The extreme sociality of naked mole-rats

There are very few animals stranger than the naked mole-rat (Heterocephalus glaber). As their name suggests, these are small rodents that live underground — although they are not very closely related evolutionarily to the mole we know in Israel. And they are also naked, meaning they have almost no fur. Their skin is pink and wrinkled, and they have a rather strange face, with small eyes and long teeth. While it is a matter of opinion, it is certainly possible that this is the ugliest animal in the world. Naked mole-rats live in East Africa, and as mentioned, they are strange — or, to put it more scientifically, they have a number of unusual characteristics. Unlike most small rodents, which live at most four to five years, naked mole-rats can live for more than thirty years, and they are much less sensitive than other mammals to diseases of aging and also to cancer. They are also resistant to certain types of pain: inflammation, for example, does not bother them at all. In addition, the naked mole-rat is among the few mammals that almost do not regulate their body temperature: their temperature changes according to the ambient temperature, as seen in reptiles ("cold-blooded").

And finally, the naked mole-rat has a lifestyle that is almost unique among mammals, and more similar to what we know from certain insects, such as ants or bees. The mole-rats live in colonies with a queen, one to three "kings" or breeding males, and a large number of workers. The queen and the males she chooses as her partners are the only ones who produce offspring. The workers are infertile and are in a pre-pubescent state. Their role, like the role of worker bees in a hive, is to care for the offspring, provide food, and guard the colony.

Eusociality: True Sociality

True sociality, living in a group, and joint rearing of offspring are very common in nature. In many bird species, the male and female both incubate the eggs and provide food for the offspring, and some, for example, the superb starling (Lamprotornis superbus), are helped by other birds from the group that also feed the chicks and guard them. Lionesses guard the cubs of their group members and even nurse them. In meerkats (Suricata suricatta), the whole group helps raise the offspring of the dominant pair. But this type of sociality is very different from what we see in social insects, such as ants, bees, and termites. In them, there is an entire class of non-reproducing workers, and their lives are dedicated to serving the group and raising the next generation, all of whom are the sons and daughters of the queen. In many cases, the queen is helpless without the workers, who care for her and feed her. All individuals of the hive or nest work for a common goal, with different groups filling different roles: defending, building, gathering food. Some researchers refer to the entire nest as a superorganism, one creature with many parts. Such a way of life is called eusociality, or "true sociality".

Over the years, various definitions have been given to this concept. Edward Wilson, the founder of the field of sociobiology who studied social insects extensively, together with Bert Hölldobler, defined three criteria that an animal must meet to be considered eusocial:

1. Division of reproductive labor — that is, there are individuals who reproduce and sterile individuals who help them.

2. Cooperation of group members in raising the offspring.

3. Overlap between different generations, so that the older individuals can care for the young.

The last two criteria are very common in the animal kingdom, so the most important criterion is the first: division of reproductive labor. And indeed, some of the later definitions focus on it, according to which an animal is eusocial only if it has a layer of individuals who are not capable of reproducing at all. If the dominant pair is the only one that produces offspring, but the rest of the individuals are biologically capable of reproducing — this is the situation, for example, with meerkats — the animal is not considered eusocial according to this definition, but as having "cooperative breeding". Other researchers noted that, like almost everything in nature, sociality is not a binary case of "yes" or "no", but a spectrum, and eusociality is only an extreme case of it. According to this approach, one can classify species as "closer" or "further" from eusociality.

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Mole-rat or bee?

Among mammals, there are very few species that show eusociality in all its glory, with clear reproductive division and suppression of fertility in individuals who do not reproduce. The naked mole-rat is the most well-known and studied, but there are also a number of other species that live in a very similar way, among them the Damaraland mole-rat (Fukomys damarensis) from southern Africa and perhaps even other species of mole-rats — they have not been studied enough for us to know this for sure. In the past, researchers thought that the naked mole-rat was evolutionarily very close to these species, and placed it with them in the mole-rat family (Bathyergidae), but a re-examination more than a decade ago placed it in its own family, the naked mole-rat family (Heterocephalidae).

Naked mole-rats live in underground colonies of up to 300 individuals, but only the queen and up to three males produce offspring. The rest are in the status of workers, and as mentioned, are not fertile. They gather food — mainly roots they find underground — feed the pups, dig tunnels and reinforce them, and protect the colony from invaders, just as worker ants and bees do. When the queen dies, the workers become fertile and some of them begin to show sexual behaviors. At the same time, a struggle for succession begins, when the females of higher status fight each other, sometimes to the death. This continues until one of the females wins, becomes pregnant, and takes her place as the new queen. However, a case of queen replacement without violent struggle was recently documented.

How does the queen suppress the fertility of the workers, and with it the aggression of the females, which erupts the moment the colony is left without a queen? Over the years, researchers have proposed various possible answers to this question. Some suggested that the queen, being larger and stronger than the other individuals, demonstrates her dominance by pushing the workers and even climbing on them. As a result, the lower-ranking mole-rats are in a constant state of stress, which affects their behavior and the hormones in their body. Others thought that, like with ants and bees, the queen secretes a pheromone, a molecule that is picked up by the workers and affects their physiology, including the levels of hormones related to reproduction.

