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.     

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.     

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.     

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.     

Exclusive rewards in mutualisms: ant proteases and plant protease inhibitors create a lock–key system to protect Acacia food bodies from exploitation

Myrmecophytic Acacia species produce food bodies (FBs) to nourish ants of the Pseudomyrmex ferrugineus group, with which they live in an obligate mutualism. We investigated how the FBs are protected from exploiting nonmutualists. Two‐dimensional gel electrophoresis of the FB proteomes and consecutive protein sequencing indicated the presence of several Kunitz‐type protease inhibitors (PIs). PIs extracted from Acacia FBs were biologically active, as they effectively reduced the trypsin‐like and elastase‐like proteolytic activity in the guts of seed‐feeding beetles (Prostephanus truncatus and Zabrotes subfasciatus), which were used as nonadapted herbivores representing potential exploiters. By contrast, the legitimate mutualistic consumers maintained high proteolytic activity dominated by chymotrypsin 1, which was insensitive to the FB PIs. Larvae of an exploiter ant (Pseudomyrmex gracilis) taken from Acacia hosts exhibited lower overall proteolytic activity than the mutualists. The proteases of this exploiter exhibited mainly elastase‐like and to a lower degree chymotrypsin 1‐like activity. We conclude that the mutualist ants possess specifically those proteases that are least sensitive to the PIs in their specific food source, whereas the congeneric exploiter ant appears partly, but not completely, adapted to consume Acacia FBs. By contrast, any consumption of the FBs by nonadapted exploiters would effectively inhibit their digestive capacities. We suggest that the term ‘exclusive rewards’ can be used to describe situations similar to the one that has evolved in myrmecophytic Acacia species, which reward mutualists with FBs but safeguard the reward from exploitation by generalists by making the FBs difficult for the nonadapted consumer to use.     

Adaptation in a hybrid world with multiple interaction types: a new mechanism for species coexistence

In ecological communities, numerous species coexist and affect each others’ population levels via various types of interspecific interactions. Previous ecological theory explaining multispecies coexistence tended to focus on a single interaction type, such as antagonism, competition, or mutualism, and its consequences on population dynamics. Hence, it remains unclear what, if any, contribution multiple coexisting interaction types have on the multispecies coexistence. Here, we show that the coexistence of multiple interaction types can be essential for multispecies coexistence. We present a simple model in which the exploiter and mutualist adaptively switch between two competing resource species. An adaptive mutualist, which favors the more abundant species, provides a mechanism of majority-advantage and, thus, potentially inhibits the coexistence of resource species. In the absence of an exploiter, an adaptive mutualist leads to competitive exclusion at the resource species level. However, the coexistence of an adaptive exploiter and a mutualist allows the coexistence of all species in the community, because the mutualist-mediated “winner” tends to be suppressed by the adaptive exploiter. The mutualist indirectly increases the abundance of the exploiter through mutualistic interactions, thereby indirectly supporting this coexistence mechanism. In fact, coexistence may occur even if the exploiter or mutualist alone cannot mediate the coexistence of two resources. We conclude that the coexistence of mutualism and antagonism may be the key to the persistence of the four-species module in the presence of adaptive switching.     

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.     

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.     

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.     

Artificial neural networks in models of specialization, guild evolution and sympatric speciation

Sympatric speciation can arise as a result of disruptive selection with assortative mating as a pleiotropic by-product. Studies on host choice, employing artificial neural networks as models for the host recognition system in exploiters, illustrate how disruptive selection on host choice coupled with assortative mating can arise as a consequence of selection for specialization. Our studies demonstrate that a generalist exploiter population can evolve into a guild of specialists with an 'ideal free' frequency distribution across hosts. The ideal free distribution arises from variability in host suitability and density-dependent exploiter fitness on different host species. Specialists are less subject to inter-phenotypic competition than generalists and to harmful mutations that are common in generalists exploiting multiple hosts.When host signals used as cues by exploiters coevolve with exploiter recognition systems, our studies show that evolutionary changes may be continuous and cyclic. Selection changes back and forth between specialization and generalization in the exploiters, and weak and strong mimicry in the hosts, where non-defended hosts use the host investing in defence as a model. Thus, host signals and exploiter responses are engaged in a red-queen mimicry process that is ultimately cyclic rather then directional. In one phase, evolving signals of exploitable hosts mimic those of hosts less suitable for exploitation (i.e. the model). Signals in the model hosts also evolve through selection to escape the mimic and its exploiters. Response saturation constraints in the model hosts lead to the mimic hosts finally perfecting its mimicry, after which specialization in the exploiter guild is lost. This loss of exploiter specialization provides an opportunity for the model hosts to escape their mimics. Therefore, this cycle then repeats.We suggest that a species can readily evolve sympatrically when disruptive selection for specialization on hosts is the first step. In a sexual reproduction setting, partial reproductive isolation may first evolve by mate choice being confined to individuals on the same host. Secondly, this disruptive selection will favour assortative mate choice on genotype, thereby leading to increased reproductive isolation.     

