Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization

Mutualisms are ubiquitous in nature, as is their exploitation by both conspecific and heterospecific cheaters. Yet, evolutionary theory predicts that cheating should be favoured by natural selection. Here, we show theoretically that asymmetrical competition for partners generally determines the evolutionary fate of obligate mutualisms facing exploitation by third-species invaders. When asymmetry in partner competition is relatively weak, mutualists may either exclude exploiters or coexist with them, in which case their co-evolutionary response to exploitation is usually benign. When asymmetry is strong, the mutualists evolve towards evolutionary attractors where they become extremely vulnerable to exploiter invasion. However, exploiter invasion at an early stage of the mutualism's history can deflect mutualists' co-evolutionary trajectories towards slightly different attractors that confer long-term stability against further exploitation. Thus, coexistence of mutualists and exploiters may often involve an historical effect whereby exploiters are co-opted early in mutualism history and provide lasting 'evolutionary immunization' against further invasion.     

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.     

HOW TO PREVENT CHEATING: A DIGESTIVE SPECIALIZATION TIES MUTUALISTIC PLANT-ANTS TO THEIR ANT-PLANT PARTNERS

Mutualisms often involve reciprocal adaptations of both partners. Acacia ant-plants defended by symbiotic Pseudomyrmex ant mutualists secrete sucrose-free extrafloral nectar, which is unattractive to generalists. We aimed to investigate whether this extrafloral nectar can also exclude exploiters, that is nondefending ant species. Mutualist workers discriminated against sucrose whereas exploiters and generalists with no affinity toward Acacia myrmecophytes preferred sucrose, because mutualist workers lacked the sucrose-cleaving enzyme invertase, which is present in workers of the other two groups. Sucrose uptake induced invertase activity in workers of parasites and generalists, but not mutualists, and in larvae of all species: the mutualists loose invertase during their ontogeny. This reduced metabolic capacity ties the mutualists to their plant hosts, but it does not completely prevent the mutualism from exploitation. We therefore investigated whether the exploiters studied here are cheaters (i.e., have evolved from former mutualists) or parasites (exploiters with no mutualistic ancestor). A molecular phylogeny demonstrates that the exploiter species did not evolve from former mutualists, and no evidence for cheaters was found. We conclude that being specialized to their partner can prevent mutualists from becoming cheaters, whereas other mechanisms are required to stabilize a mutualism against the exploitation by parasites.     

Proteases hold the key to an exclusive mutualism

Mutualisms, cooperative interactions between species, generally involve an economic exchange: species exchange commodities that are cheap for them to provide, for ones that cannot be obtained affordably or at all. But these associations can only succeed if effective partners can be enticed to interact. In some mutualisms, partners can actively seek one another out. However, plants, which use mutualists for a wide array of essential life history functions, do not have this option. Instead, natural selection has repeatedly favoured the evolution of rewards – nutritional substances (such as sugar‐rich nectar and fleshy fruit) with which plants attract certain organisms whose feeding activities can then be co‐opted for their own benefit. The trouble with rewards, however, is that they are usually also attractive to organisms that confer no benefits at all. Losing rewards to ‘exploiters’ makes a plant immediately less attractive to the mutualists it requires; if the reward cannot be renewed quickly (or at all), then mutualistic service is precluded entirely. Thus, it is in plants' interests to either restrict rewards to only the most beneficial partners or somehow punish or deter exploiters. Yet, at least in cases where the rewards are highly nutritious, we can expect counter‐selection for exploiter traits that permit them to skirt such control. How, then, can mutualisms persist? In this issue, Orona‐Tamayo et al. ( 2013 ) describe a remarkable adaptation that safeguards one particularly costly reward from nonmutualists. Their study helps to explain the evolutionary success of an iconic interaction and illuminates one way in which mutualism as a whole can persist in the face of exploitation.     

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.     

