Naked mole-rats are simultaneously the ugliest and cutest animals in the zoo. They've been described as hotdogs with teeth. And yet, so cuddly! What makes them so endearing to me and my kids is the fact that they live together as a big family unit and that they pile up when they get chilly. Also, uniquely for a mammal, naked mole-rat colonies are eusocial, like ants and termites. They have a queen that controls colony reproduction and several subordinate females that help to take care of the pups. But why do these females so willingly offer their care? A recent paper in PNAS led by Akiyuki Watarai from Azabu University, Japan, and his colleagues from several Japanese institutes determined that the cue to help lies in the queen's feces.
Watarai and his team observed that subordinate females were most willing to provide care to the queen's offspring, also called alloparental care, during a limited time window after pups were born. In other words, help was induced by something transient. But what was the trigger? They reasoned that the queen was manipulating subordinates using chemical cues transmitted in her feces. This isn't as odd as it sounds. Naked mole-rats regularly consume feces to supplement their diet and the subordinates were routinely nearby the queen, providing ample opportunities to partake of the tasty morsels. To test this idea, the researchers fed subordinate females pregnant queen's feces and found that they increased their responsiveness to pups. This provided unambiguous evidence that poop was the culprit, but didn't yet clarify which part of the poop elicited the response.
Feces contains many things: digested and undigested food, bacteria, and lots of bits and pieces of everything else going on in your body, both good and bad. This is why doctors so often take fecal samples as a read-out of your health. It turns out that the feces from pregnant mole-rat queens also contains elevated levels of the hormone estradiol, the chemical that stimulates parental care behaviors. Strikingly, when the team fed subordinate females food pellets or feces from non-pregnant queens that were supplemented with estradiol, these both induced parental care behaviors in subordinates. By contrast, unsupplemented feces from non-pregnant queens had no effect at all – other than providing a nutritious snack. Thus, by transferring hormones to subordinate females via their poo, queens can make subordinates motherly.
As cool as this is, it is unlikely that the mechanism of hormonal transfer in naked mole-rats is generalizable. Most animals are rightly averse to consuming feces. But the process of chemical coercion in social organisms is undoubtedly widespread, as long as there is a route of transfer. Social insects and some rodents carry out similar behaviors using pheromones or other odorants, but this may not work in the poorly ventilated tunnels where mole-rats live. Coprophagy – eating poo – by contrast, is both effective and reliable in this context because it takes advantage of an intrinsic eagerness to consume feces to supplement their diet and will occur preferentially in animals that are close to the queen and therefore already socially vetted. But did fecal hormonal transfer evolve as a means of behavioral manipulation, or simply as a fortuitous byproduct of the fact that queens naturally secrete pregnancy-associated hormones and mole-rats eat poop anyway? If the former, you might predict that queens produce excess estrogen beyond their own physiological requirements, or that the amount is conditional on the presence or number of subordinates. Regardless of the answers to the many remaining questions in this system, the result is fascinating. And bizarrely, it only serves to make these hideous beasts even more adorable.