Evolutionary origins and diversification of proteobacterial mutualists

Mutualistic bacteria infect most eukaryotic species in nearly every biome. Nonetheless, two dilemmas remain unresolved about bacterial–eukaryote mutualisms: how do mutualist phenotypes originate in bacterial lineages and to what degree do mutualists traits drive or hinder bacterial diversification? Here, we reconstructed the phylogeny of the hyperdiverse phylum Proteobacteria to investigate the origins and evolutionary diversification of mutualistic bacterial phenotypes. Our ancestral state reconstructions (ASRs) inferred a range of 34–39 independent origins of mutualist phenotypes in Proteobacteria, revealing the surprising frequency with which host-beneficial traits have evolved in this phylum. We found proteobacterial mutualists to be more often derived from parasitic than from free-living ancestors, consistent with the untested paradigm that bacterial mutualists most often evolve from pathogens. Strikingly, we inferred that mutualists exhibit a negative net diversification rate (speciation minus extinction), which suggests that mutualism evolves primarily via transitions from other states rather than diversification within mutualist taxa. Moreover, our ASRs infer that proteobacterial mutualist lineages exhibit a paucity of reversals to parasitism or to free-living status. This evolutionary conservatism of mutualism is contrary to long-standing theory, which predicts that selection should often favour mutants in microbial mutualist populations that exploit or abandon more slowly evolving eukaryotic hosts.     

Spatial Heterogeneity in Soil Microbes Alters Outcomes of Plant Competition

Plant species vary greatly in their responsiveness to nutritional soil mutualists, such as mycorrhizal fungi and rhizobia, and this responsiveness is associated with a trade-off in allocation to root structures for resource uptake. As a result, the outcome of plant competition can change with the density of mutualists, with microbe-responsive plant species having high competitive ability when mutualists are abundant and non-responsive plants having high competitive ability with low densities of mutualists. When responsive plant species also allow mutualists to grow to greater densities, changes in mutualist density can generate a positive feedback, reinforcing an initial advantage to either plant type. We study a model of mutualist-mediated competition to understand outcomes of plant-plant interactions within a patchy environment. We find that a microbe-responsive plant can exclude a non-responsive plant from some initial conditions, but it must do so across the landscape including in the microbe-free areas where it is a poorer competitor. Otherwise, the non-responsive plant will persist in both mutualist-free and mutualist-rich regions. We apply our general findings to two different biological scenarios: invasion of a non-responsive plant into an established microbe-responsive native population, and successional replacement of non-responders by microbe-responsive species. We find that resistance to invasion is greatest when seed dispersal by the native plant is modest and dispersal by the invader is greater. Nonetheless, a native plant that relies on microbial mutualists for competitive dominance may be particularly vulnerable to invasion because any disturbance that temporarily reduces its density or that of the mutualist creates a window for a non-responsive invader to establish dominance. We further find that the positive feedbacks from associations with beneficial soil microbes create resistance to successional turnover. Our theoretical results constitute an important first step toward developing a general understanding of the interplay between mutualism and competition in patchy landscapes, and generate qualitative predictions that may be tested in future empirical studies.     

Costs of two non-mutualistic species in a yucca/yucca moth mutualism

Mutualisms often involve significant costs for participants. Costs are inflicted by mutualists themselves, as well as by associated, non-mutualistic species. These costs are rarely quantified, however, particularly the ones extrinsic to the pairwise interaction. We compare costs inflicted by an obligate mutualist pollinator and two common exploiters of an Arizona yucca over a 2-year period. The magnitude of seed damage from seed and fruit-feeding beetle larvae (Carpophilus longus, Nitidulidae) was similar to damage from the seed-eating larvae of Yucca schottii's pollinator moth Tegeticula yuccasella (Prodoxidae), averaging about 15 seeds destroyed per fruit in each case. The two seed predators usually fed within the same fruits, although rarely side by side. In contrast, the presence of fruit-galling moth larvae (Prodoxusy-inversus, Prodoxidae) appeared to benefit the yucca: individual Tegeticula destroyed only half as many seeds in galled fruits as they did in ungalled fruits. We discuss three general implications of these results. Firstly, the costs of non-mutualists to the two mutualistic partners are not necessarily parallel. Secondly, measurable costs of non-mutualists do not necessarily translate into an impact on the success of the mutualism itself, because they may be incurred after mutualistic activities take place. Finally, the costs of mutualists to each other can differ substantially depending on the presence or absence of non-mutualistic species. Received:17 July 1996 / Accepted:10 June 1997     

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.     

