From parasitism to mutualism: partner control in asymmetric interactions

Intraspecific cooperation and interspecific mutualism often feature a marked asymmetry in the scope for exploitation. Cooperation may nevertheless persist despite one‐sided opportunities for cheating, provided that the partner vulnerable to exploitation has sufficient control over the duration of interaction. Here we develop a simple, game theoretical model of this form of partner control. We show that as a victim's ability to terminate an encounter increases, selection can favour reduced exploitation, resulting in a switch from parasitism to mutualism. For a given level of control, exploitation is likely to be less intense and the interaction to last longer when there are greater mutualistic benefits to be gained, and when the benefits of cheating are lower relative to the costs inflicted on the victim. Observations of interactions between cleaner‐fish and non‐predatory species of client are shown to match these predictions.     

Population dynamics and mutualism: functional responses of benefits and costs

We develop an approach for studying population dynamics resulting from mutualism by employing functional responses based on density-dependent benefits and costs. These functional responses express how the population growth rate of a mutualist is modified by the density of its partner. We present several possible dependencies of gross benefits and costs, and hence net effects, to a mutualist as functions of the density of its partner. Net effects to mutualists are likely a monotonically saturating or unimodal function of the density of their partner. We show that fundamental differences in the growth, limitation, and dynamics of a population can occur when net effects to that population change linearly, unimodally, or in a saturating fashion. We use the mutualism between senita cactus and its pollinating seed-eating moth as an example to show the influence of different benefit and cost functional responses on population dynamics and stability of mutualisms. We investigated two mechanisms that may alter this mutualism's functional responses: distribution of eggs among flowers and fruit abortion. Differences in how benefits and costs vary with density can alter the stability of this mutualism. In particular, fruit abortion may allow for a stable equilibrium where none could otherwise exist.     

Ecological specialization and trade affect the outcome of negotiations in mutualism

By definition, mutualisms involve the exchange of goods or services between partners. It has been shown that mutualism can grade into parasitism, but even when exchange is mutually beneficial, a conflict of interest remains because each partner benefits from reaping more benefits at a lower cost. Metaphorically, the partners negotiate the conditions of trade, the outcome of which will determine the net benefit to each partner. Each partner can adjust its allocation to self-provisioning while negotiating the ratio at which benefits are exchanged. To understand how these two features of trade affect mutualisms, we used the example of the plant-arbuscular mycorrhizal mutualism and modeled uptake and trade of two resources, phosphorus and carbon. In most contexts, the fungus specialized on phosphorus uptake while the plant took up both phosphorus and carbon. However, when phosphorus was abundant and light was scarce, the plant specialized, taking up only carbon and relying on trade for phosphorus. Resource availability was the most important factor determining specialization and the outcome of negotiation and trade, but other aspects of the context were also important. These results suggest experiments to link these two key features of trade with environmental conditions to determine the outcome of mutualism.     

The motile escape response of a sessile prey: A sponge-scallop mutualism

The association of the sponges Myxilla incrustans (Esper) and Mycale adhaerens (Lambe) with the scallops Chlamys hastata hericia Gould and C. rubida (Hines) is shown to be a mutualism, which protects the sponges from predatory sponge-rasping dorid nudibranchs and the scallops from predatory starfish. The sponge is protected by scallop motility (also shown for the Suberites ficus-hermit crab association). The sponge helps to protect the scallops by altering the surface texture of the shell so increasing the efficacy of the swimming escape response by decreasing the adhesive abilities of asteroid tube-feet. The sponge also provides tactile camouflage against certain predatory starfish. There was no evidence that either component chemically deceived or repelled the predators of the other component. Predation pressure on both components of the association appears to be the major force leading to the mutualism.     

Evolutionary stability of mutualism: interspecific population regulation as an evolutionarily stable strategy

Interspecific mutualisms are often vulnerable to instability because low benefit : cost ratios can rapidly lead to extinction or to the conversion of mutualism to parasite-host or predator-prey interactions. We hypothesize that the evolutionary stability of mutualism can depend on how benefits and costs to one mutualist vary with the population density of its partner, and that stability can be maintained if a mutualist can influence demographic rates and regulate the population density of its partner. We test this hypothesis in a model of mutualism with key features of senita cactus (Pachycereus schottii)-senita moth (Upiga virescens) interactions, in which benefits of pollination and costs of larval seed consumption to plant fitness depend on pollinator density. We show that plants can maximize their fitness by allocating resources to the production of excess flowers at the expense of fruit. Fruit abortion resulting from excess flower production reduces pre-adult survival of the pollinating seed-consumer, and maintains its density beneath a threshold that would destabilize the mutualism. Such a strategy of excess flower production and fruit abortion is convergent and evolutionarily stable against invasion by cheater plants that produce few flowers and abort few to no fruit. This novel mechanism of achieving evolutionarily stable mutualism, namely interspecific population regulation, is qualitatively different from other mechanisms invoking partner choice or selective rewards, and may be a general process that helps to preserve mutualistic interactions in nature.     

