Mycorrhizal fungi influence plant growth, local biodiversity and ecosystem function. Effects of the symbiosis on plants span the continuum from mutualism to parasitism. We sought to understand this variation in symbiotic function using meta-analysis with information theory-based model selection to assess the relative importance of factors in five categories: (1) identity of the host plant and its functional characteristics, (2) identity and type of mycorrhizal fungi (arbuscular mycorrhizal vs. ectomycorrhizal), (3) soil fertility, (4) biotic complexity of the soil and (5) experimental location (laboratory vs. field). Across most subsets of the data, host plant functional group and N-fertilization were surprisingly much more important in predicting plant responses to mycorrhizal inoculation (Ôplant responseÕ) than other factors. Non-N-fixing forbs and woody plants and C 4 grasses responded more positively to mycorrhizal inoculation than plants with N-fixing bacterial symbionts and C 3 grasses. In laboratory studies of the arbuscular mycorrhizal symbiosis, plant response was more positive when the soil community was more complex. Univariate analyses supported the hypothesis that plant response is most positive when plants are P-limited rather than N-limited. These results emphasize that mycorrhizal function depends on both abiotic and biotic context, and have implications for plant community theory and restoration ecology.
We evaluate the empirical and theoretical support for the hypothesis that a large proportion of native species richness is required to maximize ecosystem stability and sustain function. This assessment is important for conservation strategies because sustenance of ecosystem functions has been used as an argument for the conservation of species. If ecosystem functions are sustained at relatively low species richness, then arguing for the conservation of ecosystem function, no matter how important in its own right, does not strongly argue for the conservation of species. Additionally, for this to be a strong conservation argument the link between species diversity and ecosystem functions of value to the human community must be clear. We review the empirical literature to quantify the support for two hypotheses: (1) species richness is positively correlated with ecosystem function, and (2) ecosystem functions do not saturate at low species richness relative to the observed or experimental diversity. Few empirical studies demonstrate improved function at high levels of species richness. Second, we analyze recent theoretical models in order to estimate the level of species richness required to maintain ecosystem function. Again we find that, within a single trophic level, most mathematical models predict saturation of ecosystem function at a low proportion of local species richness. We also analyze a theoretical model linking species number to ecosystem stability. This model predicts that species richness beyond the first few species does not typically increase ecosystem stability. One reason that high species richness may not contribute significantly to function or stability is that most communities are characterized by strong dominance such that a few species provide the vast majority of the community biomass. Rapid turnover of species may rescue the concept that diversity leads to maximum function and stability. The role of turnover in ecosystem function and stability has not been investigated. Despite the recent rush to embrace the linkage between biodiversity and ecosystem function, we find little support for the hypothesis that there is a strong dependence of ecosystem function on the full complement of diversity within sites. Given this observation, the conservation community should take a cautious view of endorsing this linkage as a model to promote conservation goals.
Adaptive divergence among populations can result in local adaptation, whereby genotypes in native environments exhibit greater fitness than genotypes in novel environments. A body of theory has developed that predicts how different species traits, such as rates of gene flow and generation times, influence local adaptation in coevolutionary species interactions. We used a meta-analysis of local-adaptation studies across a broad range of host-parasite interactions to evaluate predictions about the effect of species traits on local adaptation. We also evaluated how experimental design influences the outcome of local adaptation experiments. In reciprocally designed experiments, the relative gene flow rate of hosts versus parasites was the strongest predictor of local adaptation, with significant parasite local adaptation only in the studies in which parasites had greater gene flow rates than their hosts. When nonreciprocal studies were included in analyses, species traits did not explain significant variation in local adaptation, although the overall level of local adaptation observed was lower in the nonreciprocal than in the reciprocal studies. This formal meta-analysis across a diversity of host-parasite systems lends insight into the role of both biology (species traits) and biologists (experimental design) in detecting local adaptation in coevolving species interactions.
Advances in ecology during the past decade have led to a much more detailed understanding of the potential negative consequences of species' introductions. Moreover, recent studies of mycorrhizal symbionts have led to an increased knowledge of the potential utility of fungal inoculations in agricultural, horticultural and ecological management. The intentional movement of mycorrhizal fungal species is growing, but the concomitant potential for negative ecological consequences of invasions by mycorrhizal fungi is poorly understood. We assess the degree to which introductions of mycorrhizal fungi may lead to unintended negative, and potentially costly, consequences. Our purpose is to make recommendations regarding appropriate management guidelines and highlight top priority research needs. Given the difficulty in discerning invasive species problems associated with mycorrhizal inoculations, we recommend the following. First, careful assessment documenting the need for inoculation, and the likelihood of success, should be conducted prior to inoculation because inoculations are not universally beneficial. Second, invasive species problems are costly and often impossible to control by the time they are recognized. We recommend using local inoculum sources whenever possible. Third, non-sterile cultures of inoculum can result in the movement of saprobes and pathogens as well as mutualists. We recommend using material that has been produced through sterile culture when local inoculum is not available. Finally, life-history characteristics of inoculated fungi may provide general guidelines relative to the likelihood of establishment and spread. We recommend that, when using non-local fungi, managers choose fungal taxa that carry life-history traits that may minimize the likelihood of deleterious invasive species problems. Additional research is needed on the potential of mycorrhizal fungi to spread to non-target areas and cause ecological damage.