Competition hierarchies among ants and predation by birds jointly determine the strength of multi‐species ant–aphid mutualisms

Protection mutualisms often involve multiple species of protector that vary in quality as mutualists. Because protectors may compete for access to mutualists, concordance between competitive ability and degree of benefit will determine the overall strength of multi‐species mutualisms. We compared the abilities of two similarly sized congener ants as competitors for, and mutualists of pine‐feeding aphids, and how insectivorous birds affected each ant–aphid mutualism. Formica planipilis and F. podzolica were indistinguishable in forager abundance, but the former was 13‐fold more abundant at competition baits and provided 11‐fold more benefits to aphids. These results highlight how, in a single environment, a great ecological distance can exist between two congener ants of similar size. Insectivorous birds disrupted the two mutualisms to a similar extent, reducing aphid and ant abundance by 91% and 39% respectively. Nevertheless, birds had an important influence on the relative benefits of the two ants to aphids: where F. planipilis consistently benefited aphids, F. podzolica only did so in the absence of birds. Consequently, the presence of insectivorous birds and ant species identity jointly determined whether ant–aphid mutualisms occurred in pine canopies and the strength of such interactions. Our study highlights the inter‐relatedness of competition, predation and mutualism, and how competition can serve to strengthen mutualism by filtering inferior mutualists.     

Kin selection and the Evolution of Mutualisms between Species

Hamilton's theory of kin selection has revolutionized and inspired fifty years of additional theories and experiments on social evolution. Whereas Hamilton's broader intent was to explain the evolutionary stability of cooperation, his focus on shared genetic history appears to have limited the application of his theory to populations within a single species rather than across interacting species. The evolutionary mechanisms for cooperation between species require both spatial and temporal correlations among interacting partners for the benefits to be not only predictable but of sufficient duration to be reliably delivered. As a consequence when the benefits returned by mutualistic partners are redirected to individuals other than the original donor, cooperation usually becomes unstable and parasitism may evolve. However, theoretically, such redirection of mutualistic benefits may actually reinforce, rather than undermine, mutualisms between species when the recipients of these redirected benefits are genetically related to the original donor. Here, I review the few mathematical models that have used Hamilton's theory of kin selection to predict the evolution of mutualisms between species. I go on to examine the applicability of these models to the most well‐studied case of mutualism, pollinating seed predators, where the role of kin selection may have been previously overlooked. Future detailed studies of the direct, and indirect, benefits of mutualism are likely to reveal additional possibilities for applying Hamilton's theory of kin selection to mutualisms between species.     

The Benefits of Mutualism: A Conceptual Framework

There are three general mechanisms by which phenotypic benefits are transferred between unrelated organisms. First, one organism may purloin benefits from another by preying on or parasitizing the other organism. Second, one organism may enjoy benefits that are incidental to or a by-product of the self-serving traits of another organism. Third, an organism may invest in another organism if that investment produces return benefits which outweigh the cost of the investment. Interactions in which both parties gain a net benefit are mutualistic. The three mechanisms by which benefits are transferred between organisms can be combined in pairs to produce six possible kinds of original or 'basal' mutualisms that can arise from an amutualistic state. A review of the literature suggests that most or all interspecific mutualism have origins in three of the six possible kinds of basal mutualism. Each of these three basal mutualisms have byproduct benefits flowing in at least one direction. The transfer of by-product benefits and investment are common to both intra- and interspecific mutualisms, so that some interspecific mutualisms have intraspecific analogs. A basal mutualism may evolve to the point where each party invests in the other, sometimes obscuring the nature of the original interaction along the way. Two prominent models for the evolution of mutualism do not include by-product benefits: Roughgarden's model for the evolution of the damsel-fish anemone mutualism and the 'Tit-for-Tat' model of reciprocity. Using the conceptual framework presented here, including in particular by-product benefits, I have shown how it is possible to construct more parsimonious alternatives to both models.     

Temporal Structure in Cooperative Interactions: What Does the Timing of Exploitation Tell Us about Its Cost?

Exploitation in cooperative interactions both within and between species is widespread. Although it is assumed to be costly to be exploited, mechanisms to control exploitation are surprisingly rare, making the persistence of cooperation a fundamental paradox in evolutionary biology and ecology. Focusing on between-species cooperation (mutualism), we hypothesize that the temporal sequence in which exploitation occurs relative to cooperation affects its net costs and argue that this can help explain when and where control mechanisms are observed in nature. Our principal prediction is that when exploitation occurs late relative to cooperation, there should be little selection to limit its effects (analogous to “tolerated theft” in human cooperative groups). Although we focus on cases in which mutualists and exploiters are different individuals (of the same or different species), our inferences can readily be extended to cases in which individuals exhibit mixed cooperative-exploitative strategies. We demonstrate that temporal structure should be considered alongside spatial structure as an important process affecting the evolution of cooperation. We also provide testable predictions to guide future empirical research on interspecific as well as intraspecific cooperation.     

