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For over 300 million years, insects have relied on symbiotic microbes for nutrition and defence. However, it is unclear whether specific ecological conditions have repeatedly favoured the evolution of symbioses, and how this has influenced insect diversification. Here, using data on 1,850 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 that is invaded.

Fluorescent nanoparticles (FNPs) have been widely used in chemistry and medicine for decades, but their employment in biology is relatively recent. Past reviews on FNPs have focused on chemical, physical or medical uses, making the extrapolation to biological applications difficult. In biology, FNPs have largely been used for biosensing and molecular tracking. However, concerns over toxicity in early types of FNPs, such as cadmium-containing quantum dots (QDs), may have prevented wide adoption. Recent developments, especially in non-Cd-containing FNPs, have alleviated toxicity problems, facilitating the use of FNPs for addressing ecological, physiological and molecule-level processes in biological research. Standardised protocols from synthesis to application and interdisciplinary approaches are critical for establishing FNPs in the biologists’ tool kit. Here, we present an introduction to FNPs, summarise their use in biological applications, and discuss technical issues such as data reliability and biocompatibility. We assess whether biological research can benefit from FNPs and suggest ways in which FNPs can be applied to answer questions in biology. We conclude that FNPs have a great potential for studying various biological processes, especially tracking, sensing and imaging in physiology and ecology.

Microbiota of crop ancestors may offer a way to enhance sustainable food production

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.

High-throughput sequencing (e.g., amplicon and shotgun) has provided new insight into the diversity and distribution of fungi around the globe, but developing a framework to understand this diversity has proved challenging. Here we review key ecological strategy theories developed for macro-organisms and discuss ways that they can be applied to fungi. We suggest that while certain elements may be applied, an easy translation does not exist. Particular aspects of fungal ecology, such as body size and growth architecture, which are critical to many existing strategy schemes, as well as guild shifting, need special consideration in fungi. Moreover, data on shifts in traits across environments, important to the development of strategy schemes for macro-organisms, also does not yet exist for fungi. We end by suggesting a way forward to add data. Additional data can open the door to the development of fungi-specific strategy schemes and an associated understanding of the trait and ecological strategy dimensions employed by the world's fungi.

SUMMARYInsects evolve dependencies - often extreme - on microbes for nutrition. These include cases where insects harbour multiple endosymbionts that function collectively as a metabolic unit. How do these metabolic co-dependencies originate, and is there a predictable sequence of events leading to the integration of new symbionts? While dependency on multiple nutrient-provisioning symbionts has evolved numerous times across sap-feeding insects, there is only one known case of metabolic co-dependency in aphids, between Buchnera aphidicola and Serratia symbiotica in the Lachninae subfamily. Here we identify three additional independent transitions to the same co-obligate symbiosis in different aphids. A comparison of recent and ancient associations allows us to investigate intermediate stages of metabolic and physical integration between the typically facultative symbiont, Serratia, and the ancient obligate symbiont Buchnera. We find that these uniquely replicated evolutionary events support the idea that co-obligate associations initiate in a predictable manner, through parallel evolutionary processes. Specifically, we show (i) how the repeated losses of the riboflavin pathway in Buchnera leads to dependency on Serratia, (ii) evidence of a stepwise process of symbiont integration, whereby dependency evolves first, then essential amino acid pathways are lost (at ~30-60MYA), which coincides with increased physical integration of the companion symbiont; and (iii) dependency can evolve prior to specialised structures (e.g. bacteriocytes), and in one case with no direct nutritional basis. More generally, our results suggest the energetic costs of synthesising nutrients may provide a unified explanation for the sequence of gene loses that occur during the evolution of co-obligate symbiosis.

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.

Outside humans, true agriculture was previously thought to be restricted to social insects farming fungus. However, obligate farming of plants by ants was recently discovered in Fiji, prompting a re-examination of plant cultivation by ants. Here, we generate a database of plant cultivation by ants, identify three main types, and show that these interactions evolved primarily for shelter rather than food. We find that plant cultivation evolved at least 65 times independently for crops (~200 plant species), and 15 times in farmer lineages (~37 ant taxa) in the Neotropics and Asia/Australasia. Because of their high evolutionary replication, and variation in partner dependence, these systems are powerful models to unveil the steps in the evolution and ecology of insect agriculture.