Benefits and costs of mutualism: demographic consequences in a pollinating seed-consumer interaction

Interspecific interactions can affect population dynamics and the evolution of species traits by altering demographic rates such as reproduction and survival. The influence of mutualism on population processes is thought to depend on both the benefits and costs of the interaction. However, few studies have explicitly quantified both benefits and costs in terms of demographic rates; furthermore there has been little consideration as to how benefits and costs depend on the demographic effects of factors extrinsic to the interaction. I studied how benefits (pollination) and costs (larval fruit consumption) of pollinating seed-consumers (senita moths) affect the reproduction of senita cacti and how these effects may rely on extrinsic water limitation for reproduction. Fruit initiation was not limited by moth pollination, but survival of initiated fruit increased when moth eggs were removed from flowers. Watered cacti produced more flowers and initiated more fruit from hand-pollinated flowers than did unwatered cacti, but fruit initiation remained low despite excess pollen. Even though water, pollination and larvae each affected a component of cactus reproduction, when all of these factors were included in a factorial experiment, pollination and water determined rates of reproduction. Counter-intuitively, larval fruit consumption had a negligible effect on cactus reproduction. By quantifying both benefits and costs of mutualism in terms of demographic rates, this study demonstrates that benefits and costs can be differentially influential to population processes and that interpretation of their influences can depend on demographic effects of factors extrinsic to the interaction.     

Nematode–bacteria mutualism: Selection within the mutualism supersedes selection outside of the mutualism

The coevolution of interacting species can lead to codependent mutualists. Little is known about the effect of selection on partners within verses apart from the association. Here, we determined the effect of selection on bacteria (Xenorhabdus nematophila) both within and apart from its mutualistic partner (a nematode, Steinernema carpocapsae). In nature, the two species cooperatively infect and kill arthropods. We passaged the bacteria either together with (M+), or isolated from (M?), nematodes under two different selection regimes: random selection (S?) and selection for increased virulence against arthropod hosts (S+). We found that the isolated bacteria evolved greater virulence under selection for greater virulence (M?S+) than under random selection (M?S?). In addition, the response to selection in the isolated bacteria (M?S+) caused a breakdown of the mutualism following reintroduction to the nematode. Finally, selection for greater virulence did not alter the evolutionary trajectories of bacteria passaged within the mutualism (M+S+ = M+S?), indicating that selection for the maintenance of the mutualism was stronger than selection for increased virulence. The results show that selection on isolated mutualists can rapidly breakdown beneficial interactions between species, but that selection within a mutualism can supersede external selection, potentially generating codependence over time.     

Parabiotic ants: the costs and benefits of symbiosis

1. Mutualisms are important drivers of co‐evolution and speciation. However, they typically imply costs for one or both partners. Each partner consequently tries to maximise benefits and minimise costs. Mutualisms can therefore develop towards commensalism or parasitism if one partner fails to provide sufficient benefits. This is particularly likely in diffuse interactions, where multiple species can associate with each other. If costs and benefits of a species vary with the identity of the partner species, this may result in a geographical mosaic of co‐evolution. 2. In the present study, inter‐specific interactions in two parabiotic associations of ants were studied (Hymenoptera: Formicidae). One Crematogaster species was associated with one of two closely related Camponotus species. We assessed cost and benefits by studying behavioural interactions, foraging behaviour, and nest defence in the associations. 3. While parabioses had been shown to be mutualistic, evidence was found for exploitation and aggressive competition between species. In spite of apparent costs of being exploited, we found no benefits for one partner (Crematogaster). The magnitude of potential costs to Crematogaster varied between the two Camponotus species. 4. We conclude that the cost/benefit ratio for Crematogaster varies between the two Camponotus partners, and between environmental conditions. Parabiosis can thus fluctuate between mutualism, commensalism, and parasitism, with Crematogaster being the species that may have higher costs than benefits. 5. We suggest that geneflow in the Crematogaster population hinders local adaptation to the resulting mosaic of locally varying selection pressures. This study demonstrates how diffuse interactions and environmental variation can result in a complex of local selection pressures.     

