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Dual-stressor selection alters eco-evolutionary dynamics in experimental communities

Abstract

Recognizing when and how rapid evolution drives ecological change is fundamental for our understanding of almost all ecological and evolutionary processes such as community assembly, genetic diversification and the stability of communities and ecosystems. Generally, rapid evolutionary change is driven through selection on genetic variation and is affected by evolutionary constraints, such as tradeoffs and pleiotropic effects, all contributing to the overall rate of evolutionary change. Each of these processes can be influenced by the presence of multiple environmental stressors reducing a population’s reproductive output. Potential consequences of multistressor selection for the occurrence and strength of the link from rapid evolution to ecological change are unclear. However, understanding these is necessary for predicting when rapid evolution might drive ecological change. Here we investigate how the presence of two stressors affects this link using experimental evolution with the bacterium Pseudomonas fluorescens and its predator Tetrahymena thermophila. We show that the combination of predation and sublethal antibiotic concentrations delays the evolution of anti-predator defence and antibiotic resistance compared with the presence of only one of the two stressors. Rapid defence evolution drives stabilization of the predator–prey dynamics but this link between evolution and ecology is weaker in the two-stressor environment, where defence evolution is slower, leading to less stable population dynamics. Tracking the molecular evolution of whole populations over time shows further that mutations in different genes are favoured under multistressor selection. Overall, we show that selection by multiple stressors can significantly alter eco-evolutionary dynamics and their predictability.

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Data availability

Data reported in the paper will be archived in a community archive. Raw sequence reads from genomic analyses have been deposited in the NCBI Sequence Read Archive under the BioProject accession number PRJNA476204. Count and trait data have been deposited at PANGAEA: https://doi.pangaea.de/10.1594/PANGAEA.895614.

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Acknowledgements

We are grateful to T. Niska, S. Suomalainen, T. Virolainen and J. Haafke for helping with data collection. This work was supported by an Emmy Noether Grant and Heisenberg Stipend from the German Research Foundation (DFG) to L.B. (grant nos. BE 4135/3-1 and 4135/9), and received support from the Academy of Finland to T.H. (project no. 106993), to J.L. (project no. 1255572) and to V.K. (project no. 1267541) and the Finnish Cultural Foundation to J.C. (grant no. 160149).

Author information

T.H., M.J. and L.B. conceived and designed the study. J.C., J.F., E.K. and L.B. analysed the sequence data. S.K. performed the sequencing. T.H. and J.C. collected the data. L.B. and T.H. analysed the data. J.F., T.H. and L.B. wrote the manuscript. All authors contributed to the final version of the manuscript.

Competing interests

The authors declare no competing interests.

Correspondence to Lutz Becks.

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Fig. 1: Eco-evolutionary dynamics of P. fluorescens populations exposed to sub-MIC levels of streptomycin and ciliates.
Fig. 2: Stability of bacteria–ciliate populations exposed to 0 × or 0.1 × MIC sub-MIC levels of streptomycin and the correlation of stability with defence levels of the bacteria populations.
Fig. 3: Trait correlations of clonal isolates from P. fluorescens populations exposed to 0.1 × MIC streptomycin and the ciliate T. thermophila from the end of the experiment (day 66).
Fig. 4: Molecular evolution of P. fluorescens populations exposed to 0.1 × MIC streptomycin and the ciliate T. thermophila in a factorial design.