Diverse forms of cultivation have evolved across the tree of life. Efficient farming requires that the farmer deciphers and actively promotes conditions that increase crop yield. For plant cultivation, this can include evaluating tradeoffs among light, nutrients, and protection against herbivores. It is not understood if, or how, nonhuman farmers evaluate local conditions to increase payoffs. Here, we address this question using an obligate farming mutualism between the ant Philidris nagasau and epiphytic plants in the genus Squamellaria that are cultivated for their nesting sites and floral rewards. We focused on the ants' active fertilization of their crops and their protection against herbivory. We found that ants benefited from cultivating plants in full sun, receiving 7.5-fold more floral food rewards compared to shade-cultivated plants. The higher reward levels correlated with higher levels of crop protection provided by the ants. However, while high-light planting yielded the greatest immediate food rewards, sun-grown crops contained less nitrogen compared to shade-grown crops. This was due to lower nitrogen input from ants feeding on floral rewards instead of insect protein gained from predation. Despite this tradeoff, farming ants optimize crop yield by selectively planting their crops in full sun. Ancestral state reconstructions across this ant-plant clade show that a full-sun farming strategy has existed for millions of years, suggesting that nonhuman farmers have evolved the means to evaluate and balance conflicting crop needs to their own benefit.

Biological market theory provides a conceptual framework to analyse trade strategies in symbiotic partnerships. A key prediction of biological market theory is that individuals can influence resource value – meaning the amount a partner is willing to pay for it – by mediating where and when it is traded. The arbuscular mycorrhizal symbiosis, characterised by roots and fungi trading phosphorus and carbon, shows many features of a biological market. However, it is unknown if or how fungi can control phosphorus value when exposed to abrupt changes in their trade environment. We mimicked an economic ‘crash’, manually severing part of the fungal network (Rhizophagus irregularis) to restrict resource access, and an economic ‘boom’ through phosphorus additions. We quantified trading strategies over a 3-wk period using a recently developed technique that allowed us to tag rock phosphate with fluorescing quantum dots of three different colours. We found that the fungus: compensated for resource loss in the ‘crash’ treatment by transferring phosphorus from alternative pools closer to the host root (Daucus carota); and stored the surplus nutrients in the ‘boom’ treatment until root demand increased. By mediating from where, when and how much phosphorus was transferred to the host, the fungus successfully controlled resource value.

Relatives are expected to cooperate more and compete less. In symbiotic partnerships, hosts may benefit from interacting with highly-related symbionts because there is less conflict. 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 (self vs. non-self) between two host plants, in both soil and in-vitro systems. To determine how fungal relatedness affected overall transfer of nutrients to host roots, we fluorescently tagged phosphorus and quantified resource distribution. We imaged fungal networks, and related fractal dimension to fungal growth strategies. We found that decreased relatedness was associated with increased fungal growth and complexity, lower transport of nutrients across the fungal network, and lower plant benefit, likely an outcome of increased fungal competition. More generally, we demonstrate how relatedness among symbionts can mediate the overall benefits of symbiotic partnerships.

While the importance of mutualisms across the tree of life is recognized, it is not understood why some organisms evolve high levels of dependence on mutualistic partnerships, while other species remain autonomous or retain or regain minimal dependence on partners. We identify four main pathways leading to the evolution of mutualistic dependence. Then, we evaluate current evidence for three predictions: ( a) Mutualisms with different levels of dependence have distinct stabilizing mechanisms against exploitation and cheating, ( b) less dependent mutualists will return to autonomy more often than those that are highly dependent, and ( c) obligate mutualisms should be less context dependent than facultative ones. Although we find evidence supporting all three predictions, we stress that mutualistic partners follow diverse paths toward—and away from—dependence. We also highlight the need to better examine asymmetry in partner dependence. Recognizing how variation in dependence influences the stability, breakdown, and context dependence of mutualisms generates new hypotheses regarding how and why the benefits of mutualistic partnerships differ over time and space.

