Monkeys checking each other for fleas on concrete fence in a park. pittawut / Shutterstock

People Aren't Altruistic. It's the Bacteria They Carry, Israeli Scientist Suggests

Do we help each other only because we're manipulated by bacteria? Evolutionary biologist Lilach Hadany says this explains the evolutionary riddle of altruism



One day, when my daughter was 3 years old, we went into a bookstore and came across Shel Silverstein’s “The Giving Tree” – which is called “The Generous Tree” in the Hebrew version. My daughter asked me what “generous” was, and I explained that someone is generous if he gives others something that is his. “It’s worthwhile being generous, right?” My face glowing, I caressed her head. She looked at me with glittering eyes and said, “It’s worthwhile to be the friend of a generous person.”

That, if you will, is the naked formula of the problem of altruism, in nature. Or, to put it another way: How did generous behavior – the forgoing of resources in favor of the Other – evolve in nature, when obviously it’s better to be the Other, the one on the receiving end?

Put aside human altruism – moral, ethical, educational – for now. In the war of survival that’s waged in nature over limited resources, the winners will be those that are best able to exploit those resources. That’s what Darwin taught us. Altruistic behavior – as expressed by helping another, acts of generosity, self-sacrifice – is the opposite of that. Biologically, altruism is defined as behavior by an individual who augments the fitness of another individual at the expense of his own fitness. And fitness, in nature, is a decidedly utilitarian matter: It represents the individual’s chances of surviving and begetting offspring.

Looked at in simple terms, we would expect selfish behavior to survive, as it’s the selfish being that obtains the resources – not the generous one who distributes them – whose fitness will be bolstered, and who will have offspring that will match him in terms of selfishness.

The legacy of generosity, then, should have disappeared from the world. Yet, generosity, helping the Other and even sacrificing something for the general good are phenomena that exist in abundance in nature. A wolf going out to hunt for food invests time and energy and endangers itself, but when it returns home, to the pack, it will share its food with others that did not take part.

Examples of generosity of a different type: Gazelles and other animal species manage a “nursery school”: Adults look after offspring that are not theirs while the biological parents are out looking for food. And we haven’t mentioned ant and bee workers, which devote themselves to caring for and protecting the offspring of the queen mother.

Why do these things happen? Throughout history, attempts to solve the riddle have been made, and it also troubled Darwin himself. He suggested that altruism that adversely affects an individual is explicable if the giving, the help and even the sacrifice of a particular individual augment the fitness of the group to which it belongs. The advantage of the group outweighs the setback to the individual, he hypothesized, and in the course of evolution groups characterized by mutual support and assistance survived better than those in which it was every individual for himself.

That theory was undermined by the discovery of genes and the emergence of the discipline of population genetics, in the early 20th century. Research showed that if a non-altruistic gene emerged – one that serves the good of the individual and is contrary to the good of the group (such as the gene that encourages the African meerkat to hide, without sounding warning cries, when a predator approaches) – it will become dominant among members of that group and won't allow for altruistic behavior.

A theory that developed following the discovery of genes maintained that what drives evolution is neither the individual nor the group to which it belongs, but the gene. According to that theory, the war of survival in nature is waged between genes and not between animals, and natural selection operates to the benefit of the most suitable genes – not necessarily for the good of the individual that carries them. An individual that cares for and cultivates members of its group or its family, those sharing the same genes, is effectively cultivating its own genes.

Known as “kin selection,” this theory was first formulated mathematically by William Hamilton but gained fame thanks to another evolutionary biologist, Richard Dawkins. Under its inspiration he coined the term “selfish gene” – also the title of his popular 1976 book. According to this conception, the gene seeks to further only its own interests, but in doing so it can also benefit the welfare of others of its group, and thus so-called selfish genes can lead to altruistic individuals.

The problem with this model, however, is that it does not apply in those many cases in nature in which altruism occurs between individuals that are not genetic kin. It certainly doesn’t explain instances in which completely different species help each other.

What can account for this phenomenon? Over time, the models have been improved, and conditions were defined in which even altruism among non-kin cases could be advantageous. For example, when there is a possibility that animals will have future interactions (“today I help you, tomorrow you help me”), or when the individuals remember and identify who did (or did not do) something for them, and punish or reward the other accordingly (“measure for measure”).

