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Plant growth responses following colonization with different isolates of a single species of an arbuscular mycorrhizal (AM) fungus can range from highly beneficial to detrimental, but the reasons for this high within-species diversity are currently unknown. To examine whether differences in growth and nutritional benefits are related to the phosphate (P) metabolism of the fungal symbiont, the effect of 31 different isolates from 10 AM fungal morphospecies on the P and nitrogen (N) nutrition of Medicago sativa and the P allocation among different P pools was examined. Based on differences in the mycorrhizal growth response, high, medium, and low performance isolates were distinguished. Plant growth benefit was positively correlated to the mycorrhizal effect on P and N nutrition. High performance isolates increased plant biomass by more than 170 % and contributed substantially to both P and N nutrition, whereas the effect of medium performance isolates particularly on the N nutrition of the host was significantly lower. Roots colonized by high performance isolates were characterized by relatively low tissue concentrations of inorganic P and short-chain polyphosphates and a high ratio between long- to short-chain polyphosphates. The high performance isolates belonged to different morphospecies and genera, indicating that the ability to contribute to P and N nutrition is widespread within the Glomeromycota and that differences in symbiotic performance and P metabolism are not specific for individual fungal morphospecies.

The 450-million-year-old symbiosis between the majority of land plants and arbuscular mycorrhizal fungi (AMF) is one of the most ancient, abundant, and ecologically important mutualisms on Earth. Yet, the evolutionary stability of mycorrhizal associations is still poorly understood, as it follows none of the constraints thought to stabilize cooperation in other well-known mutualisms. The capacity of both host and symbiont to simultaneously interact with several partners introduces a unique dilemma; detecting and punishing those exploiting the mutualism becomes increasingly difficult if these individuals can continue to access resources from alternative sources. Here, we explore four hypotheses to explain evolutionary cooperation in the arbuscular mycorrhizal symbiosis: (1) pseudo-vertical transmission and spatial structuring of plant and fungal populations leading to local adaptation of partners; (2) luxury resource exchange in which plants trade surplus carbon for excess fungal nutrients; (3) partner choice allowing partners to associate with better cooperators; and (4) host and symbiont sanctions which actively reward good partners and punish less cooperative ones. We propose that mycorrhizal cooperation is promoted by an exchange of surplus resources between partners and enforced through sanctions by one or both partners. These mechanisms may allow plant and fungal genotypes to discriminate against individuals employing exploitative strategies, promoting patterns of partner choice. Together these selection pressures provide a framework for understanding the stabilization of mycorrhizal cooperation over evolutionary time.

The arbuscular mycorrhizal (AM) symbiosis, formed between the majority of land plants and ubiquitous soil fungi of the phylum Glomeromycota, is responsible for massive nutrient transfer and global carbon sequestration. AM fungi take up nutrients from the soil and exchange them against photosynthetically fixed carbon (C) from the host. Recent studies have demonstrated that reciprocal reward strategies by plant and fungal partners guarantee a “fair trade” of phosphorus against C between partners [Kiers ET, et al. (2011) Science 333:880–882], but whether a similar reward mechanism also controls nitrogen (N) flux in the AM symbiosis is not known. Using mycorrhizal root organ cultures, we manipulated the C supply to the host and fungus and followed the uptake and transport of N sources in the AM symbiosis, the enzymatic activities of arginase and urease, and fungal gene expression in the extraradical and intraradical mycelium. We found that the C supply of the host plant triggers the uptake and transport of N in the symbiosis, and that the increase in N transport is orchestrated by changes in fungal gene expression. N transport in the symbiosis is stimulated only when the C is delivered by the host across the mycorrhizal interface, not when C is supplied directly to the fungal extraradical mycelium in the form of acetate. These findings support the importance of C flux from the root to the fungus as a key trigger for N uptake and transport and provide insight into the N transport regulation in the AM symbiosis.

