Persistence Of Mutualisms Research Articles

Coevolution and dependency influence resistance of mutualists to exploitation

A long-standing problem in the study of mutualism is to understand the effects of non-mutualistic community members that exploit the benefits of mutualism without offering commodities in exchange (i.e., ‘exploiters’). Mutualisms are continually challenged by exploiters and their persistence may depend on the costliness of exploitation or on adaptations that allow mutualists to avoid the negative effects of exploiters. Coevolution could lead to changes in mutualists and exploiters that allow mutualisms to persist. Although coevolution is considered essential for mutualism persistence and resistance to disturbance, we have yet to obtain direct experimental evidence of the role of coevolution in resistance to exploitation. Additionally, resistance to exploitation via coevolutionary processes might vary with the degree of dependency between mutualistic partners, as facultative mutualisms are thought to be under weaker coevolutionary selection than obligate mutualisms. Here, we conducted an experimental evolution study using a synthetic yeast mutualism to test how coevolution in facultative and obligate mutualisms affects their resistance to exploitation. We found that naïve facultative mutualisms were more likely to breakdown under exploitation than naïve obligate mutualisms. After 15 weeks of coevolution, both facultative and obligate evolved mutualists were more likely to survive exploitation than naïve mutualists when we reassembled mutualist communities. Additionally, coevolved exploiters were more likely to survive with mutualists, whereas naïve exploiters frequently went extinct. These results suggest that coevolution between mutualists and exploiters can lead to mutualism persistence, potentially explaining why exploitation is ubiquitous but rarely associated with mutualism breakdown.

Eco-evolutionary Logic of Mutualisms

Mutualistic interactions among members of different species are common, seemingly stable, and thus apparently enduring. This is at odds with standard mathematical models based solely on between-species interactions, which show mutualisms to be inherently unstable. Models incorporating parameters for punishment and reward strategies demonstrate that the range of conditions over which stability is observed can be extended; however, the role of community-level dynamics impacted by within-species interactions remains relatively unexplored. Here we develop a general and readily applicable approach for analysing a broad range of mutualisms. By incorporating within-species interactions, we show that mutualisms can be stably maintained across diverse environmental conditions without introducing changes to between-species interaction parameters. Further, a balance of within- and between-species interactions is sufficient to allow the persistence of mutualisms encountering ecological perturbations. Our simple and robust framework resonates with emerging empirical data highlighting the role of community-level interactions and population dynamics in maintaining mutualisms.

Spatial Structure within Root Systems Moderates Stability of Arbuscular Mycorrhizal Mutualism and Plant-Soil Feedbacks.

AbstractThe persistence of mutualisms is paradoxical, as there are fitness incentives for exploitation. This is particularly true for plant-microbe mutualisms like arbuscular mycorrhizae (AM), which are promiscuously horizontally transmitted. Preferential allocation by hosts to the best mutualist can stabilize horizontal mutualisms; however, preferential allocation is imperfect, with its fidelity likely depending on the spatial structure of symbionts in plant roots. In this study we tested AM mutualisms' dependence on two dimensions of spatial structure-the initial spatial association of fungi and the ease of fungal dispersal-through three complementary experiments. We found that fitness of the beneficial AM fungus increased when fungi were initially separate, while initial spatial mixing benefited the fitness of the nonbeneficial fungus. These effects were strongest when dispersal was limited and hosts could discriminate. Additionally, we found that changes in AM fungal proportional abundance induced by spatial structure in roots of a preferentially allocating host produced positive feedbacks on plant growth, showing that interactions between spatial structure and host choice can determine the direction of plant-soil feedbacks. Our results suggest that symbiont spatial structure within plant roots may act as an important modifier of plant preferential allocation and the dynamics of mycorrhizal mutualisms, with potentially cascading effects on plant-plant interactions.

For the road: calibrated maternal investment in light of extracellular symbiont transmission.

