Highlights d Quantum-dot technology can be used to track trading strategies of mycorrhizal fungi d Increasing exposure to inequality stimulates trade and resource movement d Fungal trade strategies are not uniform across the symbiotic network d Fungi can capitalize on trade by first moving resources to areas of high demand

Arbuscular mycorrhizal fungi function as conduits for underground nutrient transport. While the fungal partner is dependent on the plant host for its carbon (C) needs, the amount of nutrients that the fungus allocates to hosts can vary with context. Because fungal allocation patterns to hosts can change over time, they have historically been difficult to quantify accurately. We developed a technique to tag rock phosphorus (P) apatite with fluorescent quantum-dot (QD) nanoparticles of three different colors, allowing us to study nutrient transfer in an in vitro fungal network formed between two host roots of different ages and different P demands over a 3-week period. Using confocal microscopy and raster image correlation spectroscopy, we could distinguish between P transfer from the hyphae to the roots and P retention in the hyphae. By tracking QD-apatite from its point of origin, we found that the P demands of the younger root influenced both: (1) how the fungus distributed nutrients among different root hosts and (2) the storage patterns in the fungus itself. Our work highlights that fungal trade strategies are highly dynamic over time to local conditions, and stresses the need for precise measurements of symbiotic nutrient transfer across both space and time.

The rhizosphere has been called "one of the most complex ecosystems on earth" because it is a hotspot for interactions among millions of microbial cells. Many of these are microbes are also participating in a dynamic interplay with host plant tissues, signaling pathways, and metabolites. Historically, breeders have employed a plant-centric perspective when trying to harness the potential of microbiome-derived benefits to improve productivity and resilience of economically important plants. This is potentially problematic because: (i) the evolution of the microbes themselves is often ignored, and (ii) it assumes that the fitness of interacting plants and microbes is strictly aligned. In contrast, a microbe-centric perspective recognizes that putatively beneficial microbes are still under selection to increase their own fitness, even if there are costs to the host. This can lead to the evolution of sophisticated, potentially subtle, ways for microbes to manipulate the phenotype of their hosts, as well as other microbes in the rhizosphere. We illustrate this idea with a review of cases where rhizosphere microbes have been demonstrated to directly manipulate host root growth, architecture and exudation, host nutrient uptake systems, and host immunity and defense. We also discuss indirect effects, whereby fitness outcomes for the plant are a consequence of ecological interactions between rhizosphere microbes. If these consequences are positive for the plant, they can potentially be misconstrued as traits that have evolved to promote host growth, even if they are a result of selection for unrelated functions. The ubiquity of both direct microbial manipulation of hosts and context-dependent, variable indirect effects leads us to argue that an evolutionary perspective on rhizosphere microbial ecology will become increasingly important as we continue to engineer microbial communities for crop production.

Theory suggests that relatives will cooperate more, and compete less, because of an increased benefit for shared genes. In symbiotic partnerships, hosts may benefit from interacting with highly related symbionts because there is less conflict among the symbionts. This has been difficult to test empirically. We used the arbuscular mycorrhizal symbiosis to study the effects of fungal relatedness on host and fungal benefits, creating fungal networks varying in relatedness between two hosts, both in soil and in‐vitro. To determine how fungal relatedness affected overall transfer of nutrients, we fluorescently tagged phosphorus and quantified resource distribution between two root systems. We found that colonization by less‐related fungi was associated with increased fungal growth, lower transport of nutrients across the network, and lower plant benefit ‐ likely an outcome of increased fungal competition. More generally, we demonstrate how symbiont relatedness can mediate benefits of symbioses.

For over 300 million years, insects have relied on symbiotic microbes for nutrition and defence1,2. However, it is unclear whether specific ecological conditions have repeatedly favoured the evolution of symbioses, and how this has influenced insect diversification1,3,4. Using data on 1844 microbe-insect symbioses across 400 insect families, we found that symbionts have allowed insects to radiate into a range of feeding niches deficient in B vitamins, including phloem, blood and wood. In some cases, such as herbivorous insects, the shift to a new niche has resulted in spectacular species proliferation. In other niches, such as strict blood feeding, diversification has been severely constrained. Symbioses therefore appear to solve universal nutrient deficiencies for insects, but the consequences for insect diversification depend on the feeding niche invaded.

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For over 300 million years, insects have relied on symbiotic microbes for nutrition and defence1,2. However, it is unclear whether specific ecological conditions have repeatedly favoured the evolution of symbioses, and how this has influenced insect diversification1,3,4. Using data on 1849 microbe-insect symbioses across 402 insect families, we found that symbionts have allowed insects to specialize on a range of nutrient-imbalanced diets, including phloem, blood and wood. Across diets, the only limiting nutrient consistently associated with the evolution of obligate symbiosis was B vitamins. The shift to new diets, facilitated by symbionts, had mixed consequences for insect diversification. In some cases, such as herbivory, it resulted in spectacular species proliferation. In other niches, such as strict blood feeding, diversification has been severely constrained. Symbioses therefore appear to solve widespread nutrient deficiencies for insects, but the consequences for insect diversification depend on the feeding niche invaded.

No abstract