Instability of a hybrid module of antagonistic and mutualistic interactions

Mutualistic and antagonistic interactions coexist in nature. However, little is understood about their relative roles and interactive effects on multispecies coexistence. Here, using a three-species population dynamics model of a resource species, its exploiter, and a mutualist species, we show that a mixture of different interaction types may lead to dynamics that differ completely from those of the isolated interacting pairs. More specifically, a combination of globally stable antagonistic and mutualistic subsystems can lead to unstable population oscillations, suggesting the potential difficulty in the coexistence of antagonism and mutualism. Mutualism-induced instability arises from the indirect positive effect of mutualism on the exploiter. Furthermore, for a three-species system with a stronger mutualistic interaction to persist stably, a weaker antagonistic interaction is required. Network studies of communities composed of one type of interaction may not capture the dynamics of natural communities.     

Stability of a diamond-shaped module with multiple interaction types

Indirect interactions among species emerge from the complexity of ecological networks and can strongly affect the response of communities to disturbances. To determine these indirect interactions and understand better community dynamics, ecologists focused on the interactions within small sets of species or modules. Thanks to their analytical tractability, modules bring insights on the mechanisms occurring in complex interaction networks. So far, most studies have considered modules with a single type of interaction although numerous species are involved in mutualistic and antagonistic interactions simultaneously. In this study, we analyse the dynamics of a diamond-shaped module with multiple interaction types: two resource species sharing a mutualist and a consumer. We describe the different types of indirect interaction occurring between the resource species and the conditions for a stable coexistence of all species. We show that the nature of indirect interactions between resource species (i.e. apparent facilitation, competition or antagonism), as well as stable coexistence, depend on the species generalism and asymmetry of interactions, or in other words, on the distribution of interaction strengths among species. We further unveil that a balance between mutualistic and antagonistic interactions at the level of resource species favours stable coexistence, and that species are more likely to coexist stably if there is apparent facilitation between the two resource species rather than apparent competition. Our results echo existing knowledge on the trophic diamond-shaped module, and confirm that our understanding of communities combining different interaction types can gain from module analyses.     

Global stability of obligate mutualism in community modules with facultative mutualists

Mutualism is a fundamental building block of ecological communities and an important driver of biotic evolution. Classic theory suggests that a pairwise two‐species obligate mutualism is fragile, with a large perturbation potentially driving both mutualist populations into extinction. In nature, however, there are many cases of pairwise obligate mutualism. Such pairwise obligate mutualisms are occasionally associated with additional interactions with facultative mutualists. Here, we use a mathematical model to show that when a two‐species obligate mutualism has a single additional link to a third facultative mutualist, the obligate mutualism can become permanently persistent. In the model, a facultative mutualist interacts with one of two inter‐dependent obligate mutualists, and the facultative mutualist enhances the persistence not only of its directly interacting obligate mutualist, but also that of the other obligate mutualist indirectly, enabling the permanent coexistence of the three mutualist species. The effect of the facultative mutualist is strong; it can allow a three‐species permanent coexistence even when two obligate mutualists by themselves are not sustainable (i.e. not locally stable). These results suggest that facultative mutualists can play a pivotal role for the persistence of obligate mutualisms, and contribute to a better understanding on the mechanisms maintaining more complex mutualistic networks of multiple species.     

Positive interactions among competitors can produce species-rich communities

Although positive interactions between species are well documented, most ecological theory for investigating multispecies coexistence remains rooted in antagonistic interactions such as competition and predation. Standard resource-competition models from this theory predict that the number of coexisting species should not exceed the number of factors that limit population growth. Here I show that positive interactions among resource competitors can produce species-rich model communities supported by a single limiting resource. Simulations show that when resource competitors reduce each others' per capita mortality rate (e.g. by ameliorating an abiotic stress), stable multispecies coexistence with a single resource may be common, even while the net interspecific interaction remains negative. These results demonstrate that positive interactions may provide an important mechanism for generating species-rich communities in nature. They also show that focusing on the net interaction between species may conceal important coexistence mechanisms when species simultaneously engage in both antagonistic and positive interactions.     

