• The stomach
• The intestines
• The skin
• The extended microbiome

What is already known on this topic
The social structure of primates has been known to shape the composition of body microbiomes. However, how microbiomes impact a variety of processes, including social behavior of hominis, is less clear.

What this research adds
This study uses a comparative approach to understand how microbiomes in hominis assembled, in the ecological and social contexts in which they evolved since the last common ancestor (LCA) of chimpanzees and humans, six million years ago.

This study considers the possibility that social behavior among hominins, might have been influenced by prosocial microbes whose fitness was advantaged by social interactions between individuals.

Dr. Robert R. Dunn and his team at North Carolina State University, have underlined the complex evolutionary interplay between microbiomes development and human social structures. Considering four components of hominin bodies, the study highlights the possible effects of the microbiome on human social behavior and lifestyle.

Primates microbiomes represent complex communities. These influence a broad array of processes including a host’s ability to access nutrients, health, immune system priming, and even behavior and scent. The importance of microbiome communities (e.g., skin, intestinal, vaginal, oral) has led to the suggestion that the host plus its associated microbiomes, could represent one whole biological organization on which social structure and behavior developed during evolution.

Here, the researchers have reviewed four aspect of hominin bodies and behaviors that have changed, starting from when we last shared a common ancestor with chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), our last common ancestor (LCA), six million years ago. Considering the stomach, the intestines, the skin and the extended microbiome, the team have reviewed social behavior that have might influenced microbiome and vice versa.

The researchers have been reconstructing the microbiomes of ancient hominins relying on two sources of data:

  • ancient microbial DNA from humans and non-human primates
  • comparisons of modern genes, phenotypes and microbiota among humans, great apes, and other non-human primates, mammals and birds.

The stomach

The stomach is responsible in mammals for the degradation of protein and plays a role as ecological filter, allowing some species into the intestines but not others. In primates that eats mostly fruits and leaves, the amount food borne microbes accessing the intestine is limited.

However, in omnivorous primates which diets include raw meats, the risk to ingest food borne pathogens is greater, therefore the stomach is expected to be more acidic. Humans have very acidic stomachs, with a mean pH of 1.5, unlike those of any other primate. For example, chimpanzee is reported to have had a stomach pH almost neutral. This conclusion has been drawn since captive chimpanzees, hold yeast in their stomachs and not many yeast species are able to grow in hyper-acidic environments

Here, the researchers propose that the extreme acidity of human stomachs evolved after our split with the LCA with chimpanzees, especially since humans started eating meat and bones probably scavenged after being killed by another mammal, like hyena.

Therefore, acidic stomachs may have avoided food borne pathogens access in hominins, that have eaten meat before the advent of fire. Also, the low stomach pH might have been advantageous later on, when our ancestors began to hunt larger prey.

In conclusion, it is possible that the acidity of the hominin stomach may have played a role in human foraging behavior and diet, and as a consequence in the gastrointestinal selection and development of microbiomes.

The intestines

Within humans the length of the large intestine varies among individuals, even with similar genetic backgrounds. During evolution the large intestine of humans became shorter, relative to the small intestine compared to apes, while total intestine length also declined relative to body size.

The study questioned on why the shortening occurred and what consequences might have occurred for the physiology of the intestinal tract and gut microbiome composition.

The use of fire on foods including plants, fishing techniques and cooking tools, have helped to pre-digest and pre-process some foods making it easier to digest. Therefore, hominis had to rely less on microbes in their guts to break down components of their diets, such as cellulose. This could be one of the reasons for the development of smaller guts. Also, that would include the investment of energy in other body systems like the brain, smaller biomass of microbes together with a reduced retention time of foods in the gut.

However, taxonomic classes of bacteria found in the guts of both chimpanzees and humans overlap, as the same families and genera of bacteria occur in similar proportions. The team hypothesized that this overlap occurred before the human-chimpanzee split and therefore, to be characteristic of our LCA. Moreover, even if the gut microbiomes of humans are similar to those of modern chimpanzees, it appears to be even more similar to those of cercopithecine monkeys, such as baboons.