Mutualisms in a changing world: an evolutionary perspective

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

Limiting cheaters in mutualism: evidence from hybridization between mutualist and cheater yucca moths

Mutualisms are balanced antagonistic interactions where both species gain a net benefit. Because mutualisms generate resources, they can be exploited by individuals that reap the benefits of the interaction without paying any cost. The presence of such 'cheaters' may have important consequences, yet we are only beginning to understand how cheaters evolve from mutualists and how their evolution may be curtailed within mutualistic lineages. The yucca-yucca moth pollination mutualism is an excellent model in this context as there have been two origins of cheating from within the yucca moth lineage. We used nuclear and mitochondrial DNA markers to examine genetic structure in a moth population where a cheater species is parapatric with a resident pollinator. The results revealed extensive hybridization between pollinators and cheaters. Hybrids were genetically intermediate to parental populations, even though all individuals in this population had a pollinator phenotype. The results suggest that mutualisms can be stable in the face of introgression of cheater genes and that the ability of cheaters to invade a given mutualism may be more limited than previously appreciated.     

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.     

Invasive mutualists erode native pollination webs

Plant–animal mutualisms are characterized by weak or asymmetric mutual dependences between interacting species, a feature that could increase community stability. If invasive species integrate into mutualistic webs, they may alter web structure, with consequences for species persistence. However, the effect of alien mutualists on the architecture of plant–pollinator webs remains largely unexplored. We analyzed the extent of mutual dependency between interacting species, as a measure of mutualism strength, and the connectivity of 10 paired plant–pollinator webs, eight from forests of the southern Andes and two from oceanic islands, with different incidences of alien species. Highly invaded webs exhibited weaker mutualism than less-invaded webs. This potential increase in network stability was the result of a disproportionate increase in the importance and participation of alien species in the most asymmetric interactions. The integration of alien mutualists did not alter overall network connectivity, but links were transferred from generalist native species to super-generalist alien species during invasion. Therefore, connectivity among native species declined in highly invaded webs. These modifications in the structure of pollination webs, due to dominance of alien mutualists, can leave many native species subject to novel ecological and evolutionary dynamics.     

The evolution of plant-insect mutualisms

Mutualisms (cooperative interactions between species) have had a central role in the generation and maintenance of life on earth. Insects and plants are involved in diverse forms of mutualism. Here we review evolutionary features of three prominent insect-plant mutualisms: pollination, protection and seed dispersal. We focus on addressing five central phenomena: evolutionary origins and maintenance of mutualism; the evolution of mutualistic traits; the evolution of specialization and generalization; coevolutionary processes; and the existence of cheating. Several features uniting very diverse insect-plant mutualisms are identified and their evolutionary implications are discussed: the involvement of one mobile and one sedentary partner; natural selection on plant rewards; the existence of a continuum from specialization to generalization; and the ubiquity of cheating, particularly on the part of insects. Plant-insect mutualisms have apparently both arisen and been lost repeatedly. Many adaptive hypotheses have been proposed to explain these transitions, and it is unlikely that any one of them dominates across interactions differing so widely in natural history. Evolutionary theory has a potentially important, but as yet largely unfilled, role to play in explaining the origins, maintenance, breakdown and evolution of insect-plant mutualisms.     

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.     

Cheating and the evolutionary stability of mutualisms

Interspecific mutualisms have been playing a central role in the functioning of all ecosystems since the early history of life. Yet the theory of coevolution of mutualists is virtually nonexistent, by contrast with well-developed coevolutionary theories of competition, predator-prey and host-parasite interactions. This has prevented resolution of a basic puzzle posed by mutualisms: their persistence in spite of apparent evolutionary instability. The selective advantage of 'cheating', that is, reaping mutualistic benefits while providing fewer commodities to the partner species, is commonly believed to erode a mutualistic interaction, leading to its dissolution or reciprocal extinction. However, recent empirical findings indicate that stable associations of mutualists and cheaters have existed over long evolutionary periods. Here, we show that asymmetrical competition within species for the commodities offered by mutualistic partners provides a simple and testable ecological mechanism that can account for the long-term persistence of mutualisms. Cheating, in effect, establishes a background against which better mutualists can display any competitive superiority. This can lead to the coexistence and divergence of mutualist and cheater phenotypes, as well as to the coexistence of ecologically similar, but unrelated mutualists and cheaters.     