Adding biotic complexity alters the metabolic benefits of mutualism

Mutualism is ubiquitous in nature and plays an integral role in most communities. To predict the eco‐evolutionary dynamics of mutualism it is critical to extend classic pair‐wise analysis to include additional species. We investigated the effect of adding a third species to a pair‐wise mutualism in a spatially structured environment. We tested the hypotheses that selection for costly excretions in a focal population (i) decreases when an exploiter is added (ii) increases when a third mutualist is added relative to the pair‐wise scenario. We assayed the selection acting on Salmonella enterica when it exchanges methionine for carbon in an obligate mutualism with an auxotrophic Escherichia coli. A third bacterium, Methylobacterium extorquens, was then added and acted either as an exploiter of the carbon or third obligate mutualist depending on the nitrogen source. In the tripartite mutualism M. extorquens provided nitrogen to the other species. Contrary to our expectations, adding an exploiter increased selection for methionine excretion in S. enterica. Conversely, selection for cooperation was lower in the tripartite mutualism relative to the pair‐wise system. Genome‐scale metabolic models helped identify the mechanisms underlying these changes in selection. Our results highlight the utility of connecting metabolic mechanisms and eco‐evolutionary dynamics.     

Dynamical Transitions in a Pollination–Herbivory Interaction: A Conflict between Mutualism and Antagonism

Plant-pollinator associations are often seen as purely mutualistic, while in reality they can be more complex. Indeed they may also display a diverse array of antagonistic interactions, such as competition and victim–exploiter interactions. In some cases mutualistic and antagonistic interactions are carried-out by the same species but at different life-stages. As a consequence, population structure affects the balance of inter-specific associations, a topic that is receiving increased attention. In this paper, we developed a model that captures the basic features of the interaction between a flowering plant and an insect with a larval stage that feeds on the plant’s vegetative tissues (e.g. leaves) and an adult pollinator stage. Our model is able to display a rich set of dynamics, the most remarkable of which involves victim–exploiter oscillations that allow plants to attain abundances above their carrying capacities and the periodic alternation between states dominated by mutualism or antagonism. Our study indicates that changes in the insect’s life cycle can modify the balance between mutualism and antagonism, causing important qualitative changes in the interaction dynamics. These changes in the life cycle could be caused by a variety of external drivers, such as temperature, plant nutrients, pesticides and changes in the diet of adult pollinators.     

On the structure and stability of mutualistic systems: Analysis of predator-prey and competition models as modified by the action of a slow-growing mutualist

Two basic models of mutualism are presented in which interactions among three species lead to mutualism between two of them. The models represent 2-species predator-prey or competition systems in which a third species acts as a mutualist with either the predator, the prey, or one of the competitors. The models include the assumptions that there is a cost of associating with the mutualist and that the mutualist population grows much more slowly than the other two populations. Special cases of these two models correspond to six qualitatively different types of mutualistic benefit, all of which are known to occur in nature: deterring predation, increasing prey availability, feeding on (or competing with) a predator, increasing competitive interactions, decreasing competitive interactions, and feeding on (or competing with) a competitor. These models and their special cases are subjected to a local stability analysis. The results show that mutualism based upon deterring predation, competing with a predator, or decreasing competitive interactions enhances local stability, while mutualism based upon increasing prey availability or increasing competitive interactions reduces local stability. These results clearly reject the idea that mutualism is an inherently unstable process, and reinforces the idea that each different kind of mutualism will have to be considered separately. Compared to 2-species models of mutualism, the 3-species models provide a more realistic representation of the structure of many mutualistic systems, the mechanisms by which one species benefits another, and the regulation of the interaction.     

Host discrimination in modular mutualisms: a theoretical framework for meta-populations of mutualists and exploiters

Plants in multiple symbioses are exploited by symbionts that consume their resources without providing services. Discriminating hosts are thought to stabilize mutualism by preferentially allocating resources into anatomical structures (modules) where services are generated, with examples of modules including the entire inflorescences of figs and the root nodules of legumes. Modules are often colonized by multiple symbiotic partners, such that exploiters that co-occur with mutualists within mixed modules can share rewards generated by their mutualist competitors. We developed a meta-population model to answer how the population dynamics of mutualists and exploiters change when they interact with hosts with different module occupancies (number of colonists per module) and functionally different patterns of allocation into mixed modules. We find that as module occupancy increases, hosts must increase the magnitude of preferentially allocated resources in order to sustain comparable populations of mutualists. Further, we find that mixed colonization can result in the coexistence of mutualist and exploiter partners, but only when preferential allocation follows a saturating function of the number of mutualists in a module. Finally, using published data from the fig–wasp mutualism as an illustrative example, we derive model predictions that approximate the proportion of exploiter, non-pollinating wasps observed in the field.     

