Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling

Abstract

One of the most distinct but unresolved global patterns is the apparent variation in plant–symbiont nutrient strategies across biomes. This pattern is central to our understanding of plant–soil–nutrient feedbacks in the land biosphere, which, in turn, are essential for our ability to predict the future dynamics of the Earth system. Here, we present an evolution-based trait-modelling approach for resolving (1) the organization of plant–symbiont relationships across biomes worldwide and (2) the emergent consequences for plant community composition and land biogeochemical cycles. Using game theory, we allow plants to use different belowground strategies to acquire nutrients and compete within local plant–soil–nutrient cycles in boreal, temperate and tropical biomes. The evolutionarily stable strategies that emerge from this analysis allow us to predict the distribution of belowground symbioses worldwide, the sequence and timing of plant succession, the bistability of ecto- versus arbuscular mycorrhizae in temperate and tropical forests, and major differences in the land carbon and nutrient cycles across biomes. Our findings imply that belowground symbioses have been central to the evolutionary assembly of plant communities and plant–nutrient feedbacks at the scale of land biomes. We conclude that complex global patterns emerge from local between-organism interactions in the context of Darwinian natural selection and evolution, and that the underlying dynamics can be mechanistically probed by our low-dimensional modelling approach.

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Fig. 1: Timeline of the plant–symbiont relationship on land.
Fig. 2: Global geographical distribution of AMF, EMF and NFB trees.
Fig. 3: Prediction of community composition and nutrient limitation across biomes.
Fig. 4: AMF–EMF bistable states in low-fertility tropical forest, and divergence of communities into alternative stable states.
Fig. 5: Observed and predicted EMF relative abundances across the US FIA plots, and bistable dynamics in the temperate region.

Code availability

The R scripts used in Fig. 2 and MATLAB scripts used in Figs. 35 and Table 1 are available from the corresponding author upon reasonable request.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank S. Levin, D. Guo, N. Wurzburger, E. Sheffer and members of the Hedin laboratory for helpful comments, J. Sprent for sharing the nodulation database, Y. L. Qiu for sharing the mycorrhizal database, J. Lichstein and W. Liao for sharing the FIA database, Y. Sun for assisting with artwork and S. Wang for assisting with database compilation. We thank A. H. Gentry, the Missouri Botanical Garden and collectors who assisted A. H. Gentry or contributed data for specific A. H. Gentry sites. This work was supported by grants to L.O.H. from the Dean of Faculty Fund and the Carbon Mitigation Initiative at Princeton University.

Author information

M.L. and L.O.H. designed the research. M.L. compiled and analysed the belowground strategies database, performed the modelling work and analysed the output data. M.L. and L.O.H. wrote the paper.

Correspondence to Mingzhen Lu.

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Supplementary Information

Supplementary Figures 1–7, Supplementary Tables 1–3, Supplementary Notes 1–10 and Supplementary References

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Supplementary Video

Tropical forest community successional dynamics. Visual demonstration of successional dynamics (1,000 yrs) from a nutrient-poor tropical forest using a landscape of 15x15 patches. Each patch is represented by 3 trees, AMF in green, EMF in purple, and NFB in orange, with the tree height and crown radius proportional to the total biomass of each symbiotic group in each patch. The landscape recovered from 99% destruction of its equilibrium biomass, with NFB accounting for 10% of starting biomass and AMF and EMF each accounting for 45%. NFB dominated early succession, but the strategy was increasingly outcompeted by AMF as succession proceeded. In late succession, EMF became abundant and coexisted with AMF at the landscape scale as forest biomass again approached equilibrium. Throughout succession, stochastic disturbance occurred at the scale of individual patches, and contributed to the presence of NFB trees in the landscape.

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