Faithful transmission of beneficial symbionts is critical for the persistence of mutualisms. Many insect groups rely on extracellular routes that require microbial symbionts to survive outside the host during transfer. However, given a prolonged aposymbiotic phase in offspring, how do mothers mitigate the risk of symbiont loss due to unsuccessful transmission? Here, we investigated symbiont regulation and reacquisition during extracellular transfer in the tortoise beetle, Chelymorpha alternans (Coleoptera: Cassidinae). Like many cassidines, C. alternans relies on egg caplets to vertically propagate its obligate symbiont Candidatus Stammera capleta. On average, each caplet is supplied with 12 symbiont-bearing spheres where Stammera is embedded. We observe limited deviation (±2.3) in the number of spheres allocated to each caplet, indicating strict maternal control over symbiont supply. Larvae acquire Stammera 1 day prior to eclosion but are unable to do so after hatching, suggesting that a specific developmental window governs symbiont uptake. Experimentally manipulating the number of spheres available to each egg revealed that a single sphere is sufficient to ensure successful colonization by Stammera relative to the 12 typically packaged within a caplet. Collectively, our findings shed light on a tightly regulated symbiont transmission cycle optimized to ensure extracellular transfer.

An evolutionary perspective on increasing net benefits to crops from symbiotic microbes.

Plant-imposed, fitness-reducing sanctions against less-beneficial symbionts have been documented for rhizobia, mycorrhizal fungi, and fig wasps. Although most of our examples are for rhizobia, we argue that the evolutionary persistence of mutualism in any symbiosis would require such sanctions, if there are multiple symbiont genotypes per host plant. We therefore discuss methods that could be used to develop and assess crops with stricter sanctions. These include methods to screen strains for greater mutualism as resources to identify crop genotypes that impose stronger selection for mutualism. Single-strain experiments that measure costs as well as benefits have shown that diversion of resources by rhizobia can reduce nitrogen-fixation efficiency (N per C) and that some legumes can increase this efficiency by manipulating their symbionts. Plants in the field always host multiple strains with possible synergistic interactions, so benefits from different strains might best be compared by regressing plant growth or yield on each strain's abundance in a mixture. However, results from this approach have not yet been published. To measure legacy effects of stronger sanctions on future crops, single-genotype test crops could be planted in a field that recently had replicated plots with different genotypes of the sanction-imposing crop. Enhancing agricultural benefits from symbiosis may require accepting tradeoffs that constrained past natural selection, including tradeoffs between current and future benefits.

Native tube-building polychaete prefers to anchor non-native alga over other macrophytes.

Novel facultative mutualisms that develop between native and non-native ecosystem engineers can lead to the retention of the non-native partner. In some cases, behavior plays an additional, but less understood, role in the development and persistence of mutualisms. In soft-sediment marine habitats along the western Atlantic, the native decorator worm Diopatra cuprea anchors the non-native red alga Gracilaria vermiculophylla to its tube cap in a mutualism. To understand whether the worm's usage of G. vermiculophylla could represent a preference, we first surveyed the species composition of macrophytes affixed to worm tube caps at three sites in coastal Virginia, USA using transect and quadrat sampling. These unmanipulated field surveys supported previous work revealing variable, but often high frequencies (31-98%) of D. cuprea decoration with G. vermiculophylla. We next used field manipulations and controlled laboratory experiments to test the consistency of individual D. cuprea decoration with G. vermiculophylla versus three common macrophytes (Ulva sp., Agardhiella sp., and Spartina alterniflora) found in our field surveys. Twenty-four hours after removing the worm's tube cap in the field, D. cuprea decoration was dominated by both G. vermiculophylla (39.6%) and S. alterniflora (25.9%). When provided a choice of macrophytes in the laboratory, individual D. cuprea consistently decorated with G. vermiculophylla (58.7%) over the other macrophytes, showing a preference for the non-native macrophyte. Our study suggests that preference can drive strong and steadfast interactions between native and non-native organisms, facilitating the latter's persistence and spread, change available habitat, and alter community interactions.

The effects of a myrmecochore-produced chemical on entomopathogenic fungal growth and seed-dispersing ant survival rates and foraging patterns.