The origin of a mutualism: a morphological trait promoting the evolution of ant-aphid mutualisms

Mutualisms are mutually beneficial interactions between species and are fundamentally important at all levels of biological organization. It is not clear, however, why one species participates in a particular mutualism whereas another does not. Here we show that pre-existing traits can dispose particular species to evolve a mutualistic interaction. Combining morphological, ecological, and behavioral data in a comparative analysis, we show that resource use in Chaitophorus aphids (Hemiptera: Aphididae) modulates the origin of their mutualism with ants. We demonstrate that aphid species that feed on deeper phloem elements have longer mouthparts, that this inhibits their ability to withdraw their mouthparts and escape predators and that, consequently, this increases their need for protection by mutualist ants.     

Three-way coexistence in obligate mutualist-exploiter interactions: the potential role of competition

Many mutualisms host "exploiter" species that consume the benefits provided by one or both mutualists without reciprocating. Exploiters have been widely assumed to destabilize mutualisms, yet they are common. We develop models to explore conditions for local coexistence of obligate plant/pollinating seed parasite mutualisms and nonpollinating exploiters. As the larvae of both pollinators and (at a later time) exploiters consume seeds, we examine the importance of intraspecific and (asymmetric) interspecific competition among and between pollinators and exploiters for achieving three-way coexistence. With weak intra- and interspecific competition, exploiters can invade the stable mutualism and coexist with the mutualists (either stably or with oscillations), provided the exploiters' intrinsic birthrate (b(E)) slightly exceeds that of the pollinators. At higher b(E), all three species go locally extinct. When facing strong interspecific competition, exploiters cannot invade and coexist with the mutualists if intraspecific competition in pollinators and exploiters is weak. However, strong intraspecific competition in pollinators and exploiters facilitates exploiter invasion and coexistence and greatly expands the range of b(E) over which stable coexistence occurs. Our results suggest that mutualist/exploiter coexistence may be more easily achieved than previously thought, thus highlighting the need for a better understanding of competition among and between mutualists and exploiters.     

A shared limiting resource leads to competitive exclusion in a cross-feeding system

Species interactions and coexistence are often dependent upon environmental conditions. When two cross-feeding bacteria exchange essential nutrients, the addition of a cross-fed nutrient to the environment can release one species from its dependence on the other. Previous studies suggest that continued coexistence depends on relative growth rates: coexistence is maintained if the slower-growing species is released from its dependence on the other, but if the faster-growing species is released, the slower-growing species will be lost (a hypothesis that we call ‘feed the faster grower’ or FFG). Using invasion-from-rare experiments with two reciprocally cross-feeding bacteria, genome-scale metabolic modelling and classical ecological models, we explored the potential for coexistence when one cross-feeder became independent. We found that whether nutrient addition shifted an interaction from mutualism to commensalism or parasitism depended on whether the nutrient that limited total growth was required by one or both species. Parasitism resulted when both species required the growth-limiting resource. Importantly, coexistence was only lost when the interaction became parasitism, and the obligate species had a slower growth rate. Under these restricted conditions, the FFG hypothesis applied. Our results contribute to a mechanistic understanding of how resources can be manipulated to alter interactions and coexistence in microbial communities.     

Interaction-type diversity hypothesis and interaction strength: the condition for the positive complexity-stability effect to arise

Recently, a theoretical hypothesis was proposed that the coexistence of antagonism and mutualism may stabilize ecological community and even give rise to a positive complexity-stability relationship (interaction-type diversity hypothesis). This hypothesis was derived from an analysis of community model, which was developed based on two specific assumptions about the interaction strengths: those are, (i) different interaction types, antagonism and mutualism, have quantitatively comparable magnitude of effects to population growth; and (ii) interaction strength decreases with increasing interaction links of the same interaction type. However, those assumptions do not necessarily hold in real ecosystems, leaving unclear how robust this hypothesis is. Here, using a model with those two assumptions relaxed, we show (i) that the balance of interaction strength is necessary for the positive complexity effect to arise and (ii) that interaction-type diversity hypothesis may still hold when interaction strength decreases with increasing links of all interaction type for some species.     

