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The assembly and maintenance of microbial diversity in natural communities, despite the abundance of toxin-based antagonistic interactions, presents major challenges for biological understanding. A common framework for investigating such antagonistic interactions involves cyclic dominance games with pairwise interactions. The incorporation of higher-order interactions in such models permits increased levels of microbial diversity, especially in communities in which antibiotic-producing, sensitive, and resistant strains coexist. However, most such models involve a small number of discrete species, assume a notion of pure cyclic dominance, and focus on low mutation rate regimes, none of which well represent the highly interlinked, quickly evolving, and continuous nature of microbial phenotypic space. Here, we present an alternative vision of spatial dynamics for microbial communities based on antagonistic interactions—one in which a large number of species interact in continuous phenotypic space, are capable of rapid mutation, and engage in both direct and higher-order interactions mediated by production of and resistance to antibiotics. Focusing on toxin production, vulnerability, and inhibition among species, we observe highly divergent patterns of diversity and spatial community dynamics. We find that species interaction constraints (rather than mobility) best predict spatiotemporal disturbance regimes, whereas community formation time, mobility, and mutation size best explain patterns of diversity. We also report an intriguing relationship among community formation time, spatial disturbance regimes, and diversity dynamics. This relationship, which suggests that both higher-order interactions and rapid evolution are critical for the origin and maintenance of microbial diversity, has broad-ranging links to the maintenance of diversity in other systems.
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Spatiotemporal ecological chaos enables gradual evolutionary diversification without niches or tradeoffs
Ecological and evolutionary dynamics are intrinsically entwined. On short timescales, ecological interactions determine the fate and impact of new mutants, while on longer timescales evolution shapes the entire community. Here, we study the evolution of large numbers of closely related strains with generalized Lotka Volterra interactions but no niche structure. Host-pathogen-like interactions drive the community into a spatiotemporally chaotic state characterized by continual, spatially-local, blooms and busts. Upon the slow serial introduction of new strains, the community diversifies indefinitely, accommodating an arbitrarily large number of strains in spite of the absence of stabilizing niche interactions. The diversifying phase persists — albeit with gradually slowing diversification — in the presence of general, nonspecific, fitness differences between strains, which break the assumption of tradeoffs inherent in much previous work. Building on a dynamical-mean field-theory analysis of the ecological dynamics, an approximate effective model captures the evolution of the diversity and distributions of key properties. This work establishes a potential scenario for understanding how the interplay between evolution and ecology — in particular coevolution of a bacterial and a generalist phage species — could give rise to the extensive fine-scale diversity that is ubiquitous in the microbial world.
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- Award ID(s):
- 2210386
- PAR ID:
- 10435855
- Date Published:
- Journal Name:
- eLife
- Volume:
- 12
- ISSN:
- 2050-084X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.7554/eLife.82734