Benefits and costs of floral visitors to Chilopsis linearis: pollen deposition and stigma closure

In pollination mutualisms, nectar-robbers are usually considered antagonists; visitors that enter flowers (legitimate visitors) are usually considered mutualists. However, nectar-robbers may provide some benefits to plants, whereas legitimate visitors may inflict some costs. The costs and benefits of floral visitors to Chilopsis linearis (desert willow) were compared by number of pollen grains deposited and their effect on stigmas. Because these plants are self-incompatible and pollen-limited, they depend on visitors for services by pollinators to reproduce. On a per-visit basis, only one legitimate visitor, Bombus sonorus (bumblebees) generally benefited plants in terms of pollen deposition. However, no species of visitor was consistently beneficial; every one was at least sometimes ineffective in terms of pollen deposition. Chilopsis had sensitive stigmas that closed immediately upon touch and sometimes reopened later. Whether stigmas remained permanently closed or reopened depended on number of pollen grains deposited and tended also to be affected by source either, outcross or self. Legitimate visitors sometimes cost plants by causing stigma closure without depositing enough pollen to set a fruit. When abundant, a visitor such as Apis mellifera (honeybees) that was only occasionally beneficial on a per-visit basis may have provided a greater benefit to plants as a population than a more effective, but rare visitor. In contrast, nectar-robbers did not benefit plants by depositing pollen grains, but they also did not inflict costs on plants by causing stigmas to close without adequate pollen. There are two general implications of these results. First, individuals of species that appear to be mutualists can vary greatly in the benefits that they give to their partners. Second, apparent mutualists can inflict costs on plants that apparent exploiters (nectar-robbers) do not.     

An orb‐weaver spider exploits an ant–acacia mutualism for enemy‐free space

Exploiters of protection mutualisms are assumed to represent an important threat for the stability of those mutualisms, but empirical evidence for the commonness or relevance of exploiters is limited. Here, I describe results from a manipulative study showing that an orb‐weaver spider, Eustala oblonga, inhabits an ant‐acacia for protection from predators. This spider is unique in the orb‐weaver family in that it associates closely with both a specific host plant and ants. I tested the protective effect of acacia ants on E. oblonga by comparing spider abundance over time on acacias with ants and on acacias from which entire ant colonies were experimentally removed. Both juvenile and adult spider abundance significantly decreased over time on acacias without ants. Concomitantly, the combined abundance of potential spider predators increased over time on acacias without ants. These results suggest that ant protection of the ant‐acacia Acacia melanocerus also protects the spiders, thus supporting the hypothesis that E. oblonga exploits the ant–acacia mutualism for enemy‐free space. Although E. oblonga takes advantage of the protection services of ants, it likely exacts little to no cost and should not threaten the stability of the ant–acacia mutualism. Indeed, the potential threat of exploiter species to protection mutualisms in general may be limited to species that exploit the material rewards traded in such mutualisms rather than the protection services.     

The Costs of Mutualism

Mutualisms are of central importance in biological systems.Despite growing attention in recent years, however, few conceptualthemes have yet to be identified that span mutualisms differingin natural history. Here I examine the idea that the ecologyand evolution of mutualisms are shaped by diverse costs, notonly by the benefits they confer. This concept helps link mutualismto antagonisms such as herbivory, predation, and parasitism,interactions defined largely by the existence of costs. I firstbriefly review the range of costs associated with mutualisms,then describe how one cost, the consumption of seeds by pollinatoroffspring, was quantified for one fig/pollinator mutualism.I compare this cost to published values for other fig/pollinatormutualisms and for other kinds of pollinating seed parasitemutualisms, notably the yucca/yucca moth interaction. I thendiscuss four issues that fundamentally complicate comparativestudies of the cost of mutualism: problems of knowing how tomeasure the magnitude of any one cost accurately; problems associatedwith using average estimates in the absence of data on sourcesof variation; complications arising from the complex correlatesof costs, such as functional linkages between costs and benefits;and problems that arise from considering the cost of mutualismas a unilateral issue in what is fundamentally a reciprocalinteraction. The rich diversity of as-yet unaddressed questionssurrounding the costs of mutualism may best be investigatedvia detailed studies of individual interactions.     

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.