Myrmecochory, a type of ant-mediated seed dispersal, is a diffuse, widespread mutualism in which both partners are purported to benefit from the services or rewards of the other. However, ant benefits in this interaction are conflicted and understudied, especially in the context of microbial third parties. Here, we investigate the effect of a myrmecochore plant-produced antimicrobial chemical (sanguinarine) on the growth of a common entomopathogenic fungus (Beauveria bassiana). We then explore whether sanguinarine, through its effect on entomopathogen growth, might influence ant survival and foraging behavior. At high concentrations, sanguinarine increased the growth of B. bassiana, but fungal growth was not affected at concentrations of sanguinarine near natural levels produced in seeds. When ant colonies were exposed to B. bassiana, survival was not affected by a sanguinarine-supplemented diet. Furthermore, ant foraging patterns (preference for or avoidance of food items with sanguinarine) did not change when ants were exposed to the entomopathogen. Though sanguinarine promotes the growth of an entomopathogen at higher concentrations, which might pose an additional risk for ants in myrmecochory, we assert that social immune behavioral defenses (such as grooming or redispersal of seeds after elaiosome consumption) help ants mitigate this risk. By incorporating a microbial third party into this ant-plant interaction, we seek to more fully understand the risks and benefits provided to both partners in this mutualism. We encourage the investigation of third-party influences in reciprocal pairwise interactions to assist in the understanding of the evolution and persistence of mutualisms.

Species richness maintains mutualisms

Ecology Mutualistic communities of species that benefit each other are ubiquitous in ecosystems and are important for ecosystem functioning. However, the relationship between the persistence of mutualisms and species richness has remained unclear. Vidal et al. used a synthetic mutualism in brewer's yeast to experimentally test whether species richness buffers mutualistic communities against exploitation by species that do not provide benefits in return. They showed that richer mutualist communities survive exploitation more often than pairwise mutualisms and that higher species richness and functional redundancy allow mutualist communities to persist in the presence of exploiters. These results provide experimental support for the hypothesis that species richness is necessary for the function and maintenance of mutualistic communities. Science , this issue p. [346][1] [1]: /lookup/doi/10.1126/science.abb6703

Species richness and redundancy promote persistence of exploited mutualisms in yeast.

Mutualisms, or reciprocally beneficial interspecific interactions, constitute the foundation of many ecological communities and agricultural systems. Mutualisms come in different forms, from pairwise interactions to extremely diverse communities, and they are continually challenged with exploitation by nonmutualistic community members (exploiters). Thus, understanding how mutualisms persist remains an essential question in ecology. Theory suggests that high species richness and functional redundancy could promote mutualism persistence in complex mutualistic communities. Using a yeast system (Saccharomyces cerevisiae), we experimentally show that communities with the greatest mutualist richness and functional redundancy are nearly two times more likely to survive exploitation than are simple communities. Persistence increased because diverse communities were better able to mitigate the negative effects of competition with exploiters. Thus, large mutualistic networks may be inherently buffered from exploitation.

Costs and benefits of alternative food handling tactics help explain facultative exploitation of pollination mutualisms.

Many mutualisms are taken advantage of by organisms that take rewards from their partners but provide no benefit in return. In the absence of traits that limit exploitation, facultative exploiters (partners that can either exploit or cooperate) are widely predicted by mutualism theory to choose an exploitative strategy, potentially threatening mutualism stability. However, it is unknown whether facultative exploiters choose to exploit, and, if so, make this choice because it is the most beneficial strategy for them. We explored these questions in a subalpine plant-insect community in which individuals of several bumble bee species visit flowers both "legitimately" (entering via the flower opening, picking up and depositing pollen, and hence behaving mutualistically) and via nectar robbing (creating holes through corollas or using an existing hole, bypassing stigmas and anthers). We applied foraging theory to (1) quantify handling costs, benefits and foraging efficiencies incurred by three bumble bee species as they visited flowers legitimately or robbed nectar in cage experiments, and (2) determine whether these efficiencies matched the food handling tactics these bee species employed in the field. Relative efficiencies of legitimate and robbing tactics depended on the combination of bee and plant species. In some cases (Bombus mixtus visiting Corydalis caseana or Mertensia ciliata), the robbing tactic permitted more efficient nectar removal. As both mutualism and foraging theory would predict, in the field, B.mixtus visiting C.caseana were observed more frequently robbing than foraging legitimately. However, for Bombus flavifrons visiting M.ciliata, the expectation from mutualism theory did not hold: legitimate visitation was the more efficient tactic. Legitimate visitation to M.ciliata was in fact more frequently observed in free-flying B.flavifrons. Free-flying B.mixtus also frequently visited M.ciliata flowers legitimately. This may reflect lower nectar volumes in robbed than unrobbed flowers in the field. These results suggest that a foraging ecology perspective is informative to the choice of tactics facultative exploiters make. In contrast, the simple expectation that exploiters should always have an advantage, and hence could threaten mutualism persistence unless they are deterred or punished, may not be broadly applicable.