The researchers pointed out interesting data, in which has been reported that differences in gut microbiome composition are greater between humans and apes than between humans and cercopithecines. More importantly, similarities correlates strongly with geography and lifestyle. In conclusion, this suggests that the human gut microbiome has the potential to play a role in local adaptation.

The team suggest that shared microbial taxa might have increased resistance to endemic infectious diseases, might have facilitated digestion of certain foods (high in tannins, seaweeds) within social groups, and might have led to local microbial adaptations to environments. Moreover, once Homo moved bipedally and started to explore new geographic areas in the African landscape, have started to find more food choices together with new food borne microbes, and parallelly confronted more diseases.

In conclusion, the researchers support the hypothesis that human evolution has been in part facilitated by microbes that helped human adaptation success, in the environment around the world.

The skin

In mammalians apocrine glands are located primarily in armpits and are associated with evaporative cooling. In humans and apes these glands are named axillary organs, and appear to play also a role in body odors. In lemurs and in western lowland gorillas, aromas from apocrine glands can signal individual identity. Moreover, apocrine glands produce secretions and the aromas produced by the bacteria in these glands might also signal fear, stress and arousal. Human armpit odors and microbes are also very variable among humans. Interestingly, the team report that this variation on the apocrine glands, is influenced by a single nucleotide substitution variant in the ABCC11 gene.

Here, the study highlights the importance of microbes in local adaptation and lifestyle, which is supported also by the study of the composition of skin bacteria. In particular, on human skin, Staphylococcus bacteria are present and dominant and not shared with other primates. What is interesting, is that Staphylococcus is the most common genus of bacteria on the skin of some wild sheep (Ammotragus lervia), goats, cows (all of which are domesticated animals or relatives of domesticated animals) and humans. Therefore, skin Staphylococcus have spread among humans and domesticated animals during cohabitation, increasing the similarity of the aroma of domestic animals to humans and vice versa.

Here, the researchers underlie how bacterial sharing within co-habiting individuals can influence hosts’ social structure and the development of dominant skin microbial taxa.

The extended microbiome

Here, the researchers describe the role of food processing in human evolution and sociality with particular attention to fermentation, that allows the enrichment of certain components in foods and begin food processing. Many carnivore species fermented foods. For example, in hot regions, Hyenas store food items in water, in cold regions, foxes and other carnivores store and ferment foods by burying them. Is unknown when humans first controlled fermentation, however at that stage microbes began to play a central role.

Evidence that support the use of fermentation since the common ancestors exist, and relates to two genetically encoded human traits, those associated with sour taste receptors and those associated with the enzyme alcohol dehydrogenase. In nearly all primates, even slightly acidic foods are perceived as sour and not enjoyable. Instead, adult humans, night monkeys and male chimpanzees perceived acidic foods as pleasant and have learned to enjoy them. From here, assuming that both monkeys and humans like sour foods, the research team hypothesized that the preference could have been occurred in our common ancestor. A second evolutionary change that influenced the ways in which our ancestors fermented foods is the evolution of alcohol dehydrogenase. The team suggest that this gene evolved ten million years ago, probably when apes began to be more sedentary and to spend more time on the ground, consuming fermented fallen fruits that were higher in ethanol than ripe fruits picked directly from trees.

Given this, when humans started to use technologies to control fermentation also started favoring and selecting specific microbes, with characteristics that were desirable for making their foods and beverages.

In conclusion this study poses questions and give hints on how potential prosocial microbes associated with hominin, have directly favored certain kinds of social behavior and interaction with other species, wherewith shared microbes. Moreover, this comprehensive analysis suggests that our dynamic interactions with microbes, have had the potential to influence physical, social, and behavioral changes that occurred during human evolution.