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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.

SUBMITTER: Gomez A

PROVIDER: S-EPMC6669335 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints.

Gomez Andres A Sharma Ashok Kumar AK Mallott Elizabeth K EK Petrzelkova Klara J KJ Jost Robinson Carolyn A CA Yeoman Carl J CJ Carbonero Franck F Pafco Barbora B Rothman Jessica M JM Ulanov Alexander A Vlckova Klara K Amato Katherine R KR Schnorr Stephanie L SL Dominy Nathaniel J NJ Modry David D Todd Angelique A Torralba Manolito M Nelson Karen E KE Burns Michael B MB Blekhman Ran R Remis Melissa M Stumpf Rebecca M RM Wilson Brenda A BA Gaskins H Rex HR Garber Paul A PA White Bryan A BA Leigh Steven R SR

mSphere 20190731 4

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 compositio ...[more]

PMID: 31366708

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Project description:In situ adaptation to climate change will be critical for the persistence of many ectotherm species due to their relative lack of dispersal capacity. Climate change is causing increases in both the mean and the variance of environmental temperature, each of which may act as agents of selection on different traits. Importantly, these traits may not be heritable or have the capacity to evolve independently from one another. When genetic constraints prevent the "baseline" values of thermal performance traits from evolving rapidly, phenotypic plasticity driven by gene expression might become critical. We review the literature for evidence that thermal performance traits in ectotherms are heritable and have genetic architectures that permit their unconstrained evolution. Next, we examine the relationship between gene expression and both the magnitude and duration of thermal stress. Finally, we identify genes that are likely to be important for adaptation to a changing climate and determine whether they show patterns consistent with thermal adaptation. Although few studies have measured narrow-sense heritabilities of thermal performance traits, current evidence suggests that the end points of thermal reaction norms (tolerance limits) are moderately heritable and have the potential to evolve rapidly. By contrast, performance at intermediate temperatures has substantially lower evolutionary potential. Moreover, evolution in many species appears to be constrained by genetic correlations such that populations can adapt to either increases in mean temperature or temperature variability, but not both. Finally, many species have the capacity for plastic expression of the transcriptome in response to temperature shifts, with the number of differentially expressed genes increasing with the magnitude, but not the duration, of thermal stress. We use these observations to develop a conceptual model that describes the likely trajectory of genome evolution in response to changes in environmental temperature. Our results indicate that extreme weather events, rather than gradual increases in mean temperature, are more likely to drive genetic and phenotypic change in wild ectotherms.

Dataset Information

Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints.

Publications

Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints.

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