Parasites of mutualisms

Cooperation invites cheating, and nowhere is this more apparent than when different species cooperate, known as mutualism. In almost all mutualisms studied, specialist parasites have been identified that purloin the benefits that one mutualist provides another. Explaining how parasites are kept from driving mutualisms extinct remains an unsolved problem because existing theories explaining the maintenance of cooperation do not apply to parasites of mutualisms. Nonetheless, these theories can be summarized in such a way as to suggest how mutualisms can persist in the face of parasites. (1) For cooperation to occur, the recipient of a benefit must reciprocate, and the recriprocated benefit must be captured by the initial giver or its offspring. (2) For cooperation to persist, the mutualism must be re-assembled each generation. Because most mutualisms are of the "by-product' type, broadly defined, the first condition is normally always fulfilled. Thus, the maintenance of mutualism usually requires enforcement of the second condition: reliable re-assembly. Hence, I argue that the persistence of mutualism is best understood by using theories of species coexistence, because each mutualist can be considered a resource for the other, and species coexistence theory explains how multiple taxa (e.g. parasites and mutualists) can stably partition a resource over multiple generations. This approach connects the study of mutualism to theories of population regulation and helps to identify key factors that have promoted the evolution, maintenance and breakdown of mutualism. I discuss how these ideas might apply to and be tested in ant-plant, fig-wasp and yucca-moth mutualisms.     

Global stability of the coexistence equilibrium for a general class of models of facultative mutualism

Many models of mutualism have been proposed and studied individually. In this paper, we develop a general class of models of facultative mutualism that covers many of such published models. Using mild assumptions on the growth and self-limiting functions, we establish necessary and sufficient conditions on the boundedness of model solutions and prove the global stability of a unique coexistence equilibrium whenever it exists. These results allow for a greater flexibility in the way each mutualist species can be modelled and avoid the need to analyse any single model of mutualism in isolation. Our generalization also allows each of the mutualists to be subject to a weak Allee effect. Moreover, we find that if one of the interacting species is subject to a strong Allee effect, then the mutualism can overcome it and cause a unique coexistence equilibrium to be globally stable.     

Fusing spatial resource heterogeneity with a competition–colonization trade-off in model communities

Two commonly cited mechanisms of multispecies coexistence in patchy environments are spatial heterogeneity in competitive abilities caused by variation in resources and a competition–colonization trade-off. In this paper, a model that fuses these mechanisms together is presented and analyzed. The model suggests that spatial variation in resource ratios can lead to multispecies coexistence, but this mechanism by itself is weak when the number of resources for which species compete is small. However, spatial resource heterogeneity is a powerful mechanism for multispecies coexistence when it acts synergistically with a competition–colonization trade-off. The model also shows how resource supply can control the competitive balance between species that are weak competitors but superior colonizers and strong competitors/inferior colonizers. This provides additional theoretical support for a possible explanation of empirically observed hump-shaped relationships between species diversity and ecological productivity.     

The effects of space and diversity of interaction types on the stability of complex ecological networks

The relationship between structure and stability in ecological networks and the effect of spatial dynamics on natural communities have both been major foci of ecological research for decades. Network research has traditionally focused on a single interaction type at a time (e.g. food webs, mutualistic networks). Networks comprising different types of interactions have recently started to be empirically characterized. Patterns observed in these networks and their implications for stability demand for further theoretical investigations. Here, we employed a spatially explicit model to disentangle the effects of mutualism/antagonism ratios in food web dynamics and stability. We found that increasing levels of plant-animal mutualistic interactions generally resulted in more stable communities. More importantly, increasing the proportion of mutualistic vs. antagonistic interactions at the base of the food web affects different aspects of ecological stability in different directions, although never negatively. Stability is either not influenced by increasing mutualism—for the cases of population stability and species’ spatial distributions—or is positively influenced by it—for spatial aggregation of species. Additionally, we observe that the relative increase of mutualistic relationships decreases the strength of biotic interactions in general within the ecological network. Our work highlights the importance of considering several dimensions of stability simultaneously to understand the dynamics of communities comprising multiple interaction types.     

Dynamics and coexistence in a system with intraguild mutualism

It is a tenet of ecological theory that two competing consumers cannot stably coexist on a single limiting resource in a homogeneous environment. Many mechanisms and processes have since been evoked and studied, empirically and theoretically, to explain species coexistence and the observed biological diversity. Facilitative interactions clearly have the potential to enhance coexistence. Yet, even though mutual facilitation between species of the same guild is widely documented empirically, the subject has received very little theoretical attention. Here, we study one form of intraguild mutualism in the simplest possibly community module of one resource and two consumers. We incorporate mutualism as enhanced consumption in the presence of the other consumers. We find that intraguild mutualism can (a) significantly enhance coexistence of consumers, (b) induce cyclic dynamics, and (c) give rise to a bi-stability (a ‘joint’ Allee effect) and potentially catastrophic collapse of both consumer species.     