There is also the “handicap principle,” developed by the late evolutionary biologist Amotz Zahavi. He proposed a different explanation, according to which what appears to be a sacrifice for the good of the group is actually a display of robust biological fitness by the individual. For example, the deer that leaps in order to attract the predator’s attention is not trying to save the herd, but rather is signaling to the predator that pursuing it would not be worthwhile.

In any event, all the models have turned out to be only partially satisfactory. None has able to explain all cases of altruism in nature. It would be hard to say, then, that the mystery has been solved.

Cracking riddles

This is precisely the bread and butter of Prof. Lilach Hadany, from Tel Aviv University’s Department of Molecular Biology and Ecology of Plants – classic problems in evolution for which no sufficient solution has yet been found. Operating on the seamline between mathematics and the study of evolution, Hadany examines complex biological issues with the aid of mathematical models that simplify them and analyze their components in a systematic way. At present, with the assistance of Dr. Ranit Aharonov and research student Ohad Lewin-Epstein, she is trying to crack the riddle of altruistic behavior by introducing a new and highly original factor into the equation: microbes. Yes, the very bacteria that live within us, literally – in the intestines, on the skin and in the urinary tract. They apparently influence our reactions to food, our immune system, and more. But what’s their connection to ancient evolutionary conundrums?

“We have known about the existence of these bacteria for many years; their number equals or even exceeds the number of cells in our body,” Hadany says. “We also have a great deal of information about their ability to affect the behavior of their host – that is, the animal that carries them in its body. In light of this, the idea occurred to us that they might also play a role in its evolution. We asked ourselves whether the bacteria could have an ‘interest’ in having their host assist and cooperate with another host.”

What sort of interest?

Hadany: “Survival, of course. Microbial bacteria disseminate themselves in two ways. First, when the host of the bacteria produces offspring and transmits its microbes to them. In directional terms, we call this ‘vertical transmission’ – that is, from generation to generation. Second, the bacteria of one host can infect another host: When an animal helps another – feeds it, safeguards it, plucks out its fleas or embraces it – the contact and the rubbing of one against the other allow bacteria to ‘jump’ from host to host and thus to disseminate their genes as part of what is called ‘horizontal transmission’ – between friends. We are suggesting that gastrointestinal bacteria, or gut flora, manipulate their host to cause him to be altruistic and to help others, in order to be able to infect the other and also enjoy the advantage that the other gains.”

Meged Gozny

The phrase “in order to” could be misleading, of course. The evolutionary formulation is: Bacteria that successfully manipulate the host to behave altruistically and help others, infect a large number of hosts and thereby are able to disseminate their genes more effectively than other bacteria that do not engage in such manipulation.

Are you saying that altruism exists in nature because of the activity of the microbiome?

“I want to say that a model that also takes into account the influence of the microbiome [the full set of microorganisms inhabiting a body] can present a more complete picture with respect to the tendency of animals to engage in mutual help. Let’s look at the example closest to us, of parents caring for their offspring. That’s the most easily explained altruism, because of the genetic proximity: Each offspring carries half the genes of each parent, and therefore the genetic interest of the parent is to tend to his or offspring, even to take risks for them, so that the shared genes will be passed on to coming generations.

“But if we introduce the microbiome as well, we see that there is an even greater evolutionary interest in looking after offspring. We say that, in terms of the parent’s genome, looking after the offspring contributes to the survival of 50 percent of the parent’s genes. When it comes to the genome of the bacteria, parental care allows the transmission of a far higher percentage of genes to the offspring, even 100 percent. Hence, a parent that looks after its offspring cultivates its genes but also those of its microbiome. So it’s beneficial for the microbes to cause the parent to continue investing in the offspring.”

If so, we would expect fathers to look after their offspring far more than is actually the case.

“When examining evolutionary strategies – as we are doing with the aid of the mathematical models – we have to take into account a range of interests, which sometimes operate in conflicting directions. On the one hand, it pays for a father to invest in his offspring, because in that way he cultivates half of his genome – but that’s assuming they are indeed his offspring. What if they’re from a different male? Fathers can never be sure. Maybe it’s not worth their while to invest their energy in caregiving, but rather to move from place to place in order to spread their seed and beget as many offspring as possible.

