Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints.
ABSTRACT: The gut microbiome of primates, including humans, is reported to closely follow host evolutionary history, with gut microbiome composition being specific to the genetic background of its primate host. However, the comparative models used to date have mainly included a limited set of closely related primates. To further understand the forces that shape the primate gut microbiome, with reference to human populations, we expanded the comparative analysis of variation among gut microbiome compositions and their primate hosts, including 9 different primate species and 4 human groups characterized by a diverse set of subsistence patterns (n?=?448 samples). The results show that the taxonomic composition of the human gut microbiome, at the genus level, exhibits increased compositional plasticity. Specifically, we show unexpected similarities between African Old World monkeys that rely on eclectic foraging and human populations engaging in nonindustrial subsistence patterns; these similarities transcend host phylogenetic constraints. Thus, instead of following evolutionary trends that would make their microbiomes more similar to that of conspecifics or more phylogenetically similar apes, gut microbiome composition in humans from nonindustrial populations resembles that of generalist cercopithecine monkeys. We also document that wild cercopithecine monkeys with eclectic diets and humans following nonindustrial subsistence patterns harbor high gut microbiome diversity that is not only higher than that seen in humans engaging in industrialized lifestyles but also higher compared to wild primates that typically consume fiber-rich diets.IMPORTANCE The results of this study indicate a discordance between gut microbiome composition and evolutionary history in primates, calling into question previous notions about host genetic control of the primate gut microbiome. Microbiome similarities between humans consuming nonindustrialized diets and monkeys characterized by subsisting on eclectic, omnivorous diets also raise questions about the ecological and nutritional drivers shaping the human gut microbiome. Moreover, a more detailed understanding of the factors associated with gut microbiome plasticity in primates offers a framework to understand why humans following industrialized lifestyles have deviated from states thought to reflect human evolutionary history. The results also provide perspectives for developing therapeutic dietary manipulations that can reset configurations of the gut microbiome to potentially improve human health.
Project description:Bacterial communities colonizing the reproductive tracts of primates (including humans) impact the health, survival and fitness of the host, and thereby the evolution of the host species. Despite their importance, we currently have a poor understanding of primate microbiomes. The composition and structure of microbial communities vary considerably depending on the host and environmental factors. We conducted comparative analyses of the primate vaginal microbiome using pyrosequencing of the 16S rRNA genes of a phylogenetically broad range of primates to test for factors affecting the diversity of primate vaginal ecosystems. The nine primate species included: humans (Homo sapiens), yellow baboons (Papio cynocephalus), olive baboons (Papio anubis), lemurs (Propithecus diadema), howler monkeys (Alouatta pigra), red colobus (Piliocolobus rufomitratus), vervets (Chlorocebus aethiops), mangabeys (Cercocebus atys) and chimpanzees (Pan troglodytes). Our results indicated that all primates exhibited host-specific vaginal microbiota and that humans were distinct from other primates in both microbiome composition and diversity. In contrast to the gut microbiome, the vaginal microbiome showed limited congruence with host phylogeny, and neither captivity nor diet elicited substantial effects on the vaginal microbiomes of primates. Permutational multivariate analysis of variance and Wilcoxon tests revealed correlations among vaginal microbiota and host species-specific socioecological factors, particularly related to sexuality, including: female promiscuity, baculum length, gestation time, mating group size and neonatal birth weight. The proportion of unclassified taxa observed in nonhuman primate samples increased with phylogenetic distance from humans, indicative of the existence of previously unrecognized microbial taxa. These findings contribute to our understanding of host-microbe variation and coevolution, microbial biogeography, and disease risk, and have important implications for the use of animal models in studies of human sexual and reproductive diseases.