Across the tree of life, hosts have evolved mechanisms to control and mediate interactions with symbiotic partners. We suggest that the evolution of physical structures that allow hosts to spatially separate symbionts, termed compartmentalization, is a common mechanism used by hosts. Such compartmentalization allows hosts to: (i) isolate symbionts and control their reproduction; (ii) reward cooperative symbionts and punish or stop interactions with non-cooperative symbionts; and (iii) reduce direct conflict among different symbionts strains in a single host. Compartmentalization has allowed hosts to increase the benefits that they obtain from symbiotic partners across a diversity of interactions, including legumes and rhizobia, plants and fungi, squid andVibrio, insects and nutrient provisioning bacteria, plants and insects, and the human microbiome. In cases where compartmentalization has not evolved, we ask why not. We argue that when partners interact in a competitive hierarchy, or when hosts engage in partnerships which are less costly, compartmentalization is less likely to evolve. We conclude that compartmentalization is key to understanding the evolution of symbiotic cooperation.This article is part of the theme issue ‘The role of the microbiome in host evolution’.

The nutrient exchange mutualism between arbuscular mycorrhizal fungi (AMFs) and their host plants qualifies as a biological market, but several complications have hindered its appropriate use. First, fungal ‘trading agents’ are hard to identify because AMFs are potentially heterokaryotic, that is, they may contain large numbers of polymorphic nuclei. This means it is difficult to define and study a fungal ‘individual’ acting as an independent agent with a specific trading strategy. Second, because nutrient exchanges occur via communal structures (arbuscules), this temporarily reduces outbidding competition and transaction costs and hence resembles exchanges among divisions of firms, rather than traditional trade on markets. We discuss how fungal nuclei may coordinate their trading strategies, but nevertheless retain some independence, similar to human co-operatives (co-ops).

In an era of ecosystem degradation and climate change, maximizing microbial functions in agroecosystems has become a prerequisite for the future of global agriculture. However, managing species-rich communities of plant-associated microbiomes remains a major challenge. Here, we propose interdisciplinary research strategies to optimize microbiome functions in agroecosystems. Informatics now allows us to identify members and characteristics of 'core microbiomes', which may be deployed to organize otherwise uncontrollable dynamics of resident microbiomes. Integration of microfluidics, robotics and machine learning provides novel ways to capitalize on core microbiomes for increasing resource-efficiency and stress-resistance of agroecosystems.

The functional relationship between arbuscular mycorrhizal fungi (AMF) and their hosts is variable on small spatial scales. Here, we hypothesized that herbivore exclusion changes the AMF community and alters the ability of AMF to enhance plant tolerance to grazing. We grew the perennial bunchgrass, Themeda triandra Forssk in inoculum from soils collected in the Kenya Long-term Exclosure Experiment where treatments representing different levels of herbivory have been in place since 1995. We assessed AMF diversity in the field, using terminal restriction fragment length polymorphism and compared fungal diversity among treatments. We conducted clipping experiments in the greenhouse and field and assessed regrowth. Plants inoculated with AMF from areas accessed by wild herbivores and cattle had greater biomass than non-inoculated controls, while plants inoculated with AMF from where large herbivores were excluded did not benefit from AMF in terms of biomass production. However, only the inoculation with AMF from areas with wild herbivores and no cattle had a positive effect on regrowth, relative to clipped plants grown without AMF. Similarly, in the field, regrowth of plants after clipping in areas with only native herbivores was higher than other treatments. Functional differences in AMF were evident despite little difference in AMF species richness or community composition. Our findings suggest that differences in large herbivore communities over nearly two decades has resulted in localized, functional changes in AMF communities. Our results add to the accumulating evidence that mycorrhizae are locally adapted and that functional differences can evolve within small geographical areas.

Liming and fertilization of grasslands have been used for centuries to sustain hay production. Besides improving hay yields, these practices induce compositional shifts in plant and soil microbial communities, including symbiotic arbuscular mycorrhizal (AM) fungi. However, in spite of increasing interest in soil carbon (C) sequestration to offset anthropogenic CO2 emissions, little is known about the long-term effects of these agronomic interventions on soil C stocks. We examined how plants, AM fungi, and soil C respond to more than seven decades of annual applications of lime, mineral nitrogen (N), and mineral phosphorus (P) to test the hypotheses that (1) management practices increasing aboveground plant production decrease C allocation to roots, AM fungi and the soil; and (2) the relative availability of N and P predicts belowground C allocation in a consistent manner. Our study was conducted at the Rengen Grassland Experiment, established in 1941. Lime combined with N increased hay yields and promoted development of AM fungal hyphae in soil, while reducing relative C allocation to roots. Simultaneous enrichment of soil with lime, N, and P further boosted hay production, promoted grasses and suppressed other plant functional groups. This treatment also decreased soil organic C and strongly suppressed AM fungi in the soil, although the response to P varied among different AM fungal taxa. Our results indicate that agricultural management practices aimed at maximization of hay production may, in the long run, significantly (−20%) reduce belowground C storage. This is a great concern with respect to the intended use of grasslands as anthropogenic CO2 sinks because the fertilization-induced decrease in soil C stocks can partly or fully negate the C sequestration potential of the grassland ecosystems as a whole.