The mole-rat pheromone

In a study published recently, researchers discovered that the queen does indeed release a certain molecule capable of suppressing the fertility of the other mole-rats. They collected chemical samples from hundreds of colony members of different ranks and ages, and found that isopropyl myristate, or IPM for short — a substance that is also used in various cosmetic products — is secreted by the queen, but not by the workers. When the researchers removed the queen from one colony, but sprayed it every day with IPM, the workers did not become fertile. "It's an extremely effective contraceptive, if you're a naked mole-rat," said Lewin. Their behavior also did not change, and the females did not start attacking each other, as happened after they stopped spraying the substance. "We created peace and quiet," said Gary Lewin, the senior researcher who signed the paper, in an interview with the New Scientist website. "This is probably the most dramatic result."

How does one molecule cause such a significant change, both in behavior and in physiology? The researchers showed that IPM activates different areas in the brains of naked mole-rats, including the hypothalamus, which is responsible, among other things, for the production of various hormones. In non-reproducing mole-rats exposed to the molecule, the level of the hormone prolactin increased, which in turn inhibits the release of hormones related to sexual maturation and the development of reproductive organs, such as progesterone in females and testosterone in males. Prolactin is important for milk production in mammals, and in nursing mothers, its level is higher than normal. This is the reason why nursing mothers usually do not ovulate and do not have a period (although it is important to note that there are many exceptions to this rule, and many babies were born to those who relied on it as a contraceptive). The changes in hormone levels apparently also affect the behavior of the workers, keeping them in a calm and peaceful state.

The queen spreads her scent

IPM is not a very volatile molecule, and it does not pass easily through the air. How does it reach everywhere in the colony, and affect every single individual? It seems the queen takes care of this specifically. "It is known that the queen patrols all the edges of the underground colony, which in nature can reach three kilometers," said Lewin. "This is how she ensures that all members of the colony are exposed to the scent." Also, the queen's habit of climbing and crawling over the workers in the narrow tunnels helps her spread her scent effectively, directly to the noses of her subjects. This raises an interesting question: if the scent reaches everywhere, then it surely reaches the nose of the queen, who produces the molecule, and the noses of the males with whom she mates. And yet, the queen and her chosen males maintain their fertility. How does the queen manage to avoid the influence of her own scent? Researchers still do not have a clear answer to this, but there are hypotheses. They suggest that when a female reaches the status of queen, she undergoes physiological changes that cause her to stop responding to the molecule. It is possible, for example, that she has fewer receptors in the brain for prolactin, and therefore she does not respond in the same way to the increase in its level, or that there are differences between the queen and the workers in the receptors for IPM itself. The same changes may also occur in the brains and bodies of the breeding males after the queen chooses them, although we do not know what causes them. For now, these are not much more than guesses — further research will be required to answer this question.

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From dryness to sociality

The new research revealed how the eusocial society of naked mole-rats functions, and how the queen ensures that the workers remain infertile and do not threaten the social order. It does not explain, however, how eusociality developed during evolution. Such a situation is very rare in mammals — why did it appear specifically in naked mole-rats, and probably a few more species from a close family? There is still no single answer to this either, and there are several hypotheses that are not necessarily contradictory. One of the central ones attributes the development of eusociality to the harsh environmental conditions that the naked mole-rat has to deal with. Mole-rats feed on roots and tubers, but they live in dry areas where it is difficult to find such treats. On the other hand, when they find a large tuber, it can feed several mole-rats. A large colony with many individuals thus has a better chance of finding food that will be enough for everyone. In addition, when there are more individuals, it is easier to dig and maintain long tunnels, especially in areas where there is not much rain, and the soil is dry and hard. According to this hypothesis, the difficulty of obtaining food and maintaining the tunnels leads to the fact that the better strategy for the pups is to stay with the parents in the colony, so that everyone can share the tubers they find — and not go out alone for an independent life. This leads to larger groups, in which several generations live together. It is easy to see how in such groups a situation can develop where the older siblings help in raising the younger ones. Since siblings share on average about half of their genetic material, caring for their younger siblings also helps some of their shared genes to pass to the next generation.

The first problem with this hypothesis is that living in a large group, and even helping in raising the offspring, does not require eusociality and the division of individuals into queen and workers. Many animals help each other to care for pups or chicks, without being eusocial. However, one can think of a way in which the staying of the pups in the group where they were born eventually leads to eusociality. In such a case, the offspring have no one to reproduce with, except their siblings or parents — a very unrecommended thing, which increases the risk that genes with harmful mutations will be expressed. It is possible that there is an advantage, therefore, to a situation where the parents are the only ones who reproduce, and the fertility of the rest of the group members is suppressed. Those individuals who cannot reproduce contribute to the passing of their genes in the only way left to them — by caring for their siblings. Thus, one can get from offspring that stay with their parents, for example due to the difficulty of obtaining food, to the division of reproductive labor that characterizes eusociality. Another argument against the environmental conditions hypothesis is that there are quite a few other animals, including those that live in tunnels and feed on a menu similar to that of the naked mole-rat, that live in the desert and are not eusocial — or even do not live in groups at all. On the other hand, animals develop adaptations of various types to their environmental conditions, and the fact that not everyone who deals with a food shortage becomes eusocial does not mean that these conditions did not influence the evolution of eusociality in the naked mole-rat.