We thank the Calleva Research Centre, Magdalen College, the European Research Council, the Natural Environment Research Council, and the Netherlands Organization for Scientific Research for funding. The evolution of life on earth has been driven by a small number of major evolutionary transitions. These have been characterized by individuals that could previously replicate independently, cooperating to form a new, more complex life form. For example, archaea and eubacteria formed eukaryotic cells, and cells formed multicellular organisms. But not all cooperative groups are on route to major transitions. How can we explain why major evolutionary transitions have or haven't taken place on different branches of the tree of life? We break down major transitions into two steps, the formation of a cooperative group and the transformation of that group into an integrated entity. We show how these steps require cooperation, division of labour, communication, mutual dependence and negligible within group conflict. We find that certain ecological conditions and the ways in which groups form have played recurrent roles in driving multiple transitions. In contrast, we find that other factors have played relatively minor roles at many key points, such as within-group kin discrimination and mechanisms to actively repress competition. More generally, by identifying the small number of factors that have driven major transitions, we provide a simpler and more unified description of how life on earth has evolved. Postprint

Partner selection in the mycorrhizal symbiosis is thought to be a key factor stabilising the mutualism. Both plant hosts and mycorrhizal fungi have been shown to preferentially allocate resources to higher quality partners. This can help maintain underground cooperation, although it is likely that different plant species vary in the spatial precision with which they can select partners. Partner selection in the mycorrhizal symbiosis is presumably context-dependent and can be mediated by factors like (relative) resource abundance and resource fluctuations, competition among mycorrhizas, arrival order and cultivation history. Such factors complicate our current understanding of the importance of partner selection and its effectiveness in stimulating mutualistic cooperation.

Trade-offs between individual fitness and the collective performance of crop and below-ground symbiont communities are common in agriculture. Plant competitiveness for light and soil resources is key to individual fitness, but higher investments in stems and roots by a plant community to compete for those resources ultimately reduce crop yields. Similarly, rhizobia and mycorrhizal fungi may increase their individual fitness by diverting resources to their own reproduction, even if they could have benefited collectively by providing their shared crop host with more nitrogen and phosphorus, respectively. Past selection for inclusive fitness (benefits to others, weighted by their relatedness) is unlikely to have favoured community performance over individual fitness. The limited evidence for kin recognition in plants and microbes changes this conclusion only slightly. We therefore argue that there is still ample opportunity for human-imposed selection to improve cooperation among crop plants and their symbionts so that they use limited resources more efficiently. This evolutionarily informed approach will require a better understanding of how interactions among crops, and interactions with their symbionts, affected their inclusive fitness in the past and what that implies for current interactions.

The arbuscular mycorrhizal (AM) symbiosis, which forms between plant hosts and ubiquitous soil fungi of the phylum Glomeromycota, plays a key role for the nutrient uptake of the majority of land plants, including many economically important crop species. AM fungi take up nutrients from the soil and exchange them for photosynthetically fixed carbon from the host. While our understanding of the exact mechanisms controlling carbon and nutrient exchange is still limited, we recently demonstrated that (i) carbon acts as an important trigger for fungal N uptake and transport, (ii) the fungus changes its strategy in response to an exogenous supply of carbon, and that (iii) both plants and fungi reciprocally reward resources to those partners providing more benefit. Here, we summarize recent research findings and discuss the implications of these results for fungal and plant control of resource exchange in the AM symbiosis.

Research on life history strategies of microbial symbionts is key to understanding the evolution of cooperation with hosts, but also their survival between hosts. Rhizobia are soil bacteria known for fixing nitrogen inside legume root nodules. Arbuscular mycorrhizal (AM) fungi are ubiquitous root symbionts that provide plants with nutrients and other benefits. Both kinds of symbionts employ strategies to reproduce during symbiosis using host resources; to repopulate the soil; to survive in the soil between hosts; and to find and infect new hosts. Here we focus on the fitness of the microbial symbionts and how interactions at each of these stages has shaped microbial life-history strategies. During symbiosis, microbial fitness could be increased by diverting more resources to individual reproduction, but that may trigger fitness-reducing host sanctions. To survive in the soil, symbionts employ sophisticated strategies, such as persister formation for rhizobia and reversal of spore germination by mycorrhizae. Interactions among symbionts, from rhizobial quorum sensing to fusion of genetically distinct fungal hyphae, increase adaptive plasticity. The evolutionary implications of these interactions and of microbial strategies to repopulate and survive in the soil are largely unexplored.

