Socially structured gut microbiomes in wild baboons

Male yellow baboon grooming a female baboon (photo by Noah Snyder-Mackler)

Male yellow baboon grooming a female baboon (photo by Noah Snyder-Mackler)

“You can pick your friends and you can pick your nose, but you can’t pick your friend’s nose.”

Well, that old adage may still be true, but baboons certainly pick (up) their friends’ gut microbes. A new study by Jenny Tung and colleagues tested how baboon social structure, which includes both group membership and social relationships, predicted variation in gut microbiota.

Across the animal kingdom, individuals who spend more time together tend to have more similar microbiomes. Shoot, humans even share their microbiomes with their dogs (I wonder how that happens). Indeed, from bees to apes to humans, there is mounting evidence for social structuring of the gut microbiome. Most of these differences have been attributed to shared diet.

“However, social relationships could also shape gut microbiomes more directly, via transmission from shared environments or during physical contact.”

In other words, you don’t need to share food to share gut microbiota: You could share microbiota if you hug, kiss, or even high-five. Since you only hand out high-fives (and, I guess, hugs and kisses too) to your closest friends, then we would expect to see that close friends have more similar gut microbiomes than individuals who aren’t friends.

Tung et al set out to test this hypothesis using the well-studied baboons of the Amboseli Baboon Research Project. To do so, they combined detailed data on group membership, diet, and grooming patterns (kind of like baboon high-fives: they only do this with their best friends) with metagenomic shotgun sequencing of fecal samples collected from 48 adult baboons living in two different social groups.

Not-so-surprisingly, they found that baboons from the same social group had more similar gut microbes than baboons from different groups (group membership explained a whopping 18.6% of the variation in species composition). This could, however, be due to the fact that baboons from the same social group tend to be more closely related and eat the same foods… But relatedness and diet didn’t explain all of the variation in the baboon guts. First, the authors showed that social group membership was a significant predictor of the gut micorbiome even after controlling for genetic relatedness. Second, they used the detailed foraging data to show that the diets of the two groups were strikingly similar during the month that the samples were collected.

"Oh, hey girl, wanna swap gut microbes?" - male yellow baboon consorting with a female (photo by Noah Snyder-Mackler)

“Oh, hey girl, wanna swap gut microbes?” – Ryan Gosling male yellow baboon consorting with a female (photo by Noah Snyder-Mackler)

Friends let friends share microbes
Tung et al then took a figurative microscope to their subjects and honed in on the social relationships among baboons within each group – as measured by grooming patterns. Excitingly, they found that closer friends (i.e., those with stronger grooming relationships) had more similar gut microbiota – even when they controlled for diet composition and relatedness (because closely related baboons form stronger grooming relationships).

Baboons with stronger grooming relationships had more similar, or less dissimilar, gut microbiomes. (Fig. 2c from Tung et al, 2015)

Baboons with stronger grooming relationships had more similar, or less dissimilar, gut microbiomes. (Fig. 2c from Tung et al, 2015)

So what kind of bacterial do friends share?

“We reasoned that, if socially structured species depend on direct transmission between baboons…they should be less likely than other species to persist outside of a host”

Indeed, they found that socially structured species were the ones that would have more trouble surviving outside of a gut – specifically species that are anaerobic and unable to produce spores.

Overall, these findings are some of the first to show that social interactions can directly affect the gut microbiota. One of the many lingering questions is how these bacteria are transmitted. Baboons aren’t coprophagic (google it), so we don’t know exactly how the gut microbes are traveling from one individual to the next. The authors suggest two possible mechanisms:
1. “the duration and intimacy of grooming bouts, which include frequent hand-to-mouth contact, may be important in exposing baboons to the gut bacteria of their grooming partners”.
2. The fact that, during some grooming bouts, especially those involving a male and a female, individuals concentrate a lot of grooming to the female’s nether (i.e., ano-genital) regions.

“Our results argue that social interactions are an important determinant of gut microbiome composition in natural animal populations-a relationship with important ramifications for understanding how social relationships influence health, as well as the evolution of group living.”

REFERENCE

Tung J, Barreiro LB, Burns MB, Grenier J-C, Lynch J, Grieneisen LE, Altmann J, Alberts SC, Blekhman R & Archie EA (2015) Social networks predict gut microbiome composition in wild baboons. Elife 4, e05224. doi: 10.7554/eLife.05224

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About Noah Snyder-Mackler

I'm a postdoctoral fellow in the department of Evolutionary Anthropology at Duke University. Broadly, I study non-human primate genetics and genomics. More specifically, I'm interested in the interaction between behavior, genotype, and gene expression in response to social stress.
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  • Emilie

    Good evening, extremely interesting post. But then It got me wondering about form and function, baboons or humans as superorganisms hosting trillions of microbes are we more prone to social contact due to microbial exchange (the microbes push us to have social contact to proliferate) or is the microbe exchange a result of an innate biological need for social contact? I get a feeling that each influence another, I was wondering what where your thoughts on that?

    • Noah Snyder-Mackler

      Thanks for the comment Emilie. It’s a really interesting question. Baboons, like many primates, are extremely social and we know that the quality and quantity of their social relationships can have a strong impact on their health and survival. I would therefore posit that the microbial exchange is a result of the importance of social interactions in these animals and not the result of the microbes altering their behavio. There are some (extreme) examples of microbes altering the host’s behavior, but these effects have only been shown in extreme circumstances and are typically the result of infections getting into the brain (here is an overly simplistic video of what toxoplasma gondii does rats: https://www.youtube.com/watch?v=zCbxdLnYclU).

      Although this is also a literature I’m not terribly familiar with, so perhaps someone else could share their opinion/expertise?