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Given the need to predict the outcomes of (co)evolution in host-associated microbiomes, whether microbial and host fitnesses tend to trade-off, generating conflict, remains a pressing question. Examining the relationships between host and microbe fitness proxies at both the phenotypic and genomic levels can illuminate the mechanisms underlying interspecies cooperation and conflict. We examined naturally occurring genetic variation in 191 strains of the model microbial symbiont Sinorhizobium meliloti , paired with each of two host Medicago truncatula genotypes in single- or multi-strain experiments to determine how multiple proxies of microbial and host fitness were related to one another and test key predictions about mutualism evolution at the genomic scale, while also addressing the challenge of measuring microbial fitness. We found little evidence for interspecies fitness conflict; loci tended to have concordant effects on both microbe and host fitnesses, even in environments with multiple co-occurring strains. Our results emphasize the importance of quantifying microbial relative fitness for understanding microbiome evolution and thus harnessing microbiomes to improve host fitness. Additionally, we find that mutualistic coevolution between hosts and microbes acts to maintain, rather than erode, genetic diversity, potentially explaining why variation in mutualism traits persists in nature.
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Biodiversity of marine microbes is safeguarded by phenotypic heterogeneity in ecological traits
Why, contrary to theoretical predictions, do marine microbe communities harbor tremendous phenotypic heterogeneity? How can so many marine microbe species competing in the same niche coexist? We discovered a unifying explanation for both phenomena by investigating a non-cooperative game that interpolates between individual-level competitions and species-level outcomes. We identified all equilibrium strategies of the game. These strategies represent the probability distribution of competitive abilities (e.g. traits) and are characterized by maximal phenotypic heterogeneity. They are also neutral towards each other in the sense that an unlimited number of species can co-exist while competing according to the equilibrium strategies. Whereas prior theory predicts that natural selection would minimize trait variation around an optimum value, here we obtained a mathematical proof that species with maximally variable traits are those that endure. This discrepancy may reflect a disparity between predictions from models developed for larger organisms in contrast to our microbe-centric model. Rigorous mathematics proves that phenotypic heterogeneity is itself a mechanistic underpinning of microbial diversity. This discovery has fundamental ramifications for microbial ecology and may represent an adaptive reservoir sheltering biodiversity in changing environmental conditions.
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- Award ID(s):
- 1736635
- PAR ID:
- 10333562
- Editor(s):
- Belgrano, Andrea
- Date Published:
- Journal Name:
- PLOS ONE
- Volume:
- 16
- Issue:
- 8
- ISSN:
- 1932-6203
- Page Range / eLocation ID:
- e0254799
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pone.0254799