“What’s so wonderful about the mathematical models is the possibility of knowing the conditions in which it’s worthwhile or not worthwhile for an animal to invest in caring for and helping another. When you take the microbiome into account, it can be shown that it’s not in the least important whether the helper and the helped are genetic kin. From the point of view of the bacteria, it’s worth it for their host to help ordinary neighbors, too – and that is something that the regular theory has a hard time explaining.”

What’s the connection between the mathematical model you have developed and biological reality?

“A mathematical model cannot determine what will or will not happen in reality, but it can delineate the boundaries of the sector – that is, it can estimate the probability that a particular event or situation will occur under certain conditions. It can support a biological theory or it can topple it. We are interested in a bacterial gene that promotes altruistic behavior by the host, and we want to know whether it is probable that a trait like this, which appeared one day in the bacteria in the wake of a mutation, can survive despite the price it exacts from the host. In reality, a process of this kind can take millions of years. The mathematical model allows us to calculate now the feasibility of these occurrences.

Daniel Ochoa de Olza,AP

“Based on the mathematical model, we have created a computerized simulation that tracks this dynamic. We created two groups of virtual bacteria, one of which encouraged its host’s altruism, and another that did not. Across the [virtual] generations, it was found that the bacteria that promoted altruism in their hosts were more successful than bacteria that did not, so that altruism became a stable trait in the population. In principle, we can say that an altruistic animal loses something of its own fitness and augments the fitness of its neighbor, who might not be altruistic. Seemingly, then, it loses out by helping another individual to beget more offspring – but its bacteria actually benefit, because by virtue of the interaction they succeed in infecting an animal that becomes more fit and that will therefore produce far more offspring, all of which will inherit the bacteria.”

Cats and mice

Hadany’s model can be dismissed if one subscribes to the late psychologist Abraham Maslow’s observation that, “If all you have is a hammer, everything looks like a nail.” The hammer, in this case, is the microbiome, which of late has been said to be involved in so many processes that there hardly appears to be a topic that can’t be foisted on it. Nevertheless, the originality of Hadany’s thinking is nothing short of astounding. By means of its bold fusion of two completely unrelated spheres – altruism and microbes – she is offering a new perspective on a familiar reality. As an idea it’s brilliant, because it broadens the mechanisms through which evolution operates, without altering its principles.

We are still talking about the “selfish gene,” but this time the gene in question is not only that of the animal but can also be of its microbiome. The concept that animals are only hosts/carriers of genes – that is, that they themselves are marginal in evolutionary terms – remains correct, but the pool of genes has grown. Because of the vast number and diversity of bacteria, their genome has been dubbed the “second genome,” which exists alongside that of the animal itself, the “first genome.” The two of them together – the genomes of both the animal and that of its microbiome – have been called the “holobiome. ”Hadany’s model of altruism, in fact, relates to the holobiome as the totality that drives evolution.

So far, we have talked about the theory according to which microbes encourage altruistic behavior. What about biological feasibility: How can bacteria that reside in the gut influence the behavior of animals – namely, their brain?

“It’s definitely not a baseless idea. Many parasites modify the behavior of the animal that has carried them and manipulate it for their benefit. The best-known example is the rabies virus, which penetrates the body in the wake of a bite, reaches the brain of the affected animal – dog, jackal, etc. – and influences it so that it feels an impulse to bite others. The virus thus steers the host such that it transmits it to an additional host. A certain worm, one that invades crickets, manipulates them to jump into bodies of water. That’s suicide for the cricket, which drowns, but the worm benefits from this behavior because it needs the maritime environment in order to reproduce.

“Another example is the toxoplasma, a parasite that lives inside mice but actually reproduces in cats. When the parasite enters a mouse, it affects its brain, causing the mouse to start being attracted to the smell of cats’ urine – that is, to places where cats are found. In fact, the parasite pushes the mouse straight into the jaws of its predator, behavior that could cost the mouse its life but which serves the parasite.”

What about the microbiome – how does it affect behavior?

“Studies in recent years show that bacteria influence a great many things: The intestinal bacteria of flies can induce them to choose certain mates and not others; bacteria can affect the emotional state of their host – for example, when bacteria were taken from the intestines of depressive people and implanted in rats lacking that bacteria, the rats developed symptoms of depression; the microbiome also affects our biological clock; and there are many other examples.”