Cheating is a focal concept in the study of mutualism, with the majority of researchers considering cheating to be both prevalent and highly damaging. However, current definitions of cheating do not reliably capture the evolutionary threat that has been a central motivation for the study of cheating. We describe the development of the cheating concept and distill a relative-fitness-based definition of cheating that encapsulates the evolutionary threat posed by cheating, i.e. that cheaters will spread and erode the benefits of mutualism. We then describe experiments required to conclude that cheating is occurring and to quantify fitness conflict more generally. Next, we discuss how our definition and methods can generate comparability and integration of theory and experiments, which are currently divided by their respective prioritisations of fitness consequences and traits. To evaluate the current empirical evidence for cheating, we review the literature on several of the best-studied mutualisms. We find that although there are numerous observations of low-quality partners, there is currently very little support from fitness data that any of these meet our criteria to be considered cheaters. Finally, we highlight future directions for research on conflict in mutualisms, including novel research avenues opened by a relative-fitness-based definition of cheating.
Most ecological theory suggests that the conditions that would give rise to the evolution of mutualisms are rare. In contrast, empirical evidence suggests that mutualisms are common. Thus, there appears to be a need for additional theory to describe conditions under which mutualisms may evolve. Furthermore, there is a need for theory to predict the conditions under which we expect interactions to remain mutualistic once established. We adopt a biological market approach to present a model for the evolution of resource exchange mutualisms, using the relationship between plants and mycorrhizal fungi as an example. We apply the economic theory of relative advantage to investigate the conditions under which species ought to specialize and trade. A simple economic analogy demonstrates that, in a two-resource model, a species that is relatively efficient at acquiring one resource would benefit from specialization on acquisition of that resource accompanied by trade for the other resource. The theory of relative advantage extends this prediction to show that specialization and trade confer an advantage even for species that are relatively poor resource competitors for both resources. Under the assumptions of our model, we show that two species ought to specialize in the acquisition of one resource and trade for a second resource as long as each species perceives different relative acquisition costs for the two resources. We also describe the conditions under which changing resource availabilities will benefit, or harm, both partners in a mutualism. We predict conditions conducive to mutualisms to occur when the costs of resource exchange are low, the opportunity to ensure fair trade is high, or the cost of tolerating cheaters is low. Market models such as ours may help to explain the conditionality often observed in mutualisms.
BackgroundLocal adaptation, the differential success of genotypes in their native versus foreign environment, arises from various evolutionary processes, but the importance of concurrent abiotic and biotic factors as drivers of local adaptation has only recently been investigated. Local adaptation to biotic interactions may be particularly important for plants, as they associate with microbial symbionts that can significantly affect their fitness and may enable rapid evolution. The arbuscular mycorrhizal (AM) symbiosis is ideal for investigations of local adaptation because it is globally widespread among most plant taxa and can significantly affect plant growth and fitness. Using meta-analysis on 1170 studies (from 139 papers), we investigated the potential for local adaptation to shape plant growth responses to arbuscular mycorrhizal inoculation.ResultsThe magnitude and direction for mean effect size of mycorrhizal inoculation on host biomass depended on the geographic origin of the soil and symbiotic partners. Sympatric combinations of plants, AM fungi, and soil yielded large increases in host biomass compared to when all three components were allopatric. The origin of either the fungi or the plant relative to the soil was important for explaining the effect of AM inoculation on plant biomass. If plant and soil were sympatric but allopatric to the fungus, the positive effect of AM inoculation was much greater than when all three components were allopatric, suggesting potential local adaptation of the plant to the soil; however, if fungus and soil were sympatric (but allopatric to the plant) the effect of AM inoculation was indistinct from that of any allopatric combinations, indicating maladaptation of the fungus to the soil.ConclusionsThis study underscores the potential to detect local adaptation for mycorrhizal relationships across a broad swath of the literature. Geographic origin of plants relative to the origin of AM fungal communities and soil is important for describing the effect of mycorrhizal inoculation on plant biomass, suggesting that local adaptation represents a powerful factor for the establishment of novel combinations of fungi, plants, and soils. These results highlight the need for subsequent investigations of local adaptation in the mycorrhizal symbiosis and emphasize the importance of routinely considering the origin of plant, soil, and fungal components.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0698-9) contains supplementary material, which is available to authorized users.
Along with increases in empirical information about interspecific mutualisms have come both new and refined questions about them. These questions have spurred diversification in the theoretical approaches being applied to interspecific mutualism. This theoretical literature has become large and potentially confusing, but as a whole is very relevant to answering the current important questions about mutualism. We first present three important questions about mutualisms raised by recent empirical results. (1) What factors control whether interactions become mutualistic or parasitic? (2) Why are highly specialized mutualisms rare and what are the implications of this observation? (3) What is the impact of trophic complexity on the functioning of mutualisms? Second, we highlight results of recent models of mutualism that address at least one of the three questions, and point to potentially rewarding avenues of exploration for these modeling approaches. This review should be useful to both empiricists and theorists as a roadmap to both the variety of theory currently being applied to mutualisms and to results that are in need of additional theoretical and empirical exploration.
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