Figs, pollinators, and parasites: A longitudinal study of the effects of nematode infection on fig wasp fitness

Mutualisms are interactions between two species in which the fitnesses of both symbionts benefit from the relationship. Although examples of mutualism are ubiquitous in nature, the ecology, evolution, and stability of mutualism has rarely been studied in the broader, multi-species community context in which they occur. The pollination mutualism between figs and fig wasps provides an excellent model system for investigating interactions between obligate mutualists and antagonists. Compared to the community of non-pollinating fig wasps that develop within fig inflorescences at the expense of fig seeds and pollinators, consequences of interactions between female pollinating wasps and their host-specialist nematode parasites is much less well understood. Here we focus on a tri-partite system comprised of a fig (Ficus petiolaris), pollinating wasp (Pegoscapus sp.), and nematode (Parasitodiplogaster sp.), investigating geographical variation in the incidence of attack and mechanisms through which nematodes may limit the fitness of their wasp hosts at successive life history stages. Observational data reveals that nematodes are ubiquitous across their host range in Baja California, Mexico; that the incidence of nematode infection varies across seasons within- and between locations, and that infected pollinators are sometimes associated with fitness declines through reduced offspring production. We find that moderate levels of infection (1–9 juvenile nematodes per host) are well tolerated by pollinator wasps whereas higher infection levels (≥10 nematodes per host) are correlated with a significant reduction in wasp lifespan and dispersal success. This overexploitation, however, is estimated to occur in only 2.8% of wasps in each generation. The result that nematode infection appears to be largely benign – and the unexpected finding that nematodes frequently infect non-pollinating wasps – highlight gaps in our knowledge of pollinator-Parasitodiplogaster interactions and suggest previously unappreciated ways in which this nematode may influence fig and pollinator fitness, mutualism persistence, and non-pollinator community dynamics.

Modelling nutritional mutualisms: challenges and opportunities for data integration.

Nutritional mutualisms are ancient, widespread, and profoundly influential in biological communities and ecosystems. Although much is known about these interactions, comprehensive answers to fundamental questions, such as how resource availability and structured interactions influence mutualism persistence, are still lacking. Mathematical modelling of nutritional mutualisms has great potential to facilitate the search for comprehensive answers to these and other fundamental questions by connecting the physiological and genomic underpinnings of mutualisms with ecological and evolutionary processes. In particular, when integrated with empirical data, models enable understanding of underlying mechanisms and generalisation of principles beyond the particulars of a given system. Here, we demonstrate how mathematical models can be integrated with data to address questions of mutualism persistence at four biological scales: cell, individual, population, and community. We highlight select studies where data has been or could be integrated with models to either inform model structure or test model predictions. We also point out opportunities to increase model rigour through tighter integration with data, and describe areas in which data is urgently needed. We focus on plant-microbe systems, for which a wealth of empirical data is available, but the principles and approaches can be generally applied to any nutritional mutualism.

Mutualism Persistence and Abandonment during the Evolution of the Mycorrhizal Symbiosis.

Mutualistic symbioses with mycorrhizal fungi are widespread in plants. The majority of plant species associate with arbuscular mycorrhizal (AM) fungi. By contrast, the minority associate with ectomycorrhizal (EM) fungi, have abandoned the symbiosis and are nonmycorrhizal (NM), or engage in an intermediate, weakly AM symbiosis (AMNM). To understand the processes that maintain the mycorrhizal symbiosis or cause its loss, we reconstructed its evolution using a ∼3,000-species seed plant phylogeny integrated with mycorrhizal state information. Reconstruction indicated that the common ancestor of seed plants most likely associated with AM fungi and that the EM, NM, and AMNM states descended from the AM state. Direct transitions from the AM state to the EM and NM states were infrequent and generally irreversible, implying that natural selection or genetic constraint could promote stasis once a particular state evolved. However, the evolution of the NM state was more frequent via an indirect pathway through the AMNM state, suggesting that weakening of the AM symbiosis is a necessary precursor to mutualism abandonment. Nevertheless, reversions from the AMNM state back to the AM state were an order of magnitude more likely than transitions to the NM state, suggesting that natural selection favors the AM symbiosis over mutualism abandonment.