The exploitation of mutualisms

Mutualisms (interspecific cooperative interactions) are ubiquitously exploited by organisms that obtain the benefits mutualists offer, while delivering no benefits in return. The natural history of these exploiters is well-described, but relatively little effort has yet been devoted to analysing their ecological or evolutionary significance for mutualism. Exploitation is not a unitary phenomenon, but a set of loosely related phenomena: exploiters may follow mixed strategies or pure strategies at either the species or individual level, may or may not be derived from mutualists, and may or may not inflict significant costs on mutualisms. The evolutionary implications of these different forms of exploitation, especially the threats they pose to the stability of mutualism, have as yet been minimally explored. Studies of this issue are usually framed in terms of a "temptation to defect" that generates a destabilizing conflict of interest between partners. I argue that this idea is in fact rather inappropriate for interpreting most observed forms of exploitation in mutualisms. I suggest several alternative and testable ideas for how mutualism can persist in the face of exploitation.     

Negotiation, sanctions, and context dependency in the legume-Rhizobium mutualism

Two important questions about mutualisms are how the fitness costs and benefits to the mutualist partners are determined and how these mechanisms affect the evolutionary dynamics of the mutualism. We tackle these questions with a model of the legume-rhizobium symbiosis that regards the mutualism outcome as a result of biochemical negotiations between the plant and its nodules. We explore the fitness consequences of this mechanism to the plant and rhizobia and obtain four main results. First, negotiations permit the plant to differentially reward more-cooperative rhizobia--a phenomenon termed "plant sanctions"--but only when more-cooperative rhizobia also provide the plant with good outside options during negotiations with other nodules. Second, negotiations may result in seemingly paradoxical cases where the plant is worse off when it has a "choice" between two strains of rhizobia than when infected by either strain alone. Third, even when sanctions are effective, they are by themselves not sufficient to maintain cooperative rhizobia in a population: less cooperative strains always have an advantage at the population level. Finally, partner fidelity feedback, together with genetic correlations between a rhizobium strain's cooperativeness and the outside options it provides, can maintain cooperative rhizobia. Our results show how joint control over the outcome of a mutualism through the proximate mechanism of negotiation can affect the evolutionary dynamics of interspecific cooperation.     

Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae)

The landmark discovery of obligate pollination mutualism between Glochidion plants and Epicephala moths has sparked increased interest in the pollination systems of Phyllantheae plants. In this paper I review current information on the natural history and evolutionary history of obligate pollination mutualism in Phyllantheae. Currently, an estimated >500 species are mutualistic with Epicephala moths that actively pollinate flowers and whose progeny feed on the resulting seeds. The Phyllantheae also includes species that are not mutualistic with Epicephala moths and are instead pollinated by bees and/or flies or ants. Phylogenetic analyses indicate that the mutualism evolved independently five times within Phyllantheae, whereas active pollination behavior, a key innovation in this mutualism, evolved once in Epicephala . Reversal of mutualism has occurred at least once in both partner lineages, involving a Breynia species that evolved an alternative pollination system and a derived clade of Epicephala that colonized ant-pollinated Phyllantheae hosts and thereby lost the pollinating habit. The plant–moth association is highly species specific, although a strict one-to-one assumption is not perfectly met. A comparison of plant and moth phylogenies suggests signs of parallel speciation, but partner switches have occurred repeatedly at a range of taxonomic levels. Overall, the remarkable species diversity and multiple originations of the mutualism provide excellent opportunities to address many important questions on mutualism and the coevolutionary process. Although research on the biology of the mutualism is still in its infancy, the Phyllantheae– Epicephala association holds promise as a new model system in ecology and evolutionary biology.     