Interspecific population regulation and the stability of mutualism: fruit abortion and density-dependent mortality of pollinating seed-eating insects

Two questions central to the population ecology of mutualism include: (1) what mechanisms prevent the inherent positive feedback of mutualism from leading to unbounded population growth; and (2) what mechanisms prevent instability from arising due to overexploitation. Theory and empiricism suggest that preventing such instability requires density‐dependent processes. A recent theory proposes that if benefits and costs to a mutualist vary with the density of its partner, then instability can be prevented if the former species can control demographic rates and regulate (or limit) the population density of its partner. The ecological and evolutionary feasibility of this theory of interspecific population regulation has been demonstrated using quantitative models of mutualism between plants and pollinating seed‐consuming insects. In these models, resource‐limited fruit set and ensuing fruit abortion are mechanisms that can lead to density‐dependent recruitment and population regulation of the insects. Yet, there has been little interplay between these theoretical results and empirical research. A recent study empirically examined the density‐dependent effects of resource‐limited fruit set and fruit abortion in the Yucca/moth mutualism. An analysis of the study led to the conclusion that, even though fruit abortion can account for >95% of moth mortality, it is largely a density‐independent source of mortality that cannot regulate moth population density. Here, we re‐analyze those empirical data and conduct further theoretical analyses to examine the nature of fruit abortion on moth recruitment. We conclude that resource‐limited fruit set and fruit abortion can effectively regulate and limit moth populations, due to its density‐dependent feedback on moth recruitment. Nonetheless, in any given interaction, multiple sources of mortality may contribute to the regulation and limitation of populations, and hence the stability of mutualism, including, larval competition and mortality due to locule damage in the Yucca/moth mutualism.     

Carbon allocation and competition maintain variation in plant root mutualisms

Plants engage in multiple root symbioses that offer varying degrees of benefit. We asked how variation in partner quality persists using a resource‐ratio model of population growth. We considered the plant's ability to preferentially allocate carbon to mutualists and competition for plant carbon between mutualist and nonmutualist symbionts. We treated carbon as two nutritionally interchangeable, but temporally separated, resources—carbon allocated indiscriminately for the construction of the symbiosis, and carbon preferentially allocated to the mutualist after symbiosis establishment and assessment. This approach demonstrated that coexistence of mutualists and nonmutualists is possible when fidelity of the plant to the mutualist and the cost of mutualism mediate resource competition. Furthermore, it allowed us to trace symbiont population dynamics given varying degrees of carbon allocation. Specifically, coexistence occurs at intermediate levels of preferential allocation. Our findings are consistent with previous empirical studies as well the application of biological market theory to plantroot symbioses.     

Consumer–resource dynamics of indirect interactions in a mutualism–parasitism food web module

Food web dynamics are well known to vary with indirect interactions, classic examples including apparent competition, intraguild predation, exploitative competition, and trophic cascades of food chains. Such food web modules entailing predation and competition have been the focus of much theory, whereas modules involving mutualism have received far less attention. We examined an empirically common food web module involving mutualistic (N ₂) and parasitic (N ₃) consumers exploiting a resource of a basal mutualist (N ₁), as illustrated by plants, pollinators, and nectar robbers. This mutualism–parasitism food web module is structurally similar to exploitative competition, suggesting that the module of two consumers exploiting a resource is unstable. Rather than parasitic consumers destabilizing the module through (?,?) indirect interactions, two mechanisms associated with the mutualism can actually enhance the persistence of the module. First, the positive feedback of mutualism favors coexistence in stable limit cycles, whereby (+,?) indirect interactions emerge in which increases in N ₂ have positive effects on N ₃ and increases in N ₃ have negative effects on N ₂. This (+,?) indirect interaction arising from the saturating positive feedback of mutualism has broad feasibility across many types of food web modules entailing mutualism. Second, optimization of resource exploitation by the mutualistic consumer can lead to persistence of the food web module in a stable equilibrium. The mutualism–parasitism food web module is a basic unit of food webs in which mutualism favors its persistence simply through density-dependent population dynamics, rather than parasitism destabilizing the module.