not be the norm: Jarvis has removed queens from four colonies in her lab, and three times the transition to a new breeding female was smooth.

The more researchers delve into the lives of mole rats, the morethey realize how powerful the dominant female is, and how crucial she is to keeping order. Consider the plight of Michigan Queen No. 32. In the first four years of her reign after arriving in the lab, she was unchallenged as her colony’s leader. When she huddled in the nest, one of the three males she chose as mates always at- tended her; she got first pick of any food. Periodically she arose and jogged through the colony, checking on subjects. If she met one, she’d nuzzle its rear or face, sniffing to assess its reproductive status and whether its hormones were in check. Her own odors probably serve as a chemical

whip that demands submission. Sometimes her greeting was like a gentle kiss. At others it was forceful, accompanied by a harsh shove and an irritated nip. A rebuff from her would make any subject cower.

But now Queen 32’s empire is crumbling. A golf-ball-sized abscess on her right shoulder makes climbing over subjects difficult. As if insecure, she patrols more often. The colony seems unsettled, its members less submissive. Graduate student Braude could remove the abscess to help the queen recover her health. Instead, he has chosen to watch her decline, to witness the natural succession of mole rat power.

Is a healthy queen a tyrant that has enslaved the colony? Or a benevolent despot that uses power to make the colony run smoothly? When hungry, she prods her subjects to work. When satiated, she lets them rest. When conditions are normal, her autocracy seems to benefit all.

At the beginning, investigators thought mole rat colonies might be just like thos of termites, which are sometimes described as superorganisms, with individuals serving as the body parts. A mole rat colony might also be a sort of superorganism. Digging mole rats would be the big toes; food- carriers, the fingers; and the queen, the womb. By working together, the components of the superorganism are more efficient than each would be on its own–in part because the group is freed of wasteful rivalries between individuals.

However, experiences with queenless colonies, and now with No. 32, have prompted scientists to look beyond the mole rats’ apparent altruism. Do they work together because the queen forces them to–or because it’s really to their advantage to do so? Why do food carriers, when very far from the nest, sneak a snack before bringing the root bits back for the rest of the group?

There are other marked distinctions between mole rats and insects like honeybees or termites, whose nests contain thousands, sometimes millions, of members that differ in size, shape, and longevity. Like true body parts, the members of such colonies know their place and keep it.

By contrast, mole rats seem to be more like sweat bees and paperwasps, which live in smaller congregations and appear to require aggressive queens to maintain social order. These insects’ nests contain hundreds, not thousands, of members, giving each worker a much greater theoretical chance to reproduce than a termite or honeybee. Significantly, unlike female termites and honeybees, female sweat bees, paper wasps, and mole rats are more like their queens and can quickly replace them or produce their own offspring.

Interpreting mole rat cooperation requires further work, Shermanhas concluded. For example, when in a tunnel-digging brigade, the No. 2 mole rat tries to displace No. 1, its actions may be altruistic: it may be bigger and better at digging. Or No. 2 may be selfish: it may only want to be the first to find food, or the first to have a chance to escape the queen’s control, breed on its own, and establish a new colony.

Perhaps mole rats live in such tightly knit groups simply because, alone, they couldn’t dig far enough to locate the widely scattered roots they need to survive. Perhaps they formed these groups so that together they could build underground fortresses to thwart predators. If that’s the case, they’ve evolved a very sophisticated means for doing so, even while–deep down–individuals may harbor a drive to be less cooperative.

”I tend now to believe the mole rat colony isn’t a su- perorganism,” says Sherman. ”There’s conflict of interest; there are individuals still striving for their own reproduction at the expense of others under the surface of this amazing apparent cooperation.”

COPYRIGHT 1986 Discover

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