Mutualisms – cooperative interactions among different species – are known to influence global biodiversity. Nevertheless, theoretical and empirical work has led to divergent hypotheses about how mutualisms modulate diversity. We ask here when and how mutualisms influence species richness. Our synthesis suggests that mutualisms can promote or restrict species richness depending on mutualist function, the level of partner dependence, and the specificity of the partnership. These characteristics, which themselves are influenced by environmental and geographic variables, regulate species richness at different scales by modulating speciation, extinction, and community coexistence. Understanding the relative impact of these mechanisms on species richness will require the integration of new phylogenetic comparative models as well as the manipulation and monitoring of experimental communities and their resulting interaction networks.

Cooperative interactions among species, termed mutualisms, have played a crucial role in the evolution of life on Earth. However, despite key potential benefits to partners, there are many cases where two species cease to cooperate, and mutualisms break down. What factors drive the evolutionary breakdown of mutualism? We examined the pathways towards breakdowns of the mutualism between plants and arbuscular mycorrhizal (AM) fungi. Using a comparative approach, we identify ~25 independent cases of complete mutualism breakdown across global seed plants. We found that breakdown of cooperation was only stable when host plants either: (i) partner with other root symbionts or (ii) evolve alternative resource acquisition strategies. Our results suggest that key mutualistic services are only permanently lost if hosts evolve alternative symbioses or adaptations.Significance StatementCooperative interactions among species – mutualisms – are major sources of evolutionary innovation. However, despite their importance, two species that formerly cooperated sometimes cease their partnership. Why do mutualisms breakdown? We asked this question in the partnership between arbuscular mycorrhizal (AM) fungi and their plant hosts, one of the most ancient mutualisms. We analyse two potential trajectories towards evolutionary breakdown of their cooperation, symbiont switching and mutualism abandonment. We find evidence that plants stop interacting with AM fungi when they switch to other microbial mutualists or when they evolve alternative strategies to extract nutrients from the environment. Our results show vital cooperative interactions can be lost - but only if successful alternatives evolve.

International audience; Plants are exemplified by high plasticity in resource allocation strategies which allows them to maximize their fitness under changing resource conditions. In many plant species, obtaining resources involves mutualistic interactions with arbuscular mycorrhizal fungi (AMF), where plants provide the AMF with sugars in exchange for soil nutrients like phosphorus (P). These nutrient exchange rates have high context dependency, influenced by both the cooperative level of the AMF species involved (a qualitative trait) and the ambient nutrient concentrations in the soil (a quantitative value). Because this context dependency arises from a mix of both quantitative and qualitative factors, standard ordinary differential equation (ODE) modeling methods often complicate the representation of resource allocation strategies. Here, we explore the utility of a hybrid automata modeling framework that can intuitively combine the qualitative AMF traits and quantitative nutrient concentrations. This allows for a better analysis and understanding of phenotypic plasticity in resource allocation in the plant–AMF, and other nutrient exchange mutualisms. We consider a focal strategy in which nutrients are allocated to growth at times of nutrient limitations, and to storage otherwise and ask how this changes plant allocation to growth vs. storage. We first model this system dynamically to show how the plant responds to different environmental conditions and interacts with AMF and show that our hybrid automata model can replicate experimental data from the plant–AMF system. From our work, novel perceptions into the well-studied plant–AMF symbiosis and testable hypotheses can be underlined: (1) leaf biomass does not increase proportionally with the level of AMF cooperation; (2) in the context of multiple AMF simultaneously colonizing a host–plant, a narrow variance of response is observed and explained by an auction-like mechanism of the AMF to acquire C from the plant.