Ectomycorrhizal symbiosis is omnipresent in boreal forests, where it is assumed to benefit plant growth. However, experiments show inconsistent benefits for plants and volatility of individual partnerships, which calls for a re-evaluation of the presumed role of this symbiosis. We reconcile these inconsistencies by developing a model that demonstrates how mycorrhizal networking and market mechanisms shape the strategies of individual plants and fungi to promote symbiotic stability at the ecosystem level. The model predicts that plants switch abruptly from a mixed strategy with both mycorrhizal and nonmycorrhizal roots to a purely mycorrhizal strategy as soil nitrogen availability declines, in agreement with the frequency distribution of ectomycorrhizal colonization intensity across a wide-ranging data set. In line with observations in field-scale isotope labeling experiments, the model explains why ectomycorrhizal symbiosis does not alleviate plant nitrogen limitation. Instead, market mechanisms may generate self-stabilization of the mycorrhizal strategy via nitrogen depletion feedback, even if plant growth is ultimately reduced. We suggest that this feedback mechanism maintains the strong nitrogen limitation ubiquitous in boreal forests. The mechanism may also have the capacity to eliminate or even reverse the expected positive effect of rising CO2 on tree growth in strongly nitrogen-limited boreal forests.

Common mycorrhizal networks (CMNs) of arbuscular mycorrhizal (AM) fungi in the soil simultaneously provide multiple host plants with nutrients, but the mechanisms by which the nutrient transport to individual host plants within one CMN is controlled are unknown. Using radioactive and stable isotopes, we followed the transport of phosphorus (P) and nitrogen (N) in the CMNs of two fungal species to plants that differed in their carbon (C) source strength, and correlated the transport to the expression of mycorrhiza-inducible plant P (MtPt4) and ammonium (1723.m00046) transporters in mycorrhizal roots. AM fungi discriminated between host plants that shared a CMN and preferentially allocated nutrients to high-quality (nonshaded) hosts. However, the fungus also supplied low-quality (shaded) hosts with nutrients and maintained a high colonization rate in these plants. Fungal P transport was correlated to the expression of MtPt4. The expression of the putative ammonium transporter 1723.m00046 was dependent on the fungal nutrient supply and was induced when the CMN had access to N. Biological market theory has emerged as a tool with which the strategic investment of competing partners in trading networks can be studied. Our work demonstrates how fungal partners are able to retain bargaining power, despite being obligately dependent on their hosts. © 2014 New Phytologist Trust.

Symbiotic associations occur in every habitat on earth, but we know very little about their evolutionary histories. Current models of trait evolution cannot adequately reconstruct the deep history of symbiotic innovation, because they assume homogenous evolutionary processes across millions of years. Here we use a recently developed, heterogeneous and quantitative phylogenetic framework to study the origin of the symbiosis between angiosperms and nitrogen-fixing (N2) bacterial symbionts housed in nodules. We compile the largest database of global nodulating plant species and reconstruct the symbiosis’ evolution. We identify a single, cryptic evolutionary innovation driving symbiotic N2-fixation evolution, followed by multiple gains and losses of the symbiosis, and the subsequent emergence of ‘stable fixers’ (clades extremely unlikely to lose the symbiosis). Originating over 100 MYA, this innovation suggests deep homology in symbiotic N2-fixation. Identifying cryptic innovations on the tree of life is key to understanding the evolution of complex traits, including symbiotic partnerships., Symbiotic associations are widespread, yet their evolutionary histories remain poorly understood. Here, Werner et. al. show a single evolutionary innovation driving symbiotic nitrogen fixation, followed by multiple gains and losses of the symbiosis and the emergence of groups with stable nitrogen fixers.