Project description:BACKGROUND: Host-associated microbes comprise an integral part of animal digestive systems and these interactions have a long evolutionary history. It has been hypothesized that the gastrointestinal microbiome of humans and other non-human primates may have played significant roles in host evolution by facilitating a range of dietary adaptations. We have undertaken a comparative sequencing survey of the gastrointestinal microbiomes of several non-human primate species, with the goal of better understanding how these microbiomes relate to the evolution of non-human primate diversity. Here we present a comparative analysis of gastrointestinal microbial communities from three different species of Old World wild monkeys. METHODOLOGY/PRINCIPAL FINDINGS: We analyzed fecal samples from three different wild non-human primate species (black-and-white colobus [Colubus guereza], red colobus [Piliocolobus tephrosceles], and red-tailed guenon [Cercopithecus ascanius]). Three samples from each species were subjected to small subunit rRNA tag pyrosequencing. Firmicutes comprised the vast majority of the phyla in each sample. Other phyla represented were Bacterioidetes, Proteobacteria, Spirochaetes, Actinobacteria, Verrucomicrobia, Lentisphaerae, Tenericutes, Planctomycetes, Fibrobacateres, and TM7. Bray-Curtis similarity analysis of these microbiomes indicated that microbial community composition within the same primate species are more similar to each other than to those of different primate species. Comparison of fecal microbiota from non-human primates with microbiota of human stool samples obtained in previous studies revealed that the gut microbiota of these primates are distinct and reflect host phylogeny. CONCLUSION/SIGNIFICANCE: Our analysis provides evidence that the fecal microbiomes of wild primates co-vary with their hosts, and that this is manifested in higher intraspecies similarity among wild primate species, perhaps reflecting species specificity of the microbiome in addition to dietary influences. These results contribute to the limited body of primate microbiome studies and provide a framework for comparative microbiome analysis between human and non-human primates as well as a comparative evolutionary understanding of the human microbiome.
Project description:Milk is inhabited by a community of bacteria and is one of the first postnatal sources of microbial exposure for mammalian young. Bacteria in breast milk may enhance immune development, improve intestinal health, and stimulate the gut-brain axis for infants. Variation in milk microbiome structure (e.g., operational taxonomic unit [OTU] diversity, community composition) may lead to different infant developmental outcomes. Milk microbiome structure may depend on evolutionary processes acting at the host species level and ecological processes occurring over lactation time, among others. We quantified milk microbiomes using 16S rRNA high-throughput sequencing for nine primate species and for six primate mothers sampled over lactation. Our data set included humans (Homo sapiens, Philippines and USA) and eight nonhuman primate species living in captivity (bonobo [Pan paniscus], chimpanzee [Pan troglodytes], western lowland gorilla [Gorilla gorilla gorilla], Bornean orangutan [Pongo pygmaeus], Sumatran orangutan [Pongo abelii], rhesus macaque [Macaca mulatta], owl monkey [Aotus nancymaae]) and in the wild (mantled howler monkey [Alouatta palliata]). For a subset of the data, we paired microbiome data with nutrient and hormone assay results to quantify the effect of milk chemistry on milk microbiomes. We detected a core primate milk microbiome of seven bacterial OTUs indicating a robust relationship between these bacteria and primate species. Milk microbiomes differed among primate species with rhesus macaques, humans and mantled howler monkeys having notably distinct milk microbiomes. Gross energy in milk from protein and fat explained some of the variations in microbiome composition among species. Microbiome composition changed in a predictable manner for three primate mothers over lactation time, suggesting that different bacterial communities may be selected for as the infant ages. Our results contribute to understanding ecological and evolutionary relationships between bacteria and primate hosts, which can have applied benefits for humans and endangered primates in our care.
Project description:<h4>Background</h4>Comparative data from non-human primates provide insight into the processes that shaped the evolution of the human gut microbiome and highlight microbiome traits that differentiate humans from other primates. Here, in an effort to improve our understanding of the human microbiome, we compare gut microbiome composition and functional potential in 14 populations of humans from ten nations and 18 species of wild, non-human primates.<h4>Results</h4>Contrary to expectations from host phylogenetics, we find that human gut microbiome composition and functional potential are more similar to those of cercopithecines, a subfamily of Old World monkey, particularly baboons, than to those of African apes. Additionally, our data reveal more inter-individual variation in gut microbiome functional potential within the human species than across other primate species, suggesting that the human gut microbiome may exhibit more plasticity in response to environmental variation compared to that of other primates.<h4>Conclusions</h4>Given similarities of ancestral human habitats and dietary strategies to those of baboons, these findings suggest that convergent ecologies shaped the gut microbiomes of both humans and cercopithecines, perhaps through environmental exposure to microbes, diet, and/or associated physiological adaptations. Increased inter-individual variation in the human microbiome may be associated with human dietary diversity or the ability of humans to inhabit novel environments. Overall, these findings show that diet, ecology, and physiological adaptations are more important than host-microbe co-diversification in shaping the human microbiome, providing a key foundation for comparative analyses of the role of the microbiome in human biology and health.