How do they do this, physically?

“Through the substances they produce and secrete into the host’s gut. These substances [which can be neural conductors such as serotonin or dopamine, hormones, etc.] reach the host’s brain – for example, through the vagus nerve, via a route that’s called the ‘gut-brain axis’ – and do their work there.”

Are you trying to test this theory – conducting experiments that will support or refute the idea that the microbe affects the willingness to help?

Bloomberg

“Yes, even though we are generally a laboratory that engages in theoretical research and uses mathematical tools. In this case, we actually are doing an experiment, which is now in its initial stages, and our subjects are ants, which as we know display strong cooperation. That behavior is usually explained by the mechanism of kin selection, which operates for the benefit of the ants’ common genes. But when one nest contains a number of mothers and a number of fathers, and the genetic proximity among them is not clear – that explanation is not satisfactory.

“Our hypothesis is that a queen that feeds all the ants transmits its microbiome to them and thus consolidates the interests of all the genomes. To determine whether the microbiome is involved in the ants’ altruistic behavior, we intend to neutralize their intestinal bacteria, such as by feeding them antibiotics. We will then examine whether the ants continue to help each other, even without the microbiome. We evaluate that help by means of a ‘rescue test’: We bind an ant, and we examine how many other ants try to liberate it.”

Excuse me?

“It’s an accepted test in the study of altruism in ants, based on the fact that when an ant gets entangled in something, other ants come to free it, thereby displaying altruistic behavior. The question is whether, after their microbiome is removed, the same behavior will continue to exist or will disappear.”

For some reason, it surprises me to learn that ants have a microbiome.

“All the animals we’re familiar with have a microbiome, and as we said earlier, all beings carry some sort of ‘hitchhikers’ in their body. Even bacteria sometimes have hitchhikers – elements that can pass from bacterium to bacterium and even influence the bacteria to cooperate with each other.”

That makes me think that, actually, for the microbiome to be transferred from host to host, it’s not necessary for the host to carry out altruistic activity vis-a-vis others: It could simply hang out with them, mingle. That sort of interaction does not entail a “price” that the host needs to pay, and is therefore more worthwhile in evolutionary terms. In other words, it’s enough for the intestinal bacteria to cause their host to be sociable – it’s not necessary for them to spur it to help old women across the street or to give away a kidney.

“That is definitely true. Bacteria actually have an interest in impelling their host to be sociable and to interact with others, even without actually helping them: To eat together, sleep together, kiss. We know of cases in which parasites encourage their host to be sociable, and studies have shown that bacteria of a certain type can reduce social anxiety in mice. Very recently an article was published by researchers who succeeded in helping to reverse autism in mice via treatment with the microbiome.”

Has the idea of cooperation, mediated by the microbiome, afforded you new insights?

“Certainly. First, it’s clear to me that the fact that the environment is being bombarded with antibiotics is problematic, and not only because of the widely publicized issue of bacteria that are developing immunity. The harm done by antibiotics to the microbiome could have consequences for the behavior of animals and human beings. In the United States, every farm where animals are raised is flooded with antibiotics that damage the microbiome, and agricultural farms are drenched in glyphosate, a weed killer, which also damages the microbiome when it passes from plants to animals via the food chain. In the context we were talking about, this could have the effect of disrupting cooperation within various populations, particularly of social animals.

“At another level, I have all kinds of amusing thoughts about how, one day, it might be possible to produce little candies from social types of microbiomes in order to encourage cooperative behavior. But those are just wild thoughts for now, of course, totally unscientific.”

And at the personal level, does the knowledge that we’re living with a hidden partner affect you?

Hadany smiles. “Very much. For example, when I feel like having something sweet, I find myself thinking, is it me or my microbiome [talking]? Or when I want a hug – maybe it’s the microbiome that wants it?”

So now it’s not only our genes that are responsible for us to a large degree, but also the genes of our bacteria…

“Yes. There’s a kind of feeling, at times, that hardly any free will remains to us. That’s at the philosophical level. More prosaically, I notice that at family meals I am not really making sure that everyone uses only his spoon when sharing food. On the contrary: If everyone’s healthy, it’s an opportunity for microbiome sharing.”

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