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Keywords:

  • competition;
  • consumer–resource;
  • mutualism;
  • partner control

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Competition and mutualism: empirical phenomena
  5. Mechanisms of competitive asymmetry among mutualists: the cooperation–competition trade-off
  6. Mutualism and competition: evolutionary implications
  7. Conclusions
  8. Acknowledgments
  9. Conflicts of interest
  10. References

Abstract  Mutualisms are interspecific interactions that yield reciprocal benefits. Here, by adopting a consumer–resource perspective, we show how considering competition is necessary in order to understand the evolutionary and ecological dynamics of mutualism. We first review the ways in which competition shapes the ecology of mutualisms, using a graphical framework based on resource flows rather than net effects to highlight the opportunities for competition. We then describe the known mechanisms of competition and show how it is a critical driver of the evolutionary dynamics, persistence, and diversification of mutualism. We argue that empirical and theoretical research on the ecology and evolution of mutualisms will jointly progress by addressing four key points: (i) the existence and shape of physiological trade-offs among cooperation, competition, and other life-history and functional traits; (ii) the capacity for individuals to express conditional responses to variation in their mutualistic and competitive environment; (iii) the existence of heritable variation for mutualistic and competitive traits and their potentially conditional expression; and (iv) the structure of the network of consumer–resource interactions in which individuals are embedded.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Competition and mutualism: empirical phenomena
  5. Mechanisms of competitive asymmetry among mutualists: the cooperation–competition trade-off
  6. Mutualism and competition: evolutionary implications
  7. Conclusions
  8. Acknowledgments
  9. Conflicts of interest
  10. References

The study of mutualism (cooperative interactions between pairs of species) has grown rapidly in recent years. Not only are diverse cases of mutualism now understood in fine detail, but many of the largest conceptual issues surrounding their ecology and evolution are now clearly identified. With regard to evolution, five issues have been treated in particular depth.1 What are the evolutionary origins of mutualism and when and how is it maintained once it arises? How do mutualistic traits evolve? Why is there a continuum between specialized and more generalized mutualisms, and to what extent do these arise and evolve by different processes? When and how do mutualistic partners coevolve? Finally, how can mutualism (or any other form of cooperation) persist in the face of the “temptation to cheat”?

Great progress has been made in studying all of these issues. A significant factor in this progress has been the emergence of a unifying conceptual framework, developed by Holland and collaborators, in which mutualisms are viewed as consumer–resource interactions.2 In the large majority of cases, the resource provided by one species is some kind of service to its partner; the resource provided in return is a reward.3 Services are often behaviors, such as the transport of pollen between flowers by pollinators, the movement of seeds to good germination places by seed dispersers, and protection from predators and parasites by pugnacious ants. The corresponding rewards exchanged for these services are usually nectar (from plants whose pollen is transported), sugar-rich fruit (from plants whose seeds are dispersed), and nutritional secretions (from insects and plants that ants guard). Each of these is a complex exchange that may have a long evolutionary or coevolutionary history, may vary greatly in magnitude in space and time, and may be embedded in a community of other interactors. Recognizing this rich detail is critical to understanding how and when mutualisms arise, persist, and break down. However, it is simulaneously important not to become lost in system-specific details. The framework of consumer–resource interactions provides a powerful unifying approach to tackle general issues across the diversity of mutualisms.

Competition is central to our understanding of consumer–resource interactions. Treating mutualisms as consumer–resource interactions (e.g., Refs. 2 and 4) thus places competition at the core of processes that shape the ecology and evolution of mutualists. The best documented interplay between competition and mutualism is that there is competition for the commodities mutualists produce; gaining access to mutualists in turn can change competitive outcomes. There are a number of distinct ways in which competition for mutualistic resources can occur and can influence the ecological and evolutionary dynamics of mutualism. For example, there may or may not be a predictable hierarchy of competitive dominance among potential partners,5 or there may be a range of situations in which competitors actually benefit each other (via shared attraction of partners) rather than interfere.6 Competition thus lies at the heart of selection to attract, retain, and benefit from mutualisms. However, although it is widely recognized that organisms compete for mutualists, the strength and consistency of such competition are rarely measured (but see Refs. 7–10). Indeed, it is often more an assumption than fact that competition for mutualists exists and can drive the evolution of traits that attract and reward partners.

