How Eating Poop Makes These Mole-Rats More Motherly

New research suggests a colony’s queen stimulates babysitters by transferring a type of estrogen through her feces

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These wrinkly rodents continually surprise researchers. Meghan Murphy, Smithsonian's National Zoo / Flickr

In the animal kingdom, "it takes a village to raise a child" is often the norm. Rather than putting the burden on one pair of parents, often an entire social group of animals will care for newborns. Marmoset moms hand off their young to other males, who spend so much energy carrying around the babies that they lose weight. Subordinate wolves and wild hogs that have lost their own litters nurse other pups. Even ducks aren’t shy about letting someone else watch their ducklings for a bit while they grab a quick mouthful of algae.

This behavior, called alloparenting, likely has evolutionary advantages that we don't fully understand (it occurs in 9 percent of the known species of birds and around 3 percent of mammals). But we do know that those urges to lick and feed someone else’s baby are nurtured along by caregiving lessons learned early in life and a few squirts of affection-inducing hormones like prolactin, oxytocin and estrogens, though researchers haven’t figured out exactly how the system works. Add to the list of questions about alloparenting the behavior of the naked mole-rat. Members of naked mole-rat colonies take care of babies that aren't their own, despite not being able to produce their own estrogen. Now, new research published in PNAS suggests that they receive estrogen—and their motherly instincts—from a very unusual source: mole-rat feces.

The naked mole-rat, Heterocephalus glaber, is a rodent found in the Horn of Africa that lives in colonies like ants do. In the colony, only one mole-rat, the queen, is sexually mature, while subordinate handmaidens take care of her offspring, licking them, building nests, and keeping them warm. But that system baffled researchers at the veterinary school at Azabu University in Sagamihara, Japan.

Azabu researcher Kazutaka Mogi writes in an email that his team had studied alloparenting in mice, where non-moms babysit other pups. The babysitters' maternal instincts seem to be strengthened by estrogen, which the mice produce in their ovaries (just like human women). It's a virtuous cycle in which the more alloparenting a mouse does, the better she gets at it—and the more her hormones push her to do it. But naked mole rats engage in alloparenting despite having no mature sex organs. "We were surprised to hear this phenomenon and decided to investigate this subject,” he writes.

That's how the researchers stumbled onto the revolting discovery. Coprophagy—eating feces—is common among naked mole-rats. The team wondered if the subordinates could be receiving not just nutrients but hormones from eating the queen mole-rat's poop.

Researchers fed the naked mole-rats poop pellets from a pregnant queen. They then tested their estrogen levels and their response to the yipping sounds of naked mole-rat pups. The study showed that the estrogen levels in the would-be alloparents gradually rose throughout the queen’s pregnancy, peaking after the queen gave birth to her litter and was done feeding them, the time when the subordinate females more or less take over care of the young. The study showed that after eating the hormone-laced feces, the subordinates became super-responsive to the mewling pups. This poopy hormone transfer represents a previously unknown system of communication between the mole-rats.

Coprophagy is not uncommon in mammals, as many people with a dung-eating dog can attest. In many cases, especially among rabbits and rodents, it’s a normal part of digestion. There are certain nutrients that their guts can’t process in the first pass, so they ingest their own fecal pellets for a second go. Some baby animals, including elephants and hippos, also eat their parent’s caca soon after weaning to help seed their guts with the right intestinal bacteria.

It’s likely that naked mole-rats do both. In their extensive underground colonies, the animals maintain a toilet chamber where feces pellets are deposited. It also serves as a snack room, where they get a second chance to nom on the poo and digest the fibrous roots and tubers that they munch on. Mature mole rats have also been observed pooping directly into the mouths of young pups, which is probably to transfer gut bacteria and to help impart a “colony” smell to the younglings. Each naked mole-rat colony has its own specific odor, and if an intruder doesn’t have the right smell, it will be ripped to shreds.

Mogi says he and his team are unaware of any other mammal—or any creature for that matter—that transfers hormones in this manner. However, in a 2016 paper in eLife, researchers found that carpenter ants exchange food, pheromones and hormones via trophallaxis, which is essentially throwing up in one another’s mouths. It’s possible that other social insect species engage in similarly revolting forms of communication.

It’s possible that other mammals transfer hormones via feces, though it wouldn’t be surprising if naked mole-rats are the only ones: The strange animal that National Geographic describes as “bratwurst with teeth” is unique in almost every way. Besides having a society set up more like bees than mice (one of only two mammals to live in such a way), they live in underground colonies and are functionally blind. And they are indeed naked, with just a few hundred hard-to-see guide hairs and giant, sensitive buckteeth to help them navigate their dark labyrinths. While most rodents of a similar size live two to three years, naked mole-rats can live up to 30, and are thought to be almost completely immune to cancer, which has made them popular research animals. They can also survive up to 18 minutes without oxygen and are essentially cold-blooded, unusual for a mammal, and must cuddle together to regulate their body temperature in cold weather.

“I think it’s funny, on the surface they look different but you don’t think about all the cool things we know about them,” say Kenton Kerns, assistant curator of small mammals at the Smithsonian’s National Zoo, who deals with the mole-rats on a daily basis and is preparing to unveil a new colony. “And it seems like once a year if not more there’s cool new research about them. You know how grade school teachers tell children we shouldn’t cut down the rainforest because it might have the next new medicine or scientific breakthrough? Mole rats are like that, but people just slide by their exhibit saying ‘I don’t like rats or mice.’”

Diana Sarko has been studying naked mole-rats for years and currently maintains two colonies at Southern Illinois University ruled over by "Queen Cersei" and "Queen Daenerys." Her main research involves their giant teeth, which are essentially a sense organ—though her recent work has found they have the same bite strength as a lion. Sarko regularly sees alloparenting behavior taking place with subordinates moving pups around and snuggling them in the warm sleeping chambers. She isn’t surprised by the idea that hormones could be transferred via feces, though she hasn’t witnessed much poo-munching in her colonies since the food the lab animals get, like sweet potatoes, fruits and other vegetables, might be easier to digest than wild tubers.

In fact, hormones may regulate other activities within mole-rat colonies. Just last year one of Sarko’s queens was killed by a usurper.

Typically, a mole-rat queen can expect to sit on her throne into her twenties without an uprising, so the revolution in the lab colony was unexpected. “Once established, a queen usually stays put,” Sarko says. “She was overthrown after having a litter so she was somewhat weakened but otherwise she seemed healthy. I was shocked.”

Now, Sarko and her team are examining hormone levels, including the stress hormone cortisol, collected in their weekly poo samplings in the months leading up to the coup to see if hormonal changes were happening throughout the colony before the overthrow of their queen.

It doesn't end there when it comes to mole-rats and hormones. Mogi says the Azabu team has preliminary evidence that the queen has a way to influence the reproductive success of the tiny handful of sexually mature males allowed to breed with her. It’s not clear yet if it involves feces, urine, vomit, saliva or is just the naked mole-rat version of the come-hither look.

A new 24-hour webcam trained on the National Zoo's colony of naked mole rats goes live on August 31, 2018. Visitors can see the Zoo's new habit for its colony of 17 naked mole rats beginning September 1.

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