Mutualism, market effects and partner control

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. The effectiveness of the threat of terminating an encounter, however, depends upon the ease with which both the potential victim and the potential exploiter can find replacement partners. Here, we extend a simple, game-theoretical model of this form of partner control to incorporate variation in the relative abundance of potential victims and exploiters, which leads to variation in the time required for individuals of each type to find a new partner. We show that such market effects have a dramatic influence on the stable level of exploitation (and consequent duration of interaction). As the relative abundance of victims decreases, they become less tolerant to exploitation, terminating encounters earlier (for a given level of exploitation), whereas exploiters behave in a more cooperative manner. As a result, the stable duration of interaction actually increases, despite the decreasing tolerance of the victims. Below a critical level of relative victim abundance, the model suggests that the cost of finding a replacement partner becomes so great that it does not pay to exploit at all.     

Evolution of mutualism through spatial effects

Mutualism among species is ubiquitous in natural ecosystems but its evolution is not well understood. We provided a simple lattice model to clarify the importance of spatial structure for the evolution of mutualism. We assumed reproductive rates of two species are modified through interaction between species and examine conditions where mutualists of both species, that give some benefit to the other species with their own cost, invade non-mutualists populations. When dispersal of offspring is unlimited, we verified the evolution of mutualism is impossible under any condition. On the other hand, when the dispersal is limited to neighboring lattice sites, mutualists can invade if the ratio of cost to benefit is low and the intrinsic reproductive rate is low in case where the parameter values are symmetric between species. Under the same conditions, non-mutualists cannot invade mutualist populations, that is, the latter are evolutionarily stable. In case of asymmetric parameters, mutualists tend to invade if the average value of costs to two species is low or that of benefits is high, and if the intrinsic reproductive rate is low for one of the two species. A mechanistic explanation of why mutualists increase when the dispersal is limited is given by showing that mutualist pairs of the two species at the same lattice site rapidly increase at the initial phase of the invasion.     

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.     

An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction

Mutualisms can be viewed as biological markets in which partners of different species exchange goods and services to their mutual benefit. Trade between partners with conflicting interests requires mechanisms to prevent exploitation. Partner choice theory proposes that individuals might foil exploiters by preferentially directing benefits to cooperative partners. Here, we test this theory in a wild legumerhizobium symbiosis. Rhizobial bacteria inhabit legume root nodules and convert atmospheric dinitrogen (N2) to a plant available form in exchange for photosynthates. Biological market theory suits this interaction because individual plants exchange resources with multiple rhizobia. Several authors have argued that microbial cooperation could be maintained if plants preferentially allocated resources to nodules harbouring cooperative rhizobial strains. It is well known that crop legumes nodulate non-fixing rhizobia, but allocate few resources to those nodules. However, this hypothesis has not been tested in wild legumes which encounter partners exhibiting natural, continuous variation in symbiotic benefit. Our greenhouse experiment with a wild legume, Lupinus arboreus, showed that although plants frequently hosted less cooperative strains, the nodules occupied by these strains were smaller. Our survey of wild-grown plants showed that larger nodules house more Bradyrhizobia, indicating that plants may prevent the spread of exploitation by favouring better cooperators.     

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 by obligate and facultative mutualists for partners in a shrimp-goby association

Mutualist species compete intra and inter-specifically for the resources provided by their partners. Because obligate mutualists are more reliant than facultative mutualists on the resources that their partners provide, they are expected to compete more strongly for those resources. Here, I examined interference competition in two goby fishes: Nes longus (an obligate mutualist) and Ctenogobius saepepallens (a facultative mutualist). Both gobies associate with the shrimp, Alpheus floridanus. Shrimp provide gobies with refuge from predators (a burrow in the sand), and gobies provide shrimp with a warning signal when predators are near. Using an aquarium experiment, I examined the behavior of a pair of gobies with access to a single shrimp burrow. I used four different goby pairings: large N. longus and small N. longus, large N. longus and small C. saepepallens, large C. saepepallens and small N. longus, and large C. saepepallens and small C. saepepallens. When paired with large N. longus individuals, small gobies of both species were less likely to occupy the single burrow than when paired with large C. saepepallens individuals. In addition, large N. longus individuals were less likely to co-occupy the single burrow with smaller gobies than were large C. saepepallens individuals. These results seem to indicate that large N. longus individuals exclude smaller gobies from burrows, while large C. saepepallens individuals do not. This study adds evidence to the supposition that obligate mutualists in general compete more strongly for mutualist partners than do facultative mutualists.