Mutualisms are cooperative interactions between members of different species, often involving the trade of resources. Here, we suggest that otherwise-cooperative mutualists might be able to gain a benefit from actively restricting their partners' ability to obtain resources directly, hampering the ability of the restricted partner to survive and/or reproduce without the help of the restricting mutualist. We show that (i) restriction can be favoured when it makes the resources of the restricting individual more valuable to their partner, and thus allows them to receive more favourable terms of trade; (ii) restriction maintains cooperation in conditions where cooperative behaviour would otherwise collapse; and (iii) restriction can lead to either an increase or decrease in a restricted individual's fitness. We discuss the applicability of this scenario to mutualisms such as those between plants and mycorrhizal fungi. These results identify a novel conflict in mutualisms as well as several public goods dilemmas, but also demonstrate how conflict can help maintain cooperation., Mutualistic interactions involve trading benefits between cooperative species. Here, the authors show that restricting the resource acquisition of a mutualistic partner can increase mutualism by promoting resource trade, which suggests that conflict may lead to increased cooperation.

A key objective in ecology is to understand how cooperative strategies evolve and are maintained in species networks. Here, we focus on the tri-trophic relationship between arbuscular mycorrhizal (AM) fungi, host plants, and fungivores to ask if host plants are able to protect their mutualistic mycorrhizal partners from being grazed. Specifically, we test whether secondary metabolites are transferred from hosts to fungal partners to increase their defense against fungivores. We grew Plantago lanceolata hosts with and without mycorrhizal inoculum, and in the presence or absence of fungivorous springtails. We then measured fungivore effects on host biomass and mycorrhizal abundance (using quantitative PCR) in roots and soil. We used high-performance liquid chromatography to measure host metabolites in roots, shoots, and hyphae, focusing on catalpol, aucubin, and verbascoside. Our most striking result was that the metabolite catalpol was consistently found in AM fungal hyphae in host plants exposed to fungivores. When fungivores were absent, catalpol was undetectable in hyphae. Our results highlight the potential for plant-mediated protection of the mycorrhizal hyphal network. © 2013 by the Ecological Society of America.

The root microbiome is composed of an incredibly diverse microbial community that provides services to the plant. A major question in rhizosphere research is how species in root microbiome communities interact with each other and their host. In the nutrient mutualism between host plants and arbuscular mycorrhizal fungi (AMF), competition often leads to certain species dominating host colonization, with the outcome being dependent on environmental conditions. In the past, it has been difficult to quantify the abundance of closely related species and track competitive interactions in different regions of the rhizosphere, specifically within and outside the host. Here, we used an artificial root system (in vitro root organ cultures) to investigate intraradical (within the root) and extraradical (outside the root) competitive interactions between two closely related AMF species, Rhizophagus irregularis and Glomus aggregatum, under different phosphorus availabilities. We found that competitive interactions between AMF species reduced overall fungal abundance. R. irregularis was consistently the most abundant symbiont for both intraradical and extraradical colonization. Competition was the most intense for resources within the host, where both species negatively affected each other's abundance. We found the investment ratio (i.e. extraradical abundance/intraradical abundance) shifted for both species depending on whether competitors were present or not. Phosphorus availability did not change the outcome of these interactions. Our results suggest that studies on competitive interactions should focus on intraradical colonization dynamics and consider how changes in investment ratio are mediated by fungal species interactions. © 2013 John Wiley & Sons Ltd.

Given that arbuscular mycorrhizal (AM) fungi are not consistently beneficial to their host plants, it is difficult to explain the evolutionary persistence of this relationship. We tested the hypothesis that increasing either fungal or host biodiversity allows an AM fungus to persist on a host where it shows little benefit. We found that growing such a fungus (an isolate of Glomus custos associating with Plantago laceolata) in combination with certain fungi improved its success as measured by mtLSU DNA abundance. Increasing plant species richness facilitated the spread of this fungus as measured by spore density and fungal colonization; the role of host species richness was not as clear when looking at measures of root abundance. These results indicate that diversity in the AM symbiosis, both plant and fungal, can promote the persistence of low-quality fungi. By existing within a complex mycelial network fungal strains that show little growth benefit to their hosts have a better chance of persisting on that same host. This has the potential to promote selection for heterogeneous AM fungal communities on a small spatial scale.

