The unforgettably ugly naked mole rat, Heterocephalus glaber, lives in underground burrows in East Africa, in colonies that sometimes number several hundred members. Nearly all of those animals are nonbreeding virgins. Only the queen mole rat and her small harem of select males procreate, producing litters of pups every 80 days. Meanwhile the virgins forage, dig tunnels, defend the nest, and doze--that is, when they are not getting stomped on by the queen. She enforces her exclusive breeding rights with a reign of terror. Through shoves with her head, and throaty, raspy threat calls, she so bullies her female subordinates in particular that they fail even to ovulate.
The queen’s domination, however, is not as complete as was once thought. Susan Margulis, an evolutionary biologist at the University of Chicago, and her colleagues have discovered that there are always a few usurpers waiting for the mole rat queen to falter. Like the queen, these females have enough reproductive hormones coursing through their veins to render them fertile. As long as the queen is around, they take the brunt of her fury; as soon as she is out of the picture, they fight to the death to succeed her.
Margulis and her colleagues studied a 40-member mole rat colony at the Brookfield Zoo outside Chicago. For nine months the researchers carefully monitored the animals for aggressive, queenlike behavior-- basically keeping track of who shoved whom. They also sampled the animals’ urine for progesterone, a hormone produced by the ovaries that prepares the uterus to receive a fertilized egg. A high progesterone level indicates the female is ovulating.
To the researchers’ surprise, three of the subordinate females, females 8, 14, and 28, showed progesterone levels high enough to suggest that they could conceive. The queen seemed aware of the challenge: she performed nearly all the shoves the researchers observed, and she aimed most of them at the most fertile subordinate, female 8. Females 8 and 28 did the rest of the shoving, directing their attacks not at the queen but at lesser rats.
Three months into the study, the researchers removed the queen from the colony. Females 8, 14, and 28, whose progesterone levels remained high, thereupon began showing queenlike behavior--not only shoving more often but also lying end to end with other rats, sniffing and licking their genitals. Though this behavior is especially common between a queen and a breeding male, says Margulis, the queen also nuzzles females. She may thereby obtain some chemical cue that tells her which of her subordinates have the hormonal wherewithal to reproduce and are therefore in need of a good shove.
In the weeks after the queen was removed, female number 8--second after the queen on the progesterone ladder--did the lion’s share of the shoving and nuzzling, with females 14 and 28 doing the rest. But two months into the new regime there was a coup. The keepers came to me one morning, and their faces were ashen, Margulis recalls. And they said, ‘Well, females 28 and 8 had a fight.’ Female 8 was dead; female 28 was alive but badly bitten.
Female 28’s reign as queen did not last the night. The next day the keepers found her dead--along with female 14, at the opposite end of the exhibit. The two mole rats had apparently crawled off to die after eviscerating each other.
With all the pretenders thus eliminated, the drama was reenacted by females 22, 32, and 36. Female 22 was showing higher levels of progesterone. But then she was attacked by female 32, who (confusingly) showed no signs of ovulating. That prompted female 22 to abandon the struggle: she stopped shoving, and her progesterone levels dropped. About this time the hormone levels of female 36 began to rise, and she began shoving a lot. Ultimately she became queen.
Hormones alone don’t make a mole rat queen; some complicated feedback is at work between hormones and behavior, and between queen and subordinates, that isn’t fully understood yet. But the presence of fertile insurgents, while adding to the violence of mole rat life, may benefit the whole colony. In the wild, says Margulis, if a queen died and no female was ready to breed, the number of animals might decline so much that the colony would go extinct.