Competition interacts with mutualism in other ways as well. It can occur between mutualistic and nonmutualistic (exploitative) partners for a shared resource; mutualism can involve putative competitors; and competitive advantage can arise as a benefit conferred by mutualists. The diverse ways in which competition and mutualism interact has been given surprisingly little focused attention. On the theoretical side, competition is generally present within models of ecological and evolutionary dynamics of mutualism; however, with relatively few exceptions (e.g., Refs. 11–14), its role is not much remarked upon. Palmer et al. provided an outstanding overview of the ways in which competition mediates mutualist coexistence,15 but their perspective was largely descriptive and ecological. Here, we will argue that the existence of competition and of a competitive hierarchy among partners is critical to the outcome of mutualism at both ecological and evolutionary scales.

The structure of the paper is as follows. First, we synthesize the empirical literature on how competitive interactions are embedded within mutualism. To do this, we develop a novel graphical approach, built on the consumer–resource approach to mutualism. We then build on these ecological models to explore evolutionary aspects of the mutualism/competition interplay. We focus on the consequences and evolution of partner control mechanisms, then the factors fostering the evolution, persistence, and diversification of mutualism. We show how advancing our understanding of these issues requires knowledge of how competitive forces underlie mutualism. Finally, we identify intriguing evolutionary questions lying at the intersection of mutualism and competition that our approach could in the future be used to explore.

Competition and mutualism: empirical phenomena

  1. Top of page
  2. Abstract
  3. Introduction
  4. Competition and mutualism: empirical phenomena
  5. Mechanisms of competitive asymmetry among mutualists: the cooperation–competition trade-off
  6. Mutualism and competition: evolutionary implications
  7. Conclusions
  8. Acknowledgments
  9. Conflicts of interest
  10. References

Competition for mutualistic resources

Since mutualisms are defined as interactions that confer reciprocal benefits to two species, they are widely depicted as shown in Figure 1A. The partners are linked by positively labeled arrows, the top arrow in the figure indicating that species M1 confers benefits to M2, and the bottom arrow indicating that M2 confers benefits to M1. This abstraction of mutualism hides as much as it reveals, however. What are these benefits and is the exchange as simple and reciprocal as the figure might imply?

image

Figure 1. Competition for mutualistic resources. (A) The traditional net effects diagram of mutualism. The arrows show the net reciprocal benefits (+/+) of the interaction between two mutualistic species (M1 and M2). (B) A resource-based diagram of mutualism. Mutualists M1 and M2 produce resources R1 and R2, respectively, and consume the resource produced by the partner mutualist. The arrows show resource production (black) and resource consumption (red). (C) Mutualism when low-quality mutualists have a competitive advantage. M1 has now been decomposed into two individuals or two species from a mutualist guild (M1a and M1b). M1a is a better mutualist since it offers a large amount of resources to M2 (thick arrow from M1a to R1). However, M1b is a better competitor for the resources produced by M2 (thick arrow from R2 to M1b). Here, the competitive advantage comes from interference competition (dashed inhibition arrow between M1b and M1a's R2 consumption arrow). (D) Mutualism when high-quality mutualists have a competitive advantage. Again, M1a is a better mutualist by producing large amounts of R1. However, it is now a better competitor for R2 (thick arrow from R2 to M1a). In this case, the competitive advantage results from partner control by M2 (dashed inhibition arrow between M2 and M1b's R2 consumption arrow).

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Figure 1A illustrates the effects of a single bout of commodity exchange, but not its underlying mechanism. While not shown here, competition can be included quantitatively in net effects diagrams through path coefficients.16 Stanton's use of path analysis to quantify the interactions between and within guilds of mutualists was an important step in extending the study of mutualism beyond pairs of species. However, path analysis is still a top-down, phenomenological approach that does not identify the causes of the measured effects. In contrast, in Figure 1B, we try to capture more of the mechanism of commodity exchange underlying mutualism through a bottom-up depiction. Now, instead of the arrows connecting two species, the arrows point to a commodity that is then delivered to the partner. These commodities may be, in the language used above, either rewards or services; we group these into a single category, called resources (R). While we recognize their differences, we take this approach because in the context of exchange, they share two critical features: rewards and services both can be costly to offer to partners, and both can be competed for. In Figure 1B, there are still two species (M1 and M2), but now there are also two resources, R1 and R2; the arrows now are resource flows rather than (as in Fig. 1A) net effects. Black arrows indicate resources produced by a mutualist, and red arrows those that are consumed (either actually or metaphorically) by a mutualist. Thus, in Figure 1B, M1 produces R1, a resource that is consumed by M2; M2 in turn produces R2, a resource that is consumed by M1. As an example, M1 might be a plant that produces nectar (R1), which is consumed by M2, a bee, that produces the resource of pollen transport (R2) that is used profitably by M1.