Project description:The primate gastrointestinal tract is home to trillions of bacteria, whose composition is associated with numerous metabolic, autoimmune, and infectious human diseases. Although there is increasing evidence that modern and Westernized societies are associated with dramatic loss of natural human gut microbiome diversity, the causes and consequences of such loss are challenging to study. Here we use nonhuman primates (NHPs) as a model system for studying the effects of emigration and lifestyle disruption on the human gut microbiome. Using 16S rRNA gene sequencing in two model NHP species, we show that although different primate species have distinctive signature microbiota in the wild, in captivity they lose their native microbes and become colonized with Prevotella and Bacteroides, the dominant genera in the modern human gut microbiome. We confirm that captive individuals from eight other NHP species in a different zoo show the same pattern of convergence, and that semicaptive primates housed in a sanctuary represent an intermediate microbiome state between wild and captive. Using deep shotgun sequencing, chemical dietary analysis, and chloroplast relative abundance, we show that decreasing dietary fiber and plant content are associated with the captive primate microbiome. Finally, in a meta-analysis including published human data, we show that captivity has a parallel effect on the NHP gut microbiome to that of Westernization in humans. These results demonstrate that captivity and lifestyle disruption cause primates to lose native microbiota and converge along an axis toward the modern human microbiome.
Project description:Social behavior can alter the microbiome composition via transmission among social partners, but there have been few controlled experimental studies of gut microbiome transmission among social partners in primates. We collected longitudinal fecal samples from eight unrelated male-female pairs of marmoset monkeys prior to pairing and for 8 weeks following pairing. We then sequenced 16S rRNA to characterize the changes in the gut microbiome that resulted from the pairing. Marmoset pairs had a higher similarity in gut microbiome communities after pairing than before pairing. We discovered sex differences in the degrees of change in gut microbiome communities following pairing. Specifically, the gut microbiome communities in males exhibited greater dissimilarity from the prepairing stage (baseline) than the gut microbiome communities in females. Conversely, females showed a gradual stabilization in the rate of the gut microbiome community turnover. Importantly, we found that the male fecal samples harbored more female-source gut microbes after pairing, especially early in pairing (paired test, P?<?0.05), possibly linked to sex bias in the frequencies of social behavior. From this controlled study, we report for the first time that pair-living primates undergo significant changes in gut microbiome during pairing and that females transmit more microbes to their partners than males do. The potential biases influencing which microbes are transmitted on the basis of sex and whether they are due to sex biases in other behavioral or physiological features need to be widely investigated in other nonhuman primates and humans in the future.IMPORTANCE In this controlled study, we collected longitudinal fecal samples from 16 male and female marmoset monkeys for 2 weeks prior to and for 8 weeks after pairing in male-female dyads. We report for the first time that marmoset monkeys undergo significant changes to the gut microbiome following pairing and that these changes are sex-biased; i.e., females transmit more microbes to their social partners than males do. Marmosets exhibit pair bonding behavior such as spatial proximity, physical contact, and grooming, and sex biases in these behavioral patterns may contribute to the observed sex bias in social transmission of gut microbiomes.
Project description:The divergence of crown catarrhines-i.e., the split of cercopithecoids (Old World monkeys) from hominoids (apes and humans)-is a poorly understood phase in our shared evolutionary history with other primates. The two groups differ in the anatomy of the hip joint, a pattern that has been linked to their locomotor strategies: relatively restricted motion in cercopithecoids vs. more eclectic movements in hominoids. Here we take advantage of the first well-preserved proximal femur of the early Oligocene stem catarrhine Aegyptopithecus to investigate the evolution of this anatomical region using 3D morphometric and phylogenetically-informed evolutionary analyses. Our analyses reveal that cercopithecoids and hominoids have undergone divergent evolutionary transformations of the proximal femur from a similar ancestral morphology that is not seen in any living anthropoid, but is preserved in Aegyptopithecus, stem platyrrhines, and stem cercopithecoids. These results highlight the relevance of fossil evidence for illuminating key adaptive shifts in primate evolution.