Strains of arbuscular mycorrhizal fungi (AMF) differ markedly in the growth benefits they provide to plants. We investigated whether these differences depend on the chemical form of inorganic phosphorus. The closely related AMF Glomus custos and Rhizophagus irregularis were compared using Plantago lanceolata as the host plant, grown in quartz sand with either soluble orthophosphate or sparingly soluble hydroxyapatite as a sole source of phosphorus. In a growth experiment with AMF-inoculated plants in a climate chamber, sampling at 3-wk intervals enabled a detailed time-resolved analysis of shoot and root phosphorus concentrations and growth performance of P. lanceolata. The ability of AMF to enhance plant growth and deliver phosphate depended strongly on the identity of the available phosphorus source. In orthophosphate-amended substrate only modest differences in plant growth performance (dry matter accumulation and allocation, phosphorus acquisition) were observed between the two AMFs, despite evident AMF root colonization as shown by strain-specific mtLSU qPCR analysis. The treatment with hydroxyapatite however, created stringent growth-limiting conditions and significantly increased the growth benefit provided by R. irregularis over G. custos and the non-mycorrhizal treatment. Plants with R. irregularis could acquire much more phosphorus from apatite compared to G. custos. There were also differences in shoot-to-root dry matter allocation and plant tissue phosphorus concentrations between the R. irregularis and G. custos treatments. Our observations suggest that in experiments on the symbiosis between plants and mycorrhizal fungi more attention should be paid to the chemical form of phosphorus in soil.

Priority effects - the impact of a species' arrival on subsequent community development - have been shown to influence species composition in many organisms. Whether priority effects among arbuscular mycorrhizal fungi (AMF) structure fungal root communities is not well understood. Here, we investigated whether priority effects influence the success of two closely related AMF species (Rhizophagus irregularis and Glomus aggregatum), hypothesizing that a resident AMF suppresses invader success, this effect is time-dependent and a resident will experience reduced growth when invaded. We performed two glasshouse experiments using modified pots, which permitted direct inoculation of resident and invading AMF on the roots. We quantified intraradical AMF abundances using quantitative PCR and visual colonization percentages. We found that both fungi suppressed the invading species and that this effect was strongly dependent on the time lag between inoculations. In contrast to our expectations, neither resident AMF was negatively affected by invasion. We show that order of arrival can influence the abundance of AMF species colonizing a host. These priority effects can have important implications for AMF ecology and the use of fungal inocula in sustainable agriculture.

There is a widespread recognition that above- and below-ground organisms are linked through their interactions with host plants that span terrestrial subsystems. In addition to direct effects on plants, soil organisms such as root herbivores can indirectly alter interactions between plants and other community members, with potentially important effects on plant growth and fitness. We manipulated root herbivory by Acalymma vittatum in Cucumis sativus to determine indirect effects on arbuscular mycorrhizal fungi, leaf herbivory, the leaf pathogen downy mildew and pollinators. We also manipulated pollen receipt by plants to determine whether root herbivory reduced plant reproduction through changes in pollinator visitation. Overall, root herbivory had strong net negative effects on plant growth and fitness, with 34% reductions in both leaf and fruit production by high root damage levels relative to control, despite reduced infection by downy mildew. High root herbivory also reduced floral visitation by 39%, apparently due to lower flower production, as flower size and scent were unaffected. Above-ground herbivory was not affected by root herbivores. Although root herbivory reduced pollinator visits, pollen receipt manipulations had no effect on fruit set, indicating that reduced pollinator service did not affect plant reproduction. Synthesis. Root herbivory had indirect effects on a range of community members, including mutualists and antagonists both above- and below-ground. Although reduced pathogen infection associated with root herbivory would be expected to benefit plants, root herbivory had an overall strong negative effect on plant growth and reproduction, indicating that direct negative effects over-rode any potential indirect benefits. Soil organisms such as root herbivores can indirectly alter interactions between plants and other community members. Here, root damage had indirect effects on a range of community members, including mutualists and antagonists both above- and below-ground. However, direct negative effects of root herbivory were more important for reducing plant growth and fitness.

