Transmission of the gut community: Natural transmission of the mammalian microbiota is poorly understood. Some genera of bacteria are transmitted from mothers to offspring, whereas others are acquired from the wider environment. Moeller et al. derived inbred mouse lines from two wild populations of mice with distinct microbiota and monitored the populations' microbiomes for 3 years while they were kept in the same animal facility. The microbiota of the two mouse lineages remained distinct even after 10 generations. Most microbiota genera transmitted vertically. Those taxa that transmitted horizontally through the shared environment of the animal facility tended to be those that include pathogens. Science , this issue p. 453

The gut microbiomes of human populations worldwide have many core microbial species in common. However, within a species, some strains can show remarkable population specificity. The question is whether such specificity arises from a shared evolutionary history (codiversification) between humans and their microbes. To test for codiversification of host and microbiota, we analyzed paired gut metagenomes and human genomes for 1225 individuals in Europe, Asia, and Africa, including mothers and their children. Between and within countries, a parallel evolutionary history was evident for humans and their gut microbes. Moreover, species displaying the strongest codiversification independently evolved traits characteristic of host dependency, including reduced genomes and oxygen and temperature sensitivity. These findings all point to the importance of understanding the potential role of population-specific microbial strains in microbiome-mediated disease phenotypes.

Although we know there is considerable variation in gut microbial composition within host species, little is known about how this variation is shaped and why such variation exists. In humans, obesity is associated with the relative abundance of two dominant bacterial phyla: an increase in the proportion of Firmicutes and a decrease in the proportion of Bacteroidetes. As there is evidence that humans have adapted to colder climates by increasing their body mass (e.g. Bergmann's rule), we tested whether Firmicutes increase and Bacteroidetes decrease with latitude, using 1020 healthy individuals drawn from 23 populations and six published studies. We found a positive correlation between Firmicutes and latitude and a negative correlation between Bacteroidetes and latitude. The overall pattern appears robust to sex, age and bacterial detection methods. Comparisons between African Americans and native Africans and between European Americans and native Europeans suggest no evidence of host genotype explaining the observed patterns. The variation of gut microbial composition described here is consistent with the pattern expected by Bergmann's rule. This surprising link between large-scale geography and human gut microbial composition merits further investigation.

Recent studies in model organisms have shown that compositional variation in the microbiome can affect a variety of host phenotypes including those related to digestion, development, immunity, and behavior. Natural variation in the microbiome within and between natural populations and species may also affect host phenotypes and thus fitness in the wild. Here, I review recent evidence that compositional variation in the microbiome may affect host phenotypes and fitness in wild mammals. Studies over the last decade indicate that natural variation in the mammalian microbiome may be important in the assistance of energy uptake from different diet types, detoxification of plant secondary compounds, protection from pathogens, chemical communication, and behavior. I discuss the importance of combining both field observations and manipulative experiments in a single system to fully characterize the functions and fitness effects of the microbiome. Finally, I discuss the evolutionary consequences of mammal–microbiome associations by proposing a framework to test how natural selection on hosts is mediated by the microbiome.

There is a growing appreciation of the role of gut microbial communities in host biology. However, the nature of variation in microbial communities among different segments of the gastrointestinal (GI) tract is not well understood. Here, we describe microbial communities from ten different segments of the GI tract (mouth, esophagus, stomach, duodenum, ileum, proximal cecum, distal cecum, colon, rectum, and feces) in wild house mice using 16S rRNA gene amplicon sequencing. We also measured carbon and nitrogen stable isotopic ratios from hair samples of individual mice as a proxy for diet. We identified factors that may explain differences in microbial composition among gut segments, and we tested for differences among individual mice in the composition of the microbiota. Consistent with previous studies, the lower GI tract was characterized by a greater relative abundance of anaerobic bacteria and greater microbial diversity relative to the upper GI tract. The upper and lower GI tracts also differed in the relative abundances of predicted microbial gene functions, including those involved in metabolic pathways. However, when the upper and lower GI tracts were considered separately, gut microbial composition was associated with individual mice. Finally, microbial communities derived from fecal samples were similar to those derived from the lower GI tract of their respective hosts, supporting the utility of fecal sampling for studying the gut microbiota of mice. These results show that while there is substantial heterogeneity among segments of the GI tract, individual hosts play a significant role in structuring microbial communities within particular segments of the GI tract.