Loss of traits can dramatically alter the fate of species. Evidence is rapidly accumulating that the prevalence of trait loss is grossly underestimated. New findings demonstrate that traits can be lost without affecting the external phenotype, provided the lost function is compensated for by species interactions. This is important because trait loss can tighten the ecological relationship between partners, affecting the maintenance of species interactions. Here, we develop a new perspective on so-called compensated trait loss' and how this type of trait loss may affect the evolutionary dynamics between interacting organisms. We argue that: (1) the frequency of compensated trait loss is currently underestimated because it can go unnoticed as long as ecological interactions are maintained; (2) by analysing known cases of trait loss, specific factors promoting compensated trait loss can be identified and (3) genomic sequencing is a key way forwards in detecting compensated trait loss. We present a comprehensive literature survey showing that compensated trait loss is taxonomically widespread, can involve essential traits, and often occurs as replicated evolutionary events. Despite its hidden nature, compensated trait loss is important in directing evolutionary dynamics of ecological relationships and has the potential to change facultative ecological interactions into obligatory ones. © 2012 Blackwell Publishing Ltd/CNRS.

Explaining mutualistic cooperation between species remains a major challenge for evolutionary biology. Why cooperate if defection potentially reaps greater benefits? It is commonly assumed that spatial structure (limited dispersal) aligns the interests of mutualistic partners. But does spatial structure consistently promote cooperation? Here, we formally model the role of spatial structure in maintaining mutualism. We show theoretically that spatial structure can actually disfavor cooperation by limiting the suite of potential partners. The effect of spatial structuring depends on the scale (fine or coarse level) at which hosts reward their partners. We then test our predictions by using molecular methods to track the abundance of competing, closely related, cooperative, and less cooperative arbuscular mycorrhizal (AM) fungal symbionts on host roots over multiple generations. We find that when spatial structure is reduced by mixing soil, the relative success of the more cooperative AM fungal species increases. This challenges previous suggestions that high spatial structuring is critical for stabilizing cooperation in the mycorrhizal mutualism. More generally, our results show, both theoretically and empirically, that contrary to expectations, spatial structuring can select against cooperation. © 2012 by The University of Chicago.

International audience; Plants and their arbuscular mycorrhizal fungal symbionts interact in complex underground networks involving multiple partners. This increases the potential for exploitation and defection by individuals, raising the question of how partners maintain a fair, two-way transfer of resources. We manipulated cooperation in plants and fungal partners to show that plants can detect, discriminate, and reward the best fungal partners with more carbohydrates. In turn, their fungal partners enforce cooperation by increasing nutrient transfer only to those roots providing more carbohydrates. On the basis of these observations we conclude that, unlike many other mutualisms, the symbiont cannot be "enslaved." Rather, the mutualism is evolutionarily stable because control is bidirectional, and partners offering the best rate of exchange are rewarded.

Explaining mutualistic cooperation between species remains one of the greatest problems for evolutionary biology. Why do symbionts provide costly services to a host, indirectly benefiting competitors sharing the same individual host? Host monitoring of symbiont performance and the imposition of sanctions on 'cheats' could stabilize mutualism. Here we show that soybeans penalize rhizobia that fail to fix N(2) inside their root nodules. We prevented a normally mutualistic rhizobium strain from cooperating (fixing N(2)) by replacing air with an N(2)-free atmosphere (Ar:O(2)). A series of experiments at three spatial scales (whole plants, half root systems and individual nodules) demonstrated that forcing non-cooperation (analogous to cheating) decreased the reproductive success of rhizobia by about 50%. Non-invasive monitoring implicated decreased O(2) supply as a possible mechanism for sanctions against cheating rhizobia. More generally, such sanctions by one or both partners may be important in stabilizing a wide range of mutualistic symbioses.

