<p>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 (<i>Poecilochirus carabi</i>), nematode (<i>Rhomborhabditis regina</i>), and their burying beetle host (<i>Nicrophorus nepalensis</i>) 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.</p>

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

  • Yu-Hsuan Lee,
  • Wei-Jiun Lin,
  • Mu-Tzu Tsai,
  • Brendan Lan,
  • Yi-Ling Chu,
  • Jiue-In Yang,
  • Syuan-Jyun Sun

摘要

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.