Mutualistic interactions with microbes have played a crucial role in the evolution and ecology of animal hosts. However, it is unclear what factors are most important in influencing particular host–microbe associations. While closely related animal species may have more similar microbiota than distantly related species due to phylogenetic contingencies, social partnerships with other organisms, such as those in which one animal farms another, may also influence an organism's symbiotic microbiome. We studied a mutualistic network of Brachymyrmex and Lasius ants farming several honeydew‐producing Prociphilus aphids and Rhizoecus mealybugs to test whether the mutualistic microbiomes of these interacting insects are primarily correlated with their phylogeny or with their shared social partnerships. Our results confirm a phylogenetic signal in the microbiomes of aphid and mealybug trophobionts, with each species harbouring species‐specific endosymbiont strains of Buchnera (aphids), Tremblaya and Sodalis (mealybugs), and Serratia (both mealybugs and aphids) despite being farmed by the same ants. This is likely explained by strict vertical transmission of trophobiont endosymbionts between generations. In contrast, our results show the ants’ microbiome is possibly shaped by their social partnerships, with ants that farm the same trophobionts also sharing strains of sugar‐processing Acetobacteraceae bacteria, known from other honeydew‐feeding ants and which likely reside extracellularly in the ants’ guts. These ant–microbe associations are arguably more “open” and subject to horizontal transmission or social transmission within ant colonies. These findings suggest that the role of social partnerships in shaping a host's symbiotic microbiome can be variable and is likely dependent on how the microbes are transmitted across generations.

The symbiosis between plants and root‐colonizing arbuscular mycorrhizal (AM) fungi is one of the most ecologically important examples of interspecific cooperation in the world. AM fungi provide benefits to plants; in return plants allocate carbon resources to fungi, preferentially allocating more resources to higher‐quality fungi. However, preferential allocations from plants to symbionts may vary with environmental context, particularly when resource availability affects the relative value of symbiotic services. We ask how differences in atmospheric CO 2‐levels influence root colonization dynamics between AMF species that differ in their quality as symbiotic partners. We find that with increasing CO 2‐conditions and over multiple plant generations, the more beneficial fungal species is able to achieve a relatively higher abundance. This suggests that increasing atmospheric carbon supply enables plants to more effectively allocate carbon to higher‐quality mutualists, and over time helps reduce lower‐quality AM abundance. Our results illustrate how environmental context may affect the extent to which organisms structure interactions with their mutualistic partners and have potential implications for mutualism stability and persistence under global change.

Soil is likely the most complex ecosystem on earth. Despite the global importance and extraordinary diversity of soils, they have been notoriously challenging to study. We show how pioneering microfluidic techniques provide new ways of studying soil microbial ecology by allowing simulation and manipulation of chemical conditions and physical structures at the microscale in soil model habitats.

Arbuscular mycorrhizal fungi (AMF) can form complex networks in the soil that connect different host plants. Previous studies have focused on the effects of these networks on individual hosts and host communities. However, very little is known about how different host species affect the success of the fungal network itself. Given the potentially strong selection pressure against hosts that invest in a fungal network which benefits their competitors, we predict that the presence of multiple host species negatively affects the growth of the extraradical network. We designed an experiment using an in vitro culture approach to investigate the effect of different hosts (carrot, chichory and medicago) on the formation of a common mycelial network. In vitro root cultures, each inoculated with their own fungal network, were grown in a double split plate design with two host compartments and a common central compartment where fungal networks could form. We found that the size of fungal networks differs depending on the social environment of the host. When host species were propagated in a mixed species environment, the fungal abundance was significantly reduced compared to monoculture predictions. Our work demonstrates how host-to-host conflict can influence the abundance of the fungal partner.

It has been argued that cooperative behavior in the plant-mycorrhizal mutualism resembles trade in a market economy and can be understood using economic tools. Here, we assess the validity of this "biological market" analogy by investigating whether a market mechanism--that is, competition between partners over the price at which they provide goods--could be the outcome of natural selection. Then, we consider the conditions under which this market mechanism is sufficient to maintain mutualistic trade. We find that: (i) as in a market, individuals are favored to divide resources among trading partners in direct relation to the relative amount of resources received, termed linear proportional discrimination; (ii) mutualistic trade is more likely to be favored when individuals are able to interact with more partners of both species, and when there is a greater relative difference between the species in their ability to directly acquire different resources; (iii) if trade is favored, then either one or both species is favored to give up acquiring one resource directly, and vice versa. We then formulate testable predictions as to how environmental changes and coevolved responses of plants and mycorrhizal fungi will influence plant fitness (crop yields) in agricultural ecosystems.

Can egalitarian partnerships exist in nature? A new study demonstrates how protist hosts use and abuse their algal symbionts depending on their needs. While this relationship allows protists to survive in low nutrient conditions, it leaves little room for algal retaliation.

Symbiotic partnerships are a major source of evolutionary innovation. They have driven rapid diversification of organisms, allowed hosts to harness new forms of energy, and radically modified Earth's nutrient cycles. The application of next-generation sequencing and advanced microscopic techniques has revealed not only the ubiquity of symbiotic partnerships, but the extent to which partnerships can become physically, genomically, and metabolically integrated ( 1 ). When and why does this integration of once free-living organisms happen?