The evolutionary stability of mutualisms is enhanced when partners possess mechanisms to prevent overexploitation by one another. In obligate pollination-seed consumption mutualisms, selective abortion of flowers containing excessive eggs represents one such mechanism, but empirical tests have long been limited to the yucca-yucca moth mutualism. We present evidence for selective abortion in the recently discovered mutualism between Glochidion trees and Epicephala moths. In Glochidion acuminatum, proportion of aborted flowers progressively increased both with higher egg load and increased ovule damage. Selective abortion resulted in a 16% seed production increase compared with expectations under random abortion, and moths suffered fitness losses as high as 62% when ovipositing into pre-infested flowers. Moth eggs were laid singly more often than expected under random oviposition, thus avoiding potential disadvantages from multiple infestations. As new pollination mutualisms are being discovered, selective abortion mechanisms may prove to be more widespread than previously thought. © 2010 Blackwell Publishing Ltd/CNRS.

Summary 1. Root symbionts (rhizobia and arbuscular mycorrhizae) are often assumed to increase agricultural productivity consistently. However, rhizobial and mycorrhizal strains vary in effectiveness, resulting in symbiotic associations that range from parasitic to mutualistic. 2. The extent to which different farming practices mediate evolutionary changes along this continuum of symbiont effectiveness is rarely discussed. However, evolutionary theory suggests that (i) fertilizer use will favour parasitism unless host-plants impose sanctions against less-effective mutualists; (ii) tillage will have contrasting effects because it decreases within-plant symbiont relatedness but also decreases the risk that mutualism will benefit future competitors; (iii) crop rotation can act as a selective agent against dominating symbiont genotypes; and (iv) rhizobial inoculation adds beneficial strains to the soil but may increase the frequency of mixed nodules that allow parasitic strains to escape host sanctions. 3. However, the existing empirical data are inadequate to test our predictions thoroughly. Changes in species composition have been documented as a result of management practices, but evolutionary changes in symbiont effectiveness are difficult to detect. Therefore, a major aim of this study was to stimulate research that will assesses directly changes in symbiotic effectiveness as a function of management practices.

Why do mutualists perform costly behaviours that benefit individuals of a different species? One of the factors that may stabilize mutualistic interactions is when individuals preferentially reward more mutualistic (beneficial) behaviour and/or punish less mutualistic (more parasitic) behaviour. We develop a model that shows how such sanctions provide a fitness benefit to the individuals that carry them out. Although this approach could be applied to a number of symbioses, we focus on how it could be applied to the legume-rhizobia interaction. Specifically, we demonstrate how plants can be selected to supply preferentially more resources to (or be less likely to senesce) nodules that are fixing more N-2 (termed plant sanctions). We have previously argued that appreciable levels of N-2 fixation by rhizobia are only likely to be selected for in response to plant sanctions. Therefore, by showing that plant sanctions can also be favoured by natural selection, we are able to provide an explanation for the stability of the plant-legume mutualism, Why do mutualists perform costly behaviours that benefit individuals of a different species? One of the factors that may stabilize mutualistic interactions is when individuals preferentially reward more mutualistic (beneficial) behaviour and/or punish less mutualistic (more parasitic) behaviour. We develop a model that shows how such sanctions provide a fitness benefit to the individuals that carry them out. Although this approach could be applied to a number of symbioses, we focus on how it could be applied to the legume-rhizobia interaction. Specifically, we demonstrate how plants can be selected to supply preferentially more resources to (or be less likely to senesce) nodules that are fixing more N2 (termed plant sanctions). We have previously argued that appreciable levels of N2 fixation by rhizobia are only likely to be selected for in response to plant sanctions. Therefore, by showing that plant sanctions can also be favoured by natural selection, we are able to provide an explanation for the stability of the plant-legume mutualism.

Understanding how mutualistic interactions are stabilized in the presence of cheaters is a major question in evolutionary biology. The legume–rhizobia mutualism has become a model system for studying how plants control cheating partners. However, the generality and evolutionary origins of these control mechanisms are intensely debated. In this Opinion article, we argue that a novel system – the Parasponia–rhizobia mutualism – will significantly advance research in mutualism stability. Parasponia is the only non-legume lineage to have evolved a rhizobial symbiosis, which provides an evolutionary replicate to test how rhizobial exploitation is controlled. Evidence also suggests that this symbiosis is young. This allows studies at an earlier evolutionary stage in mutualisms, so the origin of control mechanisms can be better understood.