The genetics of sociality

Another hypothesis for the development of eusociality concerns the genetic closeness between group members. In ants and bees, there is a special inheritance mechanism that leads to greater genetic closeness than usual between the workers. To understand it, let's first describe how the inheritance mechanism works for us. Each of us has 46 chromosomes, each of which is a long DNA molecule. These chromosomes are actually a double set, two systems of 23 almost identical chromosomes. One system of 23 chromosomes we received from mom, and the second from dad. This is the mechanism in most animals and plants, with a varying number of chromosomes. In insects from the Hymenoptera order, which includes bees, ants, and wasps, not every individual has such a double set. The females receive one chromosome system from their father and the second from their mother, the queen, just like us. But the males develop from eggs that were not fertilized with sperm, so they have no father at all — they receive only one chromosome system, the one that came from the mother. This fact affects the genetic closeness between the workers. For us and most animals, full siblings share, on average, half of their genes. This is because each of the parents passes half of their genes to each of the children, and, on average, there will be a fifty percent overlap in the genes they will pass to each. In Hymenoptera, the father passes all his genes, the only set he has, to all his daughters — so they all receive the same genetic material from the father. The mother, in contrast to him, still passes half of her genes to her daughters. It follows that workers who are full sisters share 75 percent of their genes, on average, with their sisters — much more than with us. Such an inheritance mechanism can contribute greatly to the development of eusociality, because when the workers care for their sisters, they help their genes to pass to the next generations — and they share with them, as mentioned, a very large part of the genes, more than parents share with their offspring. If there is a gene that causes a worker to feed her sisters and care for them, there is a high chance that it will be found both in the worker and in the young ant she is caring for. The young ant will benefit from this, it will have a better chance to survive, and thus the gene will spread in the population. However, the inheritance mechanism of Hymenoptera does not guarantee eusociality — there are insects from this order, such as various species of wasps, that are not social at all — and one can reach eusociality even without it. Termites, for example, lead a lifestyle very similar to that of ants, even though there is no greater genetic closeness than usual between the workers in the nest.

A mystery in the form of a naked rodent

And what about naked mole-rats? Their genes are inherited exactly like our genes and the genes of all mammals, so siblings are not genetically special. But various studies in which researchers examined the genetic material of the mole-rats showed that they have more inbreeding compared to other mammals, something that increases the genetic similarity between colony members. Animals usually avoid mating with their close relatives, and there are various means to ensure this — for example, in many species, either the females or the males leave the group when they reach maturity and move to another group. It is possible that things are different for naked mole-rats: experiments showed that their new colonies can be formed when all the pups, males and females, stay together with the parents. However, later studies showed that there are colonies of naked mole-rats in which the genetic closeness between siblings is about fifty percent, as we would expect, and not higher due to inbreeding. It is possible that there are colonies in which the genetic closeness between their members is higher, perhaps due to external conditions that made migration between groups difficult, but it seems that this is not the rule for all naked mole-rats.

The two hypotheses we presented here do not contradict each other, and perhaps even complement each other: it is possible that the harsh environmental conditions led to the formation of large groups, and to the suppression of the tendency to leave the group in which one was born. The staying of males and females in the same group can lead to inbreeding, which increases the genetic similarity between colony members, and supports the evolution of helping and caring for offspring. However, genetic closeness alone does not explain the phenomenon, and as mentioned, inbreeding is not a necessary characteristic of all colonies. Some of the special characteristics of naked mole-rats are also likely related to eusociality — especially their long lifespan, and slow maturation. Naked mole-rats can live more than thirty years, longer than any other rodent. Females remain fertile until around age 28. Due to the long lifespan, several generations can live together in the colony, with the first ones caring for the last ones. Naked mole-rats also mature slowly compared to many small rodents, and therefore the offspring require care and feeding for a longer time. As a result, it is harder for the mother to raise them without help from group members — which she of course receives in abundance in this case. Did the long lifespan and slow maturation contribute to the evolutionary development of eusociality? Or perhaps eusociality and the joint rearing of offspring that it includes allowed the pups to mature more slowly? It is difficult to answer this question, and it is also possible that these traits feed each other and developed in parallel. There are still very many things that we do not yet know about naked mole-rats — both regarding their special lifestyle and how it developed, and regarding their other unusual characteristics. Researchers will certainly continue to uncover their secrets for many years to come.

Dr. Yonat Eshchar, Editor-in-Chief of the Davidson Institute of Science Education website, the educational arm of the Weizmann Institute of Science.