The human microbiome in evolution

Abstract

The trillions of microbes living in the gut-the gut microbiota-play an important role in human biology and disease. While much has been done to explore its diversity, a full understanding of our microbiomes demands an evolutionary perspective. In this review, we compare microbiomes from human populations, placing them in the context of microbes from humanity's near and distant animal relatives. We discuss potential mechanisms to generate host-specific microbiome configurations and the consequences of disrupting those configurations. Finally, we propose that this broader phylogenetic perspective is useful for understanding the mechanisms underlying human-microbiome interactions.

Keywords: Codiversification; Evolution; Habitat filtering; Microbiome; Transmission.

Fig. 1.

The human gut microbiome within the context of populations and deeper evolutionary landscapes. a The microbiomes of different human populations are distinct from each other, especially between industrialized populations such as in the USA and remote, non-industrialized populations such as Malawians or the Guahibo and Yanomami people of the Amazon [14, 17]. b Within the context of the greater primates lineage, these differences between human populations become smaller and a connection between humans and captive populations of non-human primates can be seen. c Zooming out to include other vertebrate lineages further diminishes those differences, as the effects of deep evolutionary splits between host species and lifestyle characteristics on the gut microbiome become evident. Methods: All data were drawn from publically available studies in Qiita (https://qiita.ucsd.edu/; studies 850, 894, 940, 963, 1056, 1696, 1734, 1736, 1747, 1773, 2182, 2259, 2300, 10052, 10171, 10315, 10376, 10407, 10522). Sequence data for all samples were generated using the same protocol [134] and sequenced on an Illumina MiSeq or HiSeq platform. Sequence data were trimmed to 100 nucleotides and OTUs were picked using the deblur method [135]. Up to five samples per species were randomly selected, rarefied to 10,000 sequences per sample, and unweighted UniFrac [136] distances between samples were computed using Qiime 1.9.1 [137]. The non-metric multidimensional scaling ordination technique was employed in R 3.3.3 [138] to visualize these distances. Silhouettes of the running woman, primate, bird, and bat in c are designed by Vexels.com and reproduced with permission

Fig. 2.

Host–microbiome interactions can affect both health and fitness. Dysbiosis is associated with a number of negative health outcomes, including obesity, asthma, and certain cancers. Negative health outcomes are not sufficient evidence for coevolution of the microbiome and host, however. Not all of these diseases result in negative fitness consequences by limiting reproductive success. Microbiomes potentially impact host fitness at multiple stages of life by affecting survival through reproductive years or reducing fertility. In infancy, microbes extract energy from non-digestible components of milk, increasing nutrient acquisition at this vulnerable age. During childhood, a stable microbiome prevents invasion of deadly pathogens. In adulthood, the microbiome potentially influences fertility, either by altering nutrition or causing disease. Finally, the microbiome may be important for lifespan. Although lifespan after menopause will not result in more children, the grandmother hypothesis predicts that care of extended kin results indirectly in higher fitness [139]. IBD inflammatory bowel disease

Fig. 3.

A non-adaptationist model for consequences of codiversification in microbiomes. In Step 1, a host lineage evolves permissive but variable filters for a gut microbiome, allowing diverse microbes to colonize its gut. In Step 2, a subset of microbes (dark outline) specialize in the host lineage, losing genes necessary to colonize diverse environments in favor of specialization on the particular host niche. As host genes creating this specific niche drift, the specialized microbes follow. In Step 3, the codiversifying microbes are now reliable environmental stimuli, and serve as developmental cues, reducing constraint on the host genome for essential processes. Mutations in the host genome arise that are neutral in the presence of these microbes, but deleterious in their absence. For example, an essential host-encoded developmental molecule X is required to signal Y. Microbial product Z elicits a similar downstream effect as X. At some point, a mutation in the host genome results in the loss of function of X, which is neutral when microbially encoded Z is present. In Step 4, in the absence of the codiversifying microbe, neither X nor Z is present to signal to Y, resulting in reduced fitness of the host