Abstract:Microorganisms typically form diverse communities of interacting species, whose activities have tremendous impact on the plants, animals and humans they associate with. The ability to predict the structure of these complex communities is crucial to understanding and managing them. Here, we propose a simple, qualitative assembly rule that predicts community structure from the outcomes of competitions between small sets of species, and experimentally assess its predictive power using synthetic microbial communit… Show more
“…Our results contrast with other studies that have found fully hierarchical competition (e.g. Grace et al., in vascular plants; Henriksson et al., in fishes; Friedman, Higgins, & Gore, in bacteria). The variety of methods used to measure competition may contribute to this lack of consensus.…”
Section: Discussioncontrasting
confidence: 99%
“…Three‐species experiments (Kerr et al., ) and mathematical models (Laird & Schamp, ; Reichenbach et al., ; Yitbarek & Vandermeer, ) suggest that intransitive competition is less frequent in mobile taxa that compete in “global” neighbourhoods as opposed to those that compete locally (sessile organisms). This is supported by the lack of intransitive competition found in other manipulative experiments with organisms growing in well‐mixed environments, such as bacteria (Friedman et al., ), aquatic protists (Vandermeer, ), or necrophagous insects (Ulrich et al., ). Despite this, we found no strong evidence for a reduction in intransitivity in mobile taxa, mainly due to the high level observed in protists (but see Carrara et al., ) and the moderate levels found in fungi.…”
Competition can be fully hierarchical or intransitive, and this degree of hierarchy is driven by multiple factors, including environmental conditions, the functional traits of the species involved or the topology of competition networks. Studies simultaneously analysing these drivers of competition hierarchy are rare. Additionally, organisms compete either directly or via interference competition for resources or space, within a local neighbourhood or across the habitat. Therefore, the drivers of competition could change accordingly and depend on the taxa studied.
We performed the first multi‐taxon study on pairwise competition across major taxonomic groups, including experiments with vascular plants, mosses, saprobic fungi, aquatic protists and soil bacteria. We evaluated how general is competition intransitivity from the pairwise competition matrix including all species and also for each possible three‐species combination (triplets). We then examined which species were likely to engage in competitive loops and the effects of environmental conditions, competitive rank and functional traits on intransitive competition.
We found some degree of competition intransitivity in all taxa studied, with 38% to 5% of triplets being intransitive. Variance in competitive rank between species and more fertile conditions strongly reduced intransitivity, with triplets composed of species differing widely in their competitive ranks much less likely to be intransitive.
Including functional traits of the species involved more than doubled the variation explained compared to models including competitive rank only. Both trait means and variance within triplets affected the odds of them being intransitive. However, the traits responsible and the direction of trait effects varied widely between taxa, suggesting that traits can have a wide variety of effects on competition.
Synthesis. We evaluated the drivers of competition across multiple taxa and showed that productivity and competitive rank are fundamental drivers of intransitivity. We also showed that not only the functional traits of each species, but also those of the accompanying species, determine competition intransitivity. Intransitive competition is common across multiple taxa but can dampen under fertile conditions or for those species with large variance in their competitive abilities. This provides a first step towards predicting the prevalence of intransitive competition in natural communities.
“…Our results contrast with other studies that have found fully hierarchical competition (e.g. Grace et al., in vascular plants; Henriksson et al., in fishes; Friedman, Higgins, & Gore, in bacteria). The variety of methods used to measure competition may contribute to this lack of consensus.…”
Section: Discussioncontrasting
confidence: 99%
“…Three‐species experiments (Kerr et al., ) and mathematical models (Laird & Schamp, ; Reichenbach et al., ; Yitbarek & Vandermeer, ) suggest that intransitive competition is less frequent in mobile taxa that compete in “global” neighbourhoods as opposed to those that compete locally (sessile organisms). This is supported by the lack of intransitive competition found in other manipulative experiments with organisms growing in well‐mixed environments, such as bacteria (Friedman et al., ), aquatic protists (Vandermeer, ), or necrophagous insects (Ulrich et al., ). Despite this, we found no strong evidence for a reduction in intransitivity in mobile taxa, mainly due to the high level observed in protists (but see Carrara et al., ) and the moderate levels found in fungi.…”
Competition can be fully hierarchical or intransitive, and this degree of hierarchy is driven by multiple factors, including environmental conditions, the functional traits of the species involved or the topology of competition networks. Studies simultaneously analysing these drivers of competition hierarchy are rare. Additionally, organisms compete either directly or via interference competition for resources or space, within a local neighbourhood or across the habitat. Therefore, the drivers of competition could change accordingly and depend on the taxa studied.
