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Context-dependent indirect effects mediate ecological transitions between parasitism and mutualism

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Abstract

Symbiotic interactions frequently shift along a mutualism-parasitism continuum, altering host fitness, population dynamics, and microbial community structure with ecological context. Here, we integrate field surveys, reciprocal breeding experiments, feeding assays, and microbiome profiling to dissect interactions between phoretic mite (Poecilochirus carabi), nematode (Rhomborhabditis regina), and their burying beetle host (Nicrophorus nepalensis) during reproduction. We show that high nematode densities reduce beetle offspring survival during metamorphosis, but co-occurring mites mitigate these costs by preying on nematodes and suppressing vertical transmission, thereby enhancing beetle fitness. Both mites and nematodes are equally effective at suppressing bacterial loads on carrion, but mites drive greater shifts in carcass microbiome composition. Carcasses exposed to both symbionts display the most pronounced shifts in bacterial communities, suggesting that inter-symbiont interactions have cascading effects on host-associated microbiota. Intriguingly, in the absence of nematodes, mites impose fitness costs on their beetle hosts. These results demonstrate that the net effects of mites on beetle fitness emerge largely through indirect, density-dependent interactions with nematodes and microbial competitors. By integrating macro-symbiont and microbiome perspectives, our study highlights how phoresy extends beyond passive dispersal to actively restructure host–symbiont networks, highlighting the overlooked potential of indirect effects in driving context-dependent mutualism within multisymbiotic systems.

Data availability

The source data behind the figures in the paper are available in Zenodo (https://doi.org/10.5281/zenodo.17397723)54. Nucleotide sequence data have been deposited in GenBank under accession numbers PZ145830–PZ145848. Raw 16S rRNA gene sequencing reads have been deposited in the NCBI Sequence Read Archive (SRA) under BioProject accession PRJNA1435584. Any remaining information can be obtained from the corresponding author upon reasonable request.

Code availability

The R script for our analyses was deposited in Zenodo (https://doi.org/10.5281/zenodo.17397723)54.

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Acknowledgements

We thank the four anonymous reviewers for their insightful comments on this manuscript. We thank Megan M.Y. Chang for helping with illustrations. We thank Shao-Chi Huang, Yi-Fei Fang, Yi-Zhen Wu and Yi-Ta Wu for logistic support in the lab. We are very grateful to Chia-Lin Chung for comments on this manuscript, as well as support for bacterial culturing assay. Y.-H.L. was supported by a College Student Research Scholarship, National Science and Technology Council (113CFA0100068); S.-J.S. was supported by the NTU New Faculty Founding Research Grant, National Science and Technology Council 2030 Cross-Generation Young Scholars Program (112-2628-B-002-013-; 113-2628-B-002-028-; 114-2628-B-002-027-), Academic Research-Career Development Project (Sprout Research Projects; 114L7869) provided by National Taiwan University, and the Yushan Fellow Program (MOE-111-YSFAG-0003-002-P1) provided by the Ministry of Education.

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Authors and Affiliations

  1. International Degree Program in Climate Change and Sustainable Development, National Taiwan University, Taipei, Taiwan

    Yu-Hsuan Lee, Mu-Tzu Tsai & Syuan-Jyun Sun

  2. Department of Plant Pathology and Microbiology, National Taiwan University, Taipei, Taiwan

    Yu-Hsuan Lee & Yi-Ling Chu

  3. Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei, Taiwan

    Wei-Jiun Lin

  4. Department of Biology, Duke University, Durham, NC, USA

    Brendan Lan

  5. Department of Nematology, University of California, Riverside, CA, USA

    Jiue-In Yang

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  1. Yu-Hsuan Lee
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Contributions

Y.-H.L. and S.-J.S. conceived the study. Y.-H.L., W.-J.L., M.-T.T., B.L., Y.-L. C. and S.-J.S. collected the data. Y.-H.L. and J.-I.Y. conducted the nematode identification. Y.-H.L. and S.-J.S. analysed the data. All authors wrote the paper and approved the final manuscript.

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Correspondence to
Syuan-Jyun Sun.

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Communications Biology thanks Enric Frago and the other anonymous reviewer(s) for their contribution to the peer review of this work. Primary Handling Editor: Rupali Sathe. A peer review file is available.

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Lee, YH., Lin, WJ., Tsai, MT. et al. Context-dependent indirect effects mediate ecological transitions between parasitism and mutualism.
Commun Biol (2026). https://doi.org/10.1038/s42003-026-09945-9

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