Selective feedback between dispersal distance and the stability of mutualism

The evolution and maintenance of mutually beneficial interactions has been one of the oldest problems for evolutionary theory. For cooperation to be stable, mechanisms such as spatial population structure must exist that prevent non‐cooperative individuals from invading cooperative groups. Selection for certain traits like increased dispersal can erode that structure. Here, I used a spatially explicit individual based dual lattice computer simulation to investigate how the evolution of dispersal interacts with the evolution of mutualism and how this interaction affects the stability of mutualism in the face of non‐mutualists. I ran simulations manipulating the self‐structuring phenotype, dispersal distance, over a range of environmental conditions, as well as letting both dispersal and mutualism evolve independently, with and without a cost of dispersal. I found that environmental productivity is negatively correlated with the stability of mutualism, and that the stability of mutualism relied on the ability of mutualists to evolve shorter dispersal distances than non‐mutualists. The inclusion of a dispersal cost essentially fixed the upper limit of dispersal, and therefore limits the ability of non‐mutualists to evolve higher average dispersal than mutualists, but as costs are relaxed, the differences are recovered. These results show how selection on seemingly unrelated traits can align suites of traits into holistic life history strategies.     

Natural selection on extrafloral nectar production in Chamaecrista fasciculata: the costs and benefits of a mutualism trait

Cost-benefit models of the evolution of mutualism predict that the current state of mutualism results from trade-offs between fitness costs of mutualist traits and the fitness benefits of association. We test the assumptions of such models by measuring patterns of natural selection on a mutualist trait, extrafloral nectar production in Chamaecrista fasciculata. Selection was measured on plants from which ants had been excluded (removing the mutualist benefit of the trait), from which all insects had been excluded (removing costs of herbivory in addition to mutualist benefits), and unmanipulated plants (where both costs and benefits were present). Selection analysis based on half-sibling-mean regressions of fitness on the trait revealed no evidence of costs of extrafloral nectar production in the absence of all insects or in the absence of ants. However, examination of the selective surfaces for these treatments suggest that costs of nectar production may exist and are exacerbated by the presence of herbivory. In the presence of ants, natural selection favors high extrafloral nectar production, consistent with a fitness benefit to this mutualist trait in the presence of the mutualist partner. In this study, the interaction of costs and benefits did not produce an evolutionary optimum for the trait within the range of variation observed, suggesting that application of a cost-benefit framework to this trait will benefit from considering the influence of temporal and spatial variation on the quality of costs and benefits.     

Understanding the coevolutionary dynamics of mutualism with population genomics

Decades of research on the evolution of mutualism has generated a wealth of possible ways whereby mutually beneficial interactions between species persist in spite of the apparent advantages to individuals that accept the benefits of mutualism without reciprocating — but identifying how any particular empirical system is stabilized against cheating remains challenging. Different hypothesized models of mutualism stability predict different forms of coevolutionary selection, and emerging high‐throughput sequencing methods allow examination of the selective histories of mutualism genes and, thereby, the form of selection acting on those genes. Here, I review the evolutionary theory of mutualism stability and identify how differing models make contrasting predictions for the population genomic diversity and geographic differentiation of mutualism‐related genes. As an example of the possibilities offered by genomic data, I analyze genes with roles in the symbiosis of Medicago truncatula and nitrogen‐fixing rhizobial bacteria, the first classic mutualism in which extensive genomic resources have been developed for both partners. Medicago truncatula symbiosis genes, as a group, differ from the rest of the genome, but they vary in the form of selection indicated by their diversity and differentiation — some show signs of selection expected from roles in sanctioning noncooperative symbionts, while others show evidence of balancing selection expected from coevolution with symbiont signaling factors. I then assess the current state of development for similar resources in other mutualistic interactions and look ahead to identify ways in which modern sequencing technology can best inform our understanding of mutualists and mutualism.     

Repeated independent evolution of obligate pollination mutualism in the Phyllantheae-Epicephala association

The well-known fig-fig wasp and yucca-yucca moth mutualisms are classic examples of obligate mutualisms that have been shaped by millions of years of coevolution. Pollination systems involving obligate seed parasites are only expected to evolve under rare circumstances where their positive effects are not swamped by abundant co-pollinators and heavy costs resulting from seed destruction. Here, we show that, in Phyllantheae, specialization to pollination by Epicephala moths evolved at least five times, involving more than 500 Phyllantheae species in this obligate association. Active pollination behaviour evolved once in Epicephala, 10-20 Myr after the initial divergence of their host plants. The pollinating Epicephala moths thus radiated on an already-diverged host lineage and successively colonized new Phyllantheae hosts, thereby giving rise to repeated independent evolution of the specialized pollination system in Phyllantheae. The present evolutionary success of this association rests entirely upon active pollination by Epicephala, making this a distinct example of an evolutionary key innovation. Overall, our findings provide a clear empirical demonstration of how a combination of evolutionary innovation and partner shifts facilitates the spread of mutualism in a coevolving species interaction.     

Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism

Mutualisms, beneficial interactions between species, are expected to be unstable because delivery of benefit likely involves fitness costs and selection should favour partners that deliver less benefit. Yet, mutualisms are common and persistent, even in the largely promiscuous associations between plants and soil microorganisms such as arbuscular mycorrhizal fungi. In two different systems, we demonstrate preferential allocation of photosynthate by host plants to the more beneficial of two AM fungal symbionts. This preferential allocation could allow the persistence of the mutualism if it confers sufficient advantage to the beneficial symbiont that it overcomes the cost of mutualism. We find that the beneficial fungus does increase in biomass when the fungi are spatially separated within the root system. However, in well-mixed fungal communities, non-beneficial fungi proliferate as expected from their reduced cost of mutualism. Our findings suggest that preferential allocation within spatially structured microbial communities can stabilize mutualisms between plants and root symbionts.     

Antagonistic bacterial interactions help shape host-symbiont dynamics within the fungus-growing ant-microbe mutualism

Conflict within mutually beneficial associations is predicted to destabilize relationships, and theoretical and empirical work exploring this has provided significant insight into the dynamics of cooperative interactions. Within mutualistic associations, the expression and regulation of conflict is likely more complex than in intraspecific cooperative relationship, because of the potential presence of: i) multiple genotypes of microbial species associated with individual hosts, ii) multiple species of symbiotic lineages forming cooperative partner pairings, and iii) additional symbiont lineages. Here we explore complexity of conflict expression within the ancient and coevolved mutualistic association between attine ants, their fungal cultivar, and actinomycetous bacteria (Pseudonocardia). Specifically, we examine conflict between the ants and their Pseudonocardia symbionts maintained to derive antibiotics against parasitic microfungi (Escovopsis) infecting the ants' fungus garden. Symbiont assays pairing isolates of Pseudonocardia spp. associated with fungus-growing ants spanning the phylogenetic diversity of the mutualism revealed that antagonism between strains is common. In contrast, antagonism was substantially less common between more closely related bacteria associated with Acromyrmex leaf-cutting ants. In both experiments, the observed variation in antagonism across pairings was primarily due to the inhibitory capabilities and susceptibility of individual strains, but also the phylogenetic relationships between the ant host of the symbionts, as well as the pair-wise genetic distances between strains. The presence of antagonism throughout the phylogenetic diversity of Pseudonocardia symbionts indicates that these reactions likely have shaped the symbiosis from its origin. Antagonism is expected to prevent novel strains from invading colonies, enforcing single-strain rearing within individual ant colonies. While this may align ant-actinomycete interests in the bipartite association, the presence of single strains of Pseudonocardia within colonies may not be in the best interest of the ants, because increasing the diversity of bacteria, and thereby antibiotic diversity, would help the ant-fungus mutualism deal with the specialized parasites.     

Control in mutualisms: Combined implications of partner choice and bargaining roles

When two species form a mutualistic association, the degree of control that each has over the interaction may be pivotal in determining the relative benefit each obtains. We incorporate the capacity for partner choice into a model of mutualism based on the exchange of goods and/or services, where one guild of mutualists plays the role of proposer (proposing a price at which the goods and/or services will be exchanged) and the other plays the role of responder (accepting or rejecting the deal). We show how the payoff structure in this scenario and other closely related ones correspond to the ultimatum and demand games of economics. In the model, there are both costs and benefits to a guild whose players have control over interactions. Control over interactions in the sense of being able to exercise partner choice can benefit a guild by selecting for mutualism in its partners, but is most effective in selecting against moderately exploitative partners, and so can give highly exploitative partners an advantage. This can generate dynamics similar to taxon cycles or those seen in models with competition-colonization tradeoffs, wherein increasingly more mutualistic partners (acting as superior competitors) are selected for up to a tipping point, at which highly exploitative strategies (akin to superior colonizers) gain an advantage. Control over interactions in the sense of being able to appropriate ‘surplus’ payoffs in each interaction, which is selected for within-guild and is equivalent to playing the role of responders, selects against high demands (and so for mutualism) in the guild with control. Combining the two mechanisms, a high degree of mutualism in both guilds and coexistence of more mutualistic and more exploitative strategies within each are both consistent with control over the interaction being highly skewed toward one side that does what is in its own short-term interests.