Project description:Alcohol-induced chronic liver disease (ALD) is becoming the most common liver disease in the world. However, there are no effective, universally accepted therapies for ALD. The etiology of ALD remains blurry so far. Historical evidence has demonstrated a link between the liver and gut microbiota. But it is difficult to distinguish the effect of gut microbiota changes caused by alcohol consumption in humans since the microbiota change detected in humans is complicated by diet and environmental factors. Due to the genetic, physiological, metabolic, and behavioral similarities to humans, the rhesus monkey provides excellent translational validity in preclinical studies, and the diet and environmental conditions can be controlled well in rhesus monkey. In our study, we explored the relationship between ALD and the gut microbiome in the rhesus monkeys with alcoholic liver steatosis. Our results showed that there was a change of the bacterial community structure in monkeys with ALD. Differences of the relative abundances of gut microbiota at phylum, order, family, genus, and species levels were observed between control monkeys and monkeys with ALD, and different pathways enriched in the monkeys with ALD were identified by metagenomic function analysis. Firmicutes, Proteobacteria, Verrucomicrobia tended to increase whereas Bacteroidetes and Actinobacteria decreased in the fecal microbiota of ALD group compared to the control group. Lactobacillales and Lactobacillus significantly decreased in ALD monkeys compared with normal monkeys, Streptococcus was lower in the ALD group compared with the control group. The non-human primate model of ALD will be useful for exploration of the microbiome markers as diagnosis and potentially prognosis for ALD. The ALD model will benefit the development of new therapeutic procedures for treating ALD and provide safety and efficacy evaluation for clinical application.
Project description:Research on the gut microbiota of free-ranging mammals is offering new insights into dietary ecology. However, for free-ranging primates, little information is available for how microbiomes are influenced by ecological variation through time. Primates inhabiting seasonal tropical dry forests undergo seasonally specific decreases in food abundance and water availability, which have been linked to adverse health effects. Throughout the course of a seasonal transition in 2014, we collected fecal samples from three social groups of free-ranging white-faced capuchin monkeys (Cebus capucinus imitator) in Sector Santa Rosa, Área de Conservación Guanacaste, Costa Rica. 16S rRNA sequencing data reveal that unlike other primates, the white-faced capuchin monkey gut is dominated by Bifidobacterium and Streptococcus. Linear mixed effects models indicate that abundances of these genera are associated with fluctuating availability and consumption of fruit and arthropods, whereas beta diversity clusters by rainfall season. Whole shotgun metagenomics revealed that the capuchin gut is dominated by carbohydrate-binding modules associated with digestion of plant polysaccharides and chitin, matching seasonal dietary patterns. We conclude that rainfall and diet are associated with the diversity, composition, and function of the capuchin gut microbiome. Additionally, microbial fluctuations are likely contributing to nutrient uptake and the health of wild primate populations.
Project description:The widespread distribution of lentiviruses among African primates, and the lack of severe pathogenesis in many of these natural reservoirs, are taken as evidence for long-term co-evolution between the simian immunodeficiency viruses (SIVs) and their primate hosts. Evidence for positive selection acting on antiviral restriction factors is consistent with virus-host interactions spanning millions of years of primate evolution. However, many restriction mechanisms are not virus-specific, and selection cannot be unambiguously attributed to any one type of virus. We hypothesized that the restriction factor TRIM5, because of its unique specificity for retrovirus capsids, should accumulate adaptive changes in a virus-specific fashion, and therefore, that phylogenetic reconstruction of TRIM5 evolution in African primates should reveal selection by lentiviruses closely related to modern SIVs. We analyzed complete TRIM5 coding sequences of 22 Old World primates and identified a tightly-spaced cluster of branch-specific adaptions appearing in the Cercopithecinae lineage after divergence from the Colobinae around 16 million years ago. Functional assays of both extant TRIM5 orthologs and reconstructed ancestral TRIM5 proteins revealed that this cluster of adaptations in TRIM5 specifically resulted in the ability to restrict Cercopithecine lentiviruses, but had no effect (positive or negative) on restriction of other retroviruses, including lentiviruses of non-Cercopithecine primates. The correlation between lineage-specific adaptations and ability to restrict viruses endemic to the same hosts supports the hypothesis that lentiviruses closely related to modern SIVs were present in Africa and infecting the ancestors of Cercopithecine primates as far back as 16 million years ago, and provides insight into the evolution of TRIM5 specificity.