The symbiotic nitrogen-fixing soil bacterium Sinorhizobium meliloti carries a large number of toxin-antitoxin (TA) modules both on the chromosome and megaplasmids. One of them, the vapBC-5 module that belongs to the type II systems was characterized here. It encodes an active toxin vapC-5, and was shown to be controlled negatively by the complex of its own proteins. Different mutants of the vapBC-5 genes exhibited diverse effects on symbiotic efficiency during interaction with the host plant Medicago sativa. The absence of the entire vapBC-5 region had no influence on nodule formation and nitrogen fixation properties. The strain carrying an insertion in the antitoxin gene showed a reduced nitrogen fixation capacity resulting in a lower plant yield. In contrast, when the toxin gene was mutated, the strain developed more efficient symbiosis with the host plant. The nitrogen fixing root nodules had a delayed senescent phenotype and contained elevated level of plant-derived molecules characteristic of later steps of nodule development. The longer bacteroid viability and abundance of active nitrogen fixing zone resulted in increased production of plant material. These data indicate that modification of the toxin/antitoxin production may influence bacteroid metabolism and may have an impact on the adaptation to changing environmental conditions.

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.

Ecology Letters (2010) 13: 1459-1474 ABSTRACT: There is growing concern that rapid environmental degradation threatens mutualistic interactions. Because mutualisms can bind species to a common fate, mutualism breakdown has the potential to expand and accelerate effects of global change on biodiversity loss and ecosystem disruption. The current focus on the ecological dynamics of mutualism under global change has skirted fundamental evolutionary issues. Here, we develop an evolutionary perspective on mutualism breakdown to complement the ecological perspective, by focusing on three processes: (1) shifts from mutualism to antagonism, (2) switches to novel partners and (3) mutualism abandonment. We then identify the evolutionary factors that may make particular classes of mutualisms especially susceptible or resistant to breakdown and discuss how communities harbouring mutualisms may be affected by these evolutionary responses. We propose a template for evolutionary research on mutualism resilience and identify conservation approaches that may help conserve targeted mutualisms in the face of environmental change.

Enforcement mechanisms are thought to be important in maintaining mutualistic cooperation between species. A clear example of an enforcement mechanism is how legumes impose sanctions on rhizobial symbionts that fail to provide sufficient fixed N 2 . However, with domestication and breeding in high-soil-N environments, humans may have altered these natural legume defences and reduced the agricultural benefits of the symbiosis. Using six genotypes of soya beans, representing 60 years of breeding, we show that, as a group, older cultivars were better able to maintain fitness than newer cultivars (seed production) when infected with a mixture of effective and ineffective rhizobial strains. Additionally, we found small differences among cultivars in the ratio of effective : ineffective rhizobia released from their nodules, an indicator of future rhizobial strain fitness. When infected by symbionts varying in quality, legume defences against poor-quality partners have apparently worsened under decades of artificial selection.

Multiple strains per plant and root-to-root (not seed-borne) transmission should favor rhizobia that invest in their own reproduction, rather than symbiotic N2 fixation, as analogous factors may favor pathogen virulence. But legumes can select for greater mutualism, controlling nodule O2 supply and reducing reproduction of rhizobia that fix less N2.

Strains of rhizobia within a single species can have three different genetically determined strategies. Mutualistic rhizobia provide their legume hosts with nitrogen. Parasitic rhizobia infect legumes, but fix little or no nitrogen. Nonsymbiotic strains are unable to infect legumes at all. Why have rhizobium strains with one of these three strategies not displaced the others? A symbiotic (mutualistic or parasitic) rhizobium that succeeds in founding a nodule may produce many millions of descendants. The chances of success can be so low, however, that nonsymbiotic rhizobia can have greater reproductive success. Legume sanctions against nodules that fix little or no nitrogen favor more mutualistic strains, but parasitic strains that use plant resources only for their own reproduction may do well when they share nodules with mutualistic strains.