International audience; Biological market theory has been used successfully to explain cooperative behavior in many animal species. Microbes also engage in cooperative behaviors, both with hosts and other microbes, that can be described in economic terms. However, a market approach is not traditionally used to analyze these interactions. Here, we extend the biological market framework to ask whether this theory is of use to evolutionary biologists studying microbes. We consider six economic strategies used by microbes to optimize their success in markets. We argue that an economic market framework is a useful tool to generate specific and interesting predictions about microbial interactions, including the evolution of partner discrimination, hoarding strategies, specialized versus diversified mutualistic services, and the role of spatial structures, such as flocks and consortia. There is untapped potential for studying the evolutionary dynamics of microbial systems. Market theory can help structure this potential by characterizing strategic investment of microbes across a diversity of conditions.

Statistical models of ecosystem functioning based on species traits are valuable tools for predicting how nutrient cycling will respond to global change. However, species such as arbuscular mycorrhizal fungi (AMF) have evolved high intraspecific trait variation, making trait characterization and inclusion in functional trait models difficult. We present a five-part framework based on experimental designs from the phenotypic plasticity literature to quantify AMF intraspecific trait variation in a nutrient cycling context. Framework experiments involve exposing AMF replicates to different environmental conditions and recording trait values to quantify the (i) degree of variation, (ii) reversibility of traits, (iii) relationships among traits, (iv) adaptive nature of traits and (v) potential for trait variation to evolve. We include a phenotypic trajectory analysis of a simulated data set to illustrate relationships among traits. To focus future research, we provide a synthesis of AMF traits whose evolution is particularly relevant to nutrient cycling and environmental factors that induce variation in those traits. Synthesis. Characterizing the depth and range of arbuscular mycorrhizal fungal trait variation is essential for predicting responses to natural and anthropogenic environmental changes, as well as understanding past and future fungal trait evolutionary trajectories in the Tree of Life. Characterizing the depth and range of arbuscular mycorrhizal fungal trait variation is essential for predicting responses to natural and anthropogenic environmental changes, as well as understanding past and future fungal trait evolutionary trajectories in the Tree of Life. Here, we present an experimental framework for characterizing arbuscular mycorrhizal fungal trait variation. © 2014 British Ecological Society.

Agricultural management has profound effects on soil communities. Activities such as fertilizer inputs can modify the composition of arbuscular mycorrhizal fungi (AMF) communities, which form important symbioses with the roots of most crop plants. Intensive conventional agricultural management may select for less mutualistic AMF with reduced benefits to host plants compared to organic management, but these differences are poorly understood. AMF are generally evaluated based on their direct growth effects on plants. However, mycorrhizal colonization also may alter plant traits such as tissue nutrients, defensive chemistry, or floral traits, which mediate important plant-insect interactions like herbivory and pollination. To determine the effect of AMF from different farming practices on plant performance and traits that putatively mediate species interactions, we performed a greenhouse study by inoculating Cucumis sativus (cucumber, Cucurbitaceae) with AMF from conventional farms, organic farms, and a commercial AMF inoculum. We measured growth and a suite of plant traits hypothesized to be important predictors of herbivore resistance and pollinator attraction. Several leaf and root traits and flower production were significantly affected by AMF inoculum. Both conventional and organic AMF reduced leaf P content but increased Na content compared to control and commercial AMF. Leaf defenses were unaffected by AMF treatments, but conventional AMF increased root cucurbitacin C, the primary defensive chemical of C. sativus, compared to organic AMF. These effects may have important consequences for herbivore preference and population dynamics. AMF from both organic and conventional farms decreased flower production relative to commercial and control treatments, which may reduce pollinator attraction and plant reproduction. AMF from both farm types also reduced seed germination, but effects on plant growth were limited. Our results suggest that studies only considering AMF effects on growth may overlook changes in plant traits that have the potential to influence interactions, and hence yield, on farms. Given the effects of AMF on plant traits documented here, and the great importance of both herbivores and pollinators to wild and cultivated plants, we advocate for comprehensive assessments of mycorrhizal effects in complex community contexts, with the aim of incorporating multispecies interactions both above and below the soil surface. © 2013 by the Ecological Society of America.