A major advantage to depicting mutualism as shown in Figure 1B rather than Figure 1A is that it makes clear how competition can lie at the heart of these interactions. In Figure 1A, it is not evident what could be competed for; in Figure 1B, it is clear that it is the resources, R1 and R2. Indeed, the best documented way in which there is interplay between competition and mutualism is that there is competition for the commodities mutualists produce. Consider pollination, the most thoroughly studied mutualism. Floral visitors are well documented to compete intraspecifically for nectar, for example, by adjusting their foraging routes in relation to the activities of conspecifics on flowers.17,18 Competition may also pit individuals of different species against one another, a phenomenon particularly well-investigated between honeybees and native bees that they may be displacing.19 On the other side of the interaction, it is common for plants to fiercely compete both intraspecifically and interspecifically for pollinators, as Mitchell et al. have thoroughly reviewed;20 competition for pollination has clearly shaped the evolution of flower sizes and numbers, floral reward chemistry and volume, and both visual and olfactory cues.20–23

Adding competition for resources explicitly into Figure 1B yields many possible outcomes, two of which are shown in Figure 1C and D. First, we decompose one mutualist (M1) into multiple individuals or species; we will explore how these entities (e.g., different pollinator individuals or species, or different nectar-producing plant individuals or species) compete for mutualistic resources. We will call these M1a and M1b. These two entities consume a shared resource, R2, and both produce a second resource, R1. Via these resources, both interact with a partner species, M2. However, M1a and M1b are not identical. The different thicknesses of the lines from M1a and M1b to R1 indicate that one entity produces more of R1 than does the other. Similarly, the different thicknesses of the lines from R2 to M1a and M1b indicate that one entity consumes more of R2 than does the other.

Figure 1C illustrates the situation in which a superior competitor is an inferior mutualist and competitive interactions play out in a way likely to be harmful to the shared partner. In Figure 1C, M1b provides less of R1 to the shared partner M2; thus, we define it as an inferior mutualist. However, M1b uses more of R2 than does the superior mutualist, M1a. M1a's lower consumption of R2 is due in some way to the presence of M1b: M1b might be actively interfering with M1a's consumption, or it may simply be consuming R2 faster or more efficiently, leaving less behind. We illustrate this effect with a dashed inhibition arrow running from the superior competitor M1b to the arrow connecting the shared resource R2 to M1a. To put this in words, the shared partner is stuck with a relatively low-quality mutualist able to reduce the success of better-quality mutualists. (This is quite realistic biologically. For example, Bennett and Bever demonstrated that the most beneficial mycorrhizal fungus species for Plantago lanceolata is the worst competitor for root space, whereas the worst fungal mutualist is the best competitor for P. lanceolata roots.9) This is a situation that might lead to the low-quality mutualist dropping resource provision altogether and becoming an exploiter of the system, leading one to question how mutualisms embodying this structure are able to persist evolutionarily. We discuss this in more detail below.

In Figure 1D, we illustrate the situation in which it is the superior mutualist that holds the competitive advantage. In contrast to the situation shown in Figure 1C, this can clearly benefit the shared partner. Here, M1a, the mutualist that consumes more of the shared resource R2, also provides more of resource R1 to the partner species M2. We have illustrated this outcome as being the result of actions of M2: it has exerted some kind of “partner control” that reduces the ability of the inferior mutualist M1b to compete for the resources it provides. This situation has been argued to permit mutualisms to persist in the presence of cheaters, as we discuss below. As in the case shown in Figure 1C, it is not difficult to identify biological examples of these relationships. Adam documented such a case in the interaction between cleaner fish and their “clients.”10 Clients (butterflyfish) are able to selectively associate with cleaners (wrasses) that provide them with the highest quality service (parasite removal). Thus, clients confer a competitive advantage to the best cleaners. Indeed, cleaners provide better service when competitors are present as this is the only way that they will be chosen by hosts.

Figure 1C and D are only two possible types of competitive interactions within guilds of interacting mutualists. Many other networks can be envisioned, and indeed are well documented in the literature. For example, we have not considered here that competitive advantage and mutualistic quality can both be functions of population size, and thus can vary over ecological time scales (e.g., Refs. 24 and 25). There is clearly much more to explore. Our overall point is simply that making the resource exchange underlying mutualism explicit (Fig. 1B), and clarifying which of these resources are competed for, which partners hold the competitive advantage, and which are the best mutualists (Fig. 1C and D), reveal a fascinating range of possible ecological and evolutionary ramifications that are completely obscured in the simple, standard net effects-based way of viewing mutualisms (Fig. 1A).