We performed the first multi‐taxon study on pairwise competition across major taxonomic groups, including experiments with vascular plants, mosses, saprobic fungi, aquatic protists and soil bacteria. We evaluated how general is competition intransitivity from the pairwise competition matrix including all species and also for each possible three‐species combination (triplets). We then examined which species were likely to engage in competitive loops and the effects of environmental conditions, competitive rank and functional traits on intransitive competition.
We found some degree of competition intransitivity in all taxa studied, with 38% to 5% of triplets being intransitive. Variance in competitive rank between species and more fertile conditions strongly reduced intransitivity, with triplets composed of species differing widely in their competitive ranks much less likely to be intransitive.
Including functional traits of the species involved more than doubled the variation explained compared to models including competitive rank only. Both trait means and variance within triplets affected the odds of them being intransitive. However, the traits responsible and the direction of trait effects varied widely between taxa, suggesting that traits can have a wide variety of effects on competition.
Synthesis. We evaluated the drivers of competition across multiple taxa and showed that productivity and competitive rank are fundamental drivers of intransitivity. We also showed that not only the functional traits of each species, but also those of the accompanying species, determine competition intransitivity. Intransitive competition is common across multiple taxa but can dampen under fertile conditions or for those species with large variance in their competitive abilities. This provides a first step towards predicting the prevalence of intransitive competition in natural communities.
“…Our results substantiate the notion that monospecies growth parameters and pairwise interactions dominate multi‐species community dynamics (Friedman et al , ). It is possible that higher‐order interactions significantly influence community dynamics in lower dimensional multi‐species assemblages, such as three‐member consortia.…”
The ecological forces that govern the assembly and stability of the human gut microbiota remain unresolved. We developed a generalizable model‐guided framework to predict higher‐dimensional consortia from time‐resolved measurements of lower‐order assemblages. This method was employed to decipher microbial interactions in a diverse human gut microbiome synthetic community. We show that pairwise interactions are major drivers of multi‐species community dynamics, as opposed to higher‐order interactions. The inferred ecological network exhibits a high proportion of negative and frequent positive interactions. Ecological drivers and responsive recipient species were discovered in the network. Our model demonstrated that a prevalent positive and negative interaction topology enables robust coexistence by implementing a negative feedback loop that balances disparities in monospecies fitness levels. We show that negative interactions could generate history‐dependent responses of initial species proportions that frequently do not originate from bistability. Measurements of extracellular metabolites illuminated the metabolic capabilities of monospecies and potential molecular basis of microbial interactions. In sum, these methods defined the ecological roles of major human‐associated intestinal species and illuminated design principles of microbial communities.
“…For example, an L-V pairwise model and a mechanistic model both correctly predicted ratio stabilization and spatial intermixing between two strongly-cooperating populations exchanging diffusible essential metabolites (Momeni et al, 2013). In other examples, pairwise models largely captured competition outcomes and metabolic activities of three-species and four-species artificial microbial communities (Vandermeer, 1969; Guo and Boedicker, 2016; Friedman et al, 2017). On the other hand, pairwise models often failed to predict species coexistence in seven-species microbial communities (Friedman et al, 2017), although this could be due to interaction modification discussed above.10.7554/eLife.25051.006Figure 2.Chemical-mediated interactions commonly found in microbial communities.Interactions can be intra- or inter-population.…”
Section: Introductionmentioning
confidence: 99%
“…In other examples, pairwise models largely captured competition outcomes and metabolic activities of three-species and four-species artificial microbial communities (Vandermeer, 1969; Guo and Boedicker, 2016; Friedman et al, 2017). On the other hand, pairwise models often failed to predict species coexistence in seven-species microbial communities (Friedman et al, 2017), although this could be due to interaction modification discussed above.10.7554/eLife.25051.006Figure 2.Chemical-mediated interactions commonly found in microbial communities.Interactions can be intra- or inter-population. Examples are meant to be illustrative instead of comprehensive. DOI:
http://dx.doi.org/10.7554/eLife.25051.006…”
Pairwise models are commonly used to describe many-species communities. In these models, an individual receives additive fitness effects from pairwise interactions with each species in the community ('additivity assumption'). All pairwise interactions are typically represented by a single equation where parameters reflect signs and strengths of fitness effects ('universality assumption'). Here, we show that a single equation fails to qualitatively capture diverse pairwise microbial interactions. We build mechanistic reference models for two microbial species engaging in commonly-found chemical-mediated interactions, and attempt to derive pairwise models. Different equations are appropriate depending on whether a mediator is consumable or reusable, whether an interaction is mediated by one or more mediators, and sometimes even on quantitative details of the community (e.g. relative fitness of the two species, initial conditions). Our results, combined with potential violation of the additivity assumption in many-species communities, suggest that pairwise modeling will often fail to predict microbial dynamics.DOI:
http://dx.doi.org/10.7554/eLife.25051.001
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