Plant preferential allocation and fungal reward decline with soil phosphorus: implications for mycorrhizal mutualism

AbstractExplaining the persistence of mutualism remains a challenge in ecology and evolutionary biology. The evolutionary stability of arbuscular mycorrhiza, a most widespread and ancient mutualistic association, is particularly intriguing because plants lack apparent mechanisms to prevent cheaters from gaining competitive advantages over cooperators. We developed a triple isotopic labeling method (14C, 32P, and 33P) within a split‐root design to measure the exchange of carbon (C) and phosphorus (P) between the host plant and two mycorrhizal partners across a soil P gradient. Host plant preferentially allocated more C to the roots associated with the fungus delivering higher P per unit plant C, and the strength of preferential allocation decreased with increasing soil P availability. The host plant received more P per unit of allocated C from the better fungus and this advantageous exchange rate did not depend upon P availability. As a result, the level of preferential allocation was correlated with the differential delivery of P from the two fungi. Our findings suggest that plant preferential allocation to better mutualists can stabilize mutualisms in environments limiting in the traded resource, but as the availability of this resource increases, plant preferential allocation declines. This environmental dependence of preferential allocation generates predictions of declining levels in relative abundance of mutualistic fungi in high‐resource environments.

Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population

Theory predicts that horizontal acquisition of symbionts by plants and animals must be coupled to release and limited dispersal of symbionts for intergenerational persistence of mutualisms. For deep-sea hydrothermal vent tubeworms (Vestimentifera, Siboglinidae), it has been demonstrated that a few symbiotic bacteria infect aposymbiotic host larvae and grow in a newly formed organ, the trophosome. However, whether viable symbionts can be released to augment environmental populations has been doubtful, because (i) the adult worms lack obvious openings and (ii) the vast majority of symbionts has been regarded as terminally differentiated. Here we show experimentally that symbionts rapidly escape their hosts upon death and recruit to surfaces where they proliferate. Estimating symbiont release from our experiments taken together with well-known tubeworm density ranges, we suggest a few million to 1.5 billion symbionts seeding the environment upon death of a tubeworm clump. In situ observations show that such clumps have rapid turnover, suggesting that release of large numbers of symbionts may ensure effective dispersal to new sites followed by active larval colonization. Moreover, release of symbionts might enable adaptations that evolve within host individuals to spread within host populations and possibly to new environments.

Reversal of mutualism in a leafflower-leafflower moth association: the possible driving role of a third-party partner

A major goal in the study of mutualism is to understand how co-operation is maintained when mutualism may potentially turn into parasitism. Although certain mechanisms facilitate the persistence of mutualism, parasitic species have repeatedly evolved from mutualistic ancestors. However, documented examples of mutualism reversals are still rare. Leafflowers (Phyllantheae; Phyllanthaceae) include approximately 500 species that engage in obligate mutualism with leafflower moths (Epicephala; Gracillariidae), which actively pollinate flowers, and whose larvae feed on the resulting seeds. We found that the Taiwanese population of the Phyllanthus reticulatus species complex was associated with six sympatric Epicephala species, of which three were derived parasites that induced gall formation on flowers/buds and produced no seeds. Notably, two parasitic species have retained mutualistic pollination behaviour, suggesting that the parasitism was likely not selected for to reduce the cost of mutualism. We propose that the galling habit evolved as an adaptation to escape parasitism by a specialized braconid wasp. The tough gall produced by one species was almost free of braconid parasitism, and the swollen gall induced by the other species probably prevents attack as a result of the larger airspace inside the gall. Our findings suggest that the presence of a third-party partner can greatly influence the evolutionary fate of mutualisms, regardless of whether the pairwise interaction continues to favour co-operation.

