Metagenomics: Social behavior and the microbiome

  1. Jack A Gilbert  Is a corresponding author
  1. Argonne National Laboratory, United States

Why did social interactions evolve? Complex rules govern how we interact when we meet, and while these principles are often bewildering, they are also somehow intrinsic to the fabric of any human society. Now, in eLife, Elizabeth Archie, Jenny Tung and co-workers have provided compelling evidence to support the theory that physical interaction evolved in vertebrates to help share potentially health-promoting bacteria (Tung et al., 2015).

Tung et al. sequenced the genomes of the various microbes found in the faeces of 48 baboons from two different social groups in Amboseli in Kenya. They found that these ‘microbiomes’ differed between the two social groups, despite them living in overlapping areas and eating similar foods. It has been shown that diet influences the composition and structure of the microbial communities living in the human gut (David et al., 2013). So why were the microbiomes of these groups of baboons not more similar?

The answer lies in the fact that baboons interact by grooming each other (Figure 1). Baboons that groomed each other more frequently had more similar microbiomes, which suggests that physical interactions with others are very important in shaping the microbial communities in these individuals. Baboons don't tend to groom baboons from different social groups (much like humans), so social activities within a group act to consolidate shared communities of microbes.

Baboons that groom each other more often have more similar gut microbiomes.

Image credit: Elizabeth A. Miller.

The need for physical interaction or the presence of others is central to human cognitive psychology. Embodied cognition is the study of how the presence of others affects thoughts, feelings, and behaviors (Meier et al., 2012); for example, we tend to distance ourselves physically from those we don't like or trust, whereas we tend to be more physically close and have more physical interactions with our friends and family.

It is highly probable that evolution has shaped social behavior. Physical interactions with those we love feels good; hugs, kisses, and even basic skin-to-skin contact have positive influences on our thoughts and feelings. The hand-shake—which is the standard mode of introduction in many societies—represents this concept. But why did these interactions evolve? Are they purely social constructs, or is physical interaction instinctive, driven by some selective advantage? Sharing microbes in this way can be beneficial: for example, bumblebees living in the same hive share bacteria through fecal pellets (Koch and Schmid-Hempel, 2011). This protects the bees from the virulent parasite Crithidia bombi, and therefore gives these bees a selective advantage over other bees that don't share bacteria.

Acquiring a beneficial microbiome may actually have shaped the evolution of the immune system, whose primary role is to maintain the balance of ‘good’ and ‘bad’ microbes in the microbiome. The immune system aims to control the exposure of host tissues to the microbiome, which it does in part by directly interacting with the bacteria. For example, the protein immunoglobulin A is released into the gut, where it binds to certain species of bacteria: this reduces the ability of the bacteria to move and keeps them away from the cells of the intestine (Hooper et al., 2012). It is likely that this mechanism is also used to capture certain beneficial microbes and retain them in the gut.

Sharing of microbes through physical interaction has been shown to happen in several vertebrate species. For example, my own work in humans demonstrates that family relationships and co-housing can influence the similarity of the microbiomes of individuals (Lax et al., 2014). In fact, in one of the groups examined, a young couple was shown to have much more similar microbiomes on their skin and in their nose than a lodger living with them in their home: however, the lodger had more microbes in common with the couple than he did with anyone else in the study.

Unlike the baboons—who only share significant amounts of microbes due to physical grooming activity—humans can also share microbes through the artificial environment we have constructed for ourselves. Over the last 100 years or so, these indoor environments have become increasingly isolated from the natural world outside. The microbiome of individuals living in the same indoor space can be shared through the air and via surfaces because humans are the main source of the microbes, and therefore most of the microbes in the space are readily able to colonize the human occupants.

This sharing of microbes might seem like a good idea; it worked for the bees. However, there is now mounting evidence to suggest that the over-sharing of the microbiome may be reducing our exposure to richer microbiomes from other sources, thereby limiting the development of our immune system (Lax et al., 2015). Wild baboons are exposed to many different sources of microbes in their environment, and—while their physical interactions may indeed help to share beneficial bacteria—these other microbes are also likely to support their physical, immunological and neurological development.

One of my colleagues, the eminent microbiologist and microbial ecologist Norman Pace, says that his exploration of the microbial world has made him reluctant to share other people's microbiomes (Personal Communication). In fact, Norman now only ‘fist bumps’ when he meets other people, and never shakes their hands. Is this reduced microbial exposure potentially detrimental to his health? Or could it be that in our modern world, Norman has the right idea?

References

Article and author information

Author details

  1. Jack A Gilbert

    Department of Biosciences and Institute for Genomic and Systems Biology, Argonne National Laboratory, Chicago, United States
    For correspondence
    gilbertjack@anl.gov
    Competing interests
    The author declare that no competing interests exist.

Publication history

  1. Version of Record published:

Copyright

© 2015, Gilbert

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,929
    views
  • 387
    downloads
  • 18
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Jack A Gilbert
(2015)
Metagenomics: Social behavior and the microbiome
eLife 4:e07322.
https://doi.org/10.7554/eLife.07322
  1. Further reading

Further reading

    1. Ecology
    Chao Wen, Yuyi Lu ... Lars Chittka
    Research Article

    Bumblebees (Bombus terrestris) have been shown to engage in string-pulling behavior to access rewards. The objective of this study was to elucidate whether bumblebees display means-end comprehension in a string-pulling task. We presented bumblebees with two options: one where a string was connected to an artificial flower containing a reward and the other presenting an interrupted string. Bumblebees displayed a consistent preference for pulling connected strings over interrupted ones after training with a stepwise pulling technique. When exposed to novel string colors, bees continued to exhibit a bias towards pulling the connected string. This suggests that bumblebees engage in featural generalization of the visual display of the string connected to the flower in this task. If the view of the string connected to the flower was restricted during the training phase, the proportion of bumblebees choosing the connected strings significantly decreased. Similarly, when the bumblebees were confronted with coiled connected strings during the testing phase, they failed to identify and reject the interrupted strings. This finding underscores the significance of visual consistency in enabling the bumblebees to perform the task successfully. Our results suggest that bumblebees’ ability to distinguish between continuous strings and interrupted strings relies on a combination of image matching and associative learning, rather than means-end understanding. These insights contribute to a deeper understanding of the cognitive processes employed by bumblebees when tackling complex spatial tasks.

    1. Ecology
    Mathilde Delacoux, Fumihiro Kano
    Research Article

    During collective vigilance, it is commonly assumed that individual animals compromise their feeding time to be vigilant against predators, benefiting the entire group. One notable issue with this assumption concerns the unclear nature of predator ‘detection’, particularly in terms of vision. It remains uncertain how a vigilant individual utilizes its high-acuity vision (such as the fovea) to detect a predator cue and subsequently guide individual and collective escape responses. Using fine-scale motion-capture technologies, we tracked the head and body orientations of pigeons (hence reconstructed their visual fields and foveal projections) foraging in a flock during simulated predator attacks. Pigeons used their fovea to inspect predator cues. Earlier foveation on a predator cue was linked to preceding behaviors related to vigilance and feeding, such as head-up or down positions, head-scanning, and food-pecking. Moreover, earlier foveation predicted earlier evasion flights at both the individual and collective levels. However, we also found that relatively long delay between their foveation and escape responses in individuals obscured the relationship between these two responses. While our results largely support the existing assumptions about vigilance, they also underscore the importance of considering vision and addressing the disparity between detection and escape responses in future research.