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© LEONID ANDRONOV/SHUTTERSTOCKThe structure of a pheromone
We, people, typically think of ourselves as people. It can be jarring to remember that we're also mammals who, like most other mammalian species, unconsciously send odor signals to each other carrying information about our gender, our health, our reproductive state, our mood, and even our potential to be a compatible mate. If the idea that your secretions say something about you creeps you out, then you won't welcome the news that the revealing scent signals we emit may actually be the end-products of microbial fermentations carried out in our bodies' damp, low-oxygen creases. A recent study of scent signals in hyenas presents the best evidence to date that bacteria are responsible for producing pheromones in a mammalian species. The implication of these results is that the bacteria in our underarms may have a surprisingly complex role in our social lives.

That microbes are actually the makers of mammalian pheromones is an idea that dates back to the 1970s when several scientists proposed the "fermentation hypothesis." Their idea was that, because scent glands are typically found in warm, damp, low-oxygen areas of the body, microbes that thrive in those areas ferment the body's nutrient-rich secretions into the odorous chemical signals used by most mammals to communicate.

What we communicate likely depends, at least in part, on the microbes we're harboring.

The fermentation hypothesis has been difficult to test in any definitive way, until recently. Technological breakthroughs in DNA analysis opened access to new realms of the microbial world that were previously nearly invisible, including the trillions of symbiotic bacteria that live on and in us. In recent years, studies of these symbiotic microbes have revealed that they modulate the effects of our diet, prime our immune systems, and generally play an influential role in our health. Some scientists are pushing this microbial paradigm even further: symbiotic bacteria may also play a role in animal behavior, as a key component of mammals' chemical communication system. For the first time, scientists have the tools to truly test the fermentation hypothesis.

A group at Michigan State led by Kevin Theis, Kay Holekamp, and Thomas Schmidt, set out to test the fermentation hypothesis in two species of hyenas, mammals that actively use scent markings to communicate territorial boundaries and other important social information. The chemical composition of a hyena's scent can vary, depending on an individual's group membership, gender, and reproductive state. The researchers' aim was to discover whether the kinds of bacteria in the hyenas' scent glands changed with the varying chemical composition of the scent. This was important because a major criticism of the fermentation hypothesis was that symbiotic bacteria were unlikely to be diverse enough to produce the many different chemicals in mammalian scents.

Theis and his colleagues collected scent secretions, called "pastes," from the glands of anesthetized hyenas and then analyzed the chemical and bacterial composition of the paste. They found, as expected, that the odor molecules in the paste varied among different species, different hyena social groups, and hyenas that were pregnant or lactating. They could even identify differences in the chemical signatures of male hyenas that had immigrated from one social group to another.

Crucially, the researchers found that differences in the species of bacteria in the pastes tracked very closely with the differences in the paste chemicals. They could tell the difference between a pregnant and a lactating hyena just by the bacteria in the hyenas' scent glands.

These results offer the strongest support yet for the fermentation hypothesis, but there is a crucial piece of evidence still missing. The researchers did not show that symbiotic bacteria actually produced the different chemicals in the hyenas' pastes. But we do have evidence that bacteria produce odor molecules in another species: humans. Scientists have established that many of the chemicals in underarm odor are the fermentation products of bacteria. While much of this research has been focused on the sources of bad odor, it's becoming increasingly likely that our underarm sweat communicates more than just our personal grooming habits. What we communicate likely depends, at least in part, on the microbes we're harboring.

The degree to which human behavior is influenced by unconscious scent signals is still largely unknown, but the important role of symbiotic bacteria in our physiology is now beyond doubt. All life exists in an environment shaped by the remarkably diverse chemistry carried out by millions of different kinds of microbes. The next step is to understand how much of who we are actually depends on our intimate relationship with these microbes.