Persistence of mutualisms with bidirectional interactions in a two-species system

In Lotka–Volterra equations (LVEs) of mutualisms, population densities of mutualists will increase infinitely if the mutualisms between them are strong, which is called the divergence problem. In order to avoid the problem, a mutualism system of two species is analyzed in this work. The model is derived from reactions on lattice and has a form similar to that of LVEs. Population densities of species will not increase infinitely because of spatial limitation on the lattice. Stability analysis of the model demonstrates basic mechanisms by which the mutualisms lead to coexistence/extinction of the species. When in coexistence, intermediate mutualistic effect is shown to lead to the maximal density in certain parameter ranges, while a strong or weak mutualistic effect is not so good. Furthermore, the stability analysis exhibits that extremely strong/weak mutualisms will result in extinction of one/both species.

The cryptic role of biodiversity in the emergence of host-microbial mutualisms.

The persistence of mutualisms in host-microbial - or holobiont - systems is difficult to explain because microbial mutualists, who bear the costs of providing benefits to their host, are always prone to being competitively displaced by non-mutualist 'cheater' species. This disruptive effect of competition is expected to be particularly strong when the benefits provided by the mutualists entail costs such as reduced competitive ability. Using a metacommunity model, we show that competition between multiple cheaters within the host's microbiome, when combined with the spatial structure of host-microbial interactions, can have a constructive rather than a disruptive effect by allowing the emergence and maintenance of mutualistic microorganisms within the host. These results indicate that many of the microorganisms inhabiting a host's microbiome, including those that would otherwise be considered opportunistic or even potential pathogens, play a cryptic yet critical role in promoting the health and persistence of the holobiont across spatial scales.

Flowering asynchrony and mating system effects on reproductive assurance and mutualism persistence in fragmented fig–fig wasp populations

Plants and animals may experience reproductive Allee effects in fragmented populations, and obligate pollination mutualisms may be especially sensitive to extinction risk via this density-dependent process. In this study we examine how a shift from within-crown reproductive synchrony to asynchrony influences reproductive assurance through contributions to selfing and outcrossing in small, spatially isolated populations of Ficus. The research focuses on the monoecious fig F. petiolaris and consists of phenological analyses and genetic assessments of selfing and outcrossing for populations located in Baja California's Sonoran Desert. Phenological censuses of eight populations revealed within-crown asynchrony in 44% of reproducing trees, with 16% having sufficient overlap of male and female flowering phases to permit selfing via the cycling of pollinating fig wasps within natal trees. In mating system analyses of two of these populations, however, multilocus outcrossing rates (t(m)) were indistinguishable from 1. This result, combined with low levels of inbreeding, indicates selfing to be absent or at best a minor contributor to reproductive assurance. The results indicate that the fitness benefits of within-crown asynchrony lie not with selfing, as commonly asserted, but with increased opportunities for outcross pollen transmission and receipt, changing our understanding of the mechanisms by which reproduction is facilitated and extinction risk minimized in naturally fragmented Ficus populations. Given the role of fig fruit as a keystone food resource in many tropical environments, trait variation leading to reproductive assurance in figs, such as within-crown asynchrony, has broader ecosystem-level implications.

Plant species differ in their ability to reduce allocation to non‐beneficial arbuscular mycorrhizal fungi

Theory suggests that cheaters threaten the persistence of mutualisms, but that sanctions to prevent cheating can stabilize mutualisms. In the arbuscular mycorrhizal symbiosis, reports of parasitism suggest that reductions in plant carbon allocation are not universally effective. I asked whether plant species differences in mycorrhizal responsiveness would affect both their susceptibility to parasitism and their reduction in allocation to non-beneficial arbuscular mycorrhizal fungi (AMF) in high-phosphorus soils. In a greenhouse experiment, I found that two C3 grasses, Bromus inermis and Elymus repens, effectively suppressed root colonization and AMF hyphal abundance. Increases in soil phosphorus did not reduce the degree to which AMF increased plant biomass. In contrast, two C4 grasses, Andropogon gerardii and Schizachyrium scoparium, more weakly reduced root colonization and failed to suppress AMF hyphal abundance. Consequently, they experienced strong declines in their response to AMF, and one species suffered parasitism. Thus, species differ in susceptibility to parasitism and their reduction in allocation to non-beneficial AMF. These differences may affect the distribution and abundance of plants and AMF, as well as the stability of the mutualism.