Dataset Information

Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes.

ABSTRACT: The theoretical description of the forces that shape ecological communities focuses around two classes of models. In niche theory, deterministic interactions between species, individuals, and the environment are considered the dominant factor, whereas in neutral theory, stochastic forces, such as demographic noise, speciation, and immigration, are dominant. Species abundance distributions predicted by the two classes of theory are difficult to distinguish empirically, making it problematic to deduce ecological dynamics from typical measures of diversity and community structure. Here, we show that the fusion of species abundance data with genome-derived measures of evolutionary distance can provide a clear indication of ecological dynamics, capable of quantifying the relative roles played by niche and neutral forces. We apply this technique to six gastrointestinal microbiomes drawn from three different domesticated vertebrates, using high-resolution surveys of microbial species abundance obtained from carefully curated deep 16S rRNA hypervariable tag sequencing data. Although the species abundance patterns are seemingly well fit by the neutral theory of metacommunity assembly, we show that this theory cannot account for the evolutionary patterns in the genomic data; moreover, our analyses strongly suggest that these microbiomes have, in fact, been assembled through processes that involve a significant nonneutral (niche) contribution. Our results demonstrate that high-resolution genomics can remove the ambiguities of process inference inherent in classic ecological measures and permits quantification of the forces shaping complex microbial communities.

SUBMITTER: Jeraldo P

PROVIDER: S-EPMC3382495 | biostudies-literature | 2012 Jun

REPOSITORIES: biostudies-literature

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Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes.

Jeraldo Patricio P Sipos Maksim M Chia Nicholas N Brulc Jennifer M JM Dhillon A Singh AS Konkel Michael E ME Larson Charles L CL Nelson Karen E KE Qu Ani A Schook Lawrence B LB Yang Fang F White Bryan A BA Goldenfeld Nigel N

Proceedings of the National Academy of Sciences of the United States of America 20120521 25

The theoretical description of the forces that shape ecological communities focuses around two classes of models. In niche theory, deterministic interactions between species, individuals, and the environment are considered the dominant factor, whereas in neutral theory, stochastic forces, such as demographic noise, speciation, and immigration, are dominant. Species abundance distributions predicted by the two classes of theory are difficult to distinguish empirically, making it problematic to de ...[more]

PMID: 22615407

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Project description:The human microbiome consists of five major regional biomes distributed in or on our five body sites including skin, oral, lung, gut, and reproductive tract. Its biogeography (the spatial and temporal distribution of its biodiversity) has far-reaching implications to our health and diseases. Nevertheless, we currently have very limited understanding on the mechanisms shaping the biogeography, since it is often rather difficult to determine the relative importance of drift, dispersal, speciation, and selection, the four processes (mechanisms) determining the patterns of microbial biogeography and community dynamics according to a recent synthesis in community ecology and biogeography. To disentangle these mechanisms, I utilize multisite neutral (MSN) model and niche-neutral hybrid (NNH) model to analyze large number of truly multisite microbiome samples covering all five major human microbiome habitats, including 699 metacommunities and 5,420 local communities. Approximately 89% of metacommunities and 92% local communities exhibit patterns indistinguishable from neutral, and 20% indistinguishable from niche-neutral hybrid model, indicating the relative significance of stochastic neutral forces versus deterministic niche selection in shaping the biogeography of human microbiome. These findings cast supporting evidence to van der Gast's revision to classic Bass-Becking doctrine of microbial biogeography: "Some things are everywhere and some things are not. Sometimes the environment selects and sometimes it doesn't," offering the first educated guess for "some" and "sometimes" in the revised doctrine. Furthermore, the logistic/Cox regression models describing the relationships among community neutrality, niche differentiation, and key community/species characteristics (including community diversity, community/species dominance, speciation, and migration rates) were constructed to quantitatively describe the niche-neutral continuum and the influences of community/species properties on the continuum.

Project description:Using 2,733 longitudinal vaginal microbiome samples (representing local microbial communities) from 79 individuals (representing meta-communities) in the states of healthy, BV (bacterial vaginosis) and pregnancy, we assess and interpret the relative importance of stochastic forces (e.g., stochastic drifts in bacteria demography, and stochastic dispersal) vs. deterministic selection (e.g., host genome, and host physiology) in shaping the dynamics of human vaginal microbiome (HVM) diversity by an integrated analysis with multi-site neutral (MSN) and niche-neutral hybrid (NNH) modeling. It was found that, when the traditional "default" P-value = 0.05 was specified, the neutral drifts were predominant (≥50% metacommunities indistinguishable from the MSN prediction), while the niche differentiations were moderate (<20% from the NNH prediction). The study also analyzed two challenging uncertainties in testing the neutral and/or niche-neutral hybrid models, i.e., lack of full model specificity - non-unique fittings of same datasets to multiple models with potentially different mechanistic assumptions - and lack of definite rules for setting the P-value thresholds (also noted as P t -value when referring to the threshold of P-value in this article) in testing null hypothesis (model). Indeed, the two uncertainties can be interdependent, which further complicates the statistical inferences. To deal with the uncertainties, the MSN/NNH test results under a series of P-values ranged from 0.05 to 0.95 were presented. Furthermore, the influence of P-value threshold-setting on the model specificity, and the effects of woman's health status on the neutrality level of HVM were examined. It was found that with the increase of P-value threshold from 0.05 to 0.95, the overlap (non-unique) fitting of MSN and NNH decreased from 29.1 to 1.3%, whereas the specificity (uniquely fitted to data) of MSN model was kept between 55.7 and 82.3%. Also with the rising P-value threshold, the difference between healthy and BV groups become significant. These findings suggested that traditional single P-value threshold (such as the de facto standard P-value = 0.05) might be insufficient for testing the neutral and/or niche neutral hybrid models.

Project description:Background and Aims:Clines, the gradual variation in measurable traits along a geographical axis, play a major role in evolution and can contribute to our understanding of the relative roles of selective and neutral process in trait variation. Using genetic and morphological analyses, the relative contributions of neutral and non-neutral processes were explored to infer the evolutionary history of species of the series Sakawanum (genus Asarum), which shows significant clinal variation in calyx lobe length. Methods:A total of 27 populations covering the natural geographical distribution of the series Sakawanum were sampled. Six nuclear microsatellite markers were used to investigate genetic structure and genetic diversity. The lengths of calyx lobes of multiple populations were measured to quantify their geographical and taxonomic differentiation. To detect the potential impact of selective pressure, morphological differentiation was compared with genetic differentiation (QCT-FST comparison). Key Results:Average calyx lobe length of A. minamitanianum was 124.11 mm, while that of A. costatum was 13.80 mm. Though gradually changing along the geographical axis within series, calyx lobe lengths were significantly differentiated among the taxa. Genetic differentiation between taxa was low (FST = 0.099), but a significant geographical structure along the morphological cline was detected. Except for one taxon pair, pairwise QCT values were significantly higher than the neutral genetic measures of FST and G'ST. Conclusions:Divergent selection may have driven the calyx lobe length variation in series Sakawanum taxa, although the underlying mechanism is still not clear. The low genetic differentiation indicates recent divergence and/or gene flows between geographically close taxa. These neutral processes would also affect the clinal variation in calyx lobe lengths. Overall, this study implies the roles of population history and divergent selection in shaping the current cline of a flower trait in the series Sakawanum.

Dataset Information

Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes.

Publications

Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes.

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