Competition between mutualists and exploiters

Almost all mutualisms are afflicted with individuals and species that gain the benefits that mutualism offers, while investing little or nothing in return.26–28 A perennial question about mutualism is how it can persist ecologically and evolutionarily in the face of these organisms (hereafter, exploiters) that would seem to be at an advantage. To answer this question, it is essential to think beyond the comparative effects of exploiters and mutualists on their shared partners. These are relatively well studied. One also needs to consider the nature and outcome of competition between exploiters and the species that share that partner. This issue has barely been addressed in the growing literature on cheating within mutualism (but see, for instance, Refs. 13 and 29–31).

First, it is necessary to illustrate the interactions in question, as we did in Figure 1, for mutualisms in the absence of exploitation. Parallel to Figure 1A, Figure 2A gives the standard, net effects-based illustration of a mutualism that is associated with an exploiter, E. The arrows are labeled to indicate that E benefits from M1 but is detrimental to it, and that E and M2 are detrimental to each other (since they share a partner). A well-known example is the well-studied network of interactions among plants, pollinators, and nectar-robbers, floral visitors that feed on nectar but do not pick up or deposit pollen.32 Nectar-robbers (E) and pollinators (M2) both interact with plants (M1), but only M2 confers a benefit to M1. As in Figure 1A, no mechanisms are shown.

image

Figure 2. Competition between mutualists and exploiters. (A) A net effects diagram. The core mutualism between M1 and M2 is the same as in Figure 1A. An exploiter (E) has been added. E gains a benefit (+) from M1, but inflicts a net cost (–) on M1, since E does not reciprocate any benefit. Both E and M2 gain benefits from M1, thus they are competitors (–/–) for these benefits. (B) A resource-based diagram. The core mutualism is the same as in Figure 1B. The added species, E, does not produce any resources. However, E consumes R1 thereby competing with M2 for this resource. (C) Exploited mutualism when the exploiter has a competitive advantage. E is a better competitor for R1. Here, the competitive advantage comes from interference competition. (D) Exploited mutualism when partner control gives a competitive advantage to the mutualistic partner. M2 is able to gain more of R1 due to partner control by M1. (E) Exploited mutualism when mutualists are superior competitors. Again, M2 is able to gain more of R1; however, it is now because M2 interferes directly with E. For the resource-based diagrams, (B–E), arrows represent resource production (black arrows), resource consumption (red arrows), increased resource production or consumption (thick arrows), and interference with resource consumption (dashed inhibition arrows).

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The other panels in Figure 2 take a resource-exchange rather than a net effects-based approach to these interactions, as did Figure 1B–D. The resources of exchange are added into Figure 2B, parallel to Figure 1B. Note that the M1-R1-M2-R2 network in Figure 2B is identical to that shown in Figure 1B. However, an exploiter species has now been added. Like M2, E consumes the resource R1, but unlike M2, it does not provide the resource R2 to the partner M1. Interestingly, moving to a resource-exchange perspective has served to simplify the net effects depiction (Fig. 2A) by making it clear what it is that species share, exchange, and compete for. In the case of plant—pollinator–nectar-robber interactions, for example, Figure 2B clarifies that pollinators (M2) and nectar-robbers (E) both utilize a resource, nectar (R1), but that only pollinators deliver a resource (R2), pollen transport, to the shared partner.

Parallel to Figure 1C and D, Figure 2C–E shows distinct ways in which competition for a resource shared between a mutualist and exploiter can occur and be mediated. Each suggests distinct ecological and evolutionary outcomes, and each captures a phenomenon represented in the empirical literature.

In Figure 2C, the exploiter is competitively superior at obtaining the resource from the shared mutualist. (We refer readers to the discussion of Figure 1C for an explanation of how to read these effects based on the colors, arrow thicknesses, and arrow patterns.) This gives rise to a situation in which mutualists can potentially be competitively excluded by exploiters, raising the obvious question of if and how mutualism can persist under these conditions. Examples can be found in nature. For example, Dohzono et al. studied a case in which a nectar-robbing bumble bee, Bombus terrestris, competes with native pollinating bumble bees for a shared nectar-producing plant, Corydalis ambigua, in Japan.33 Once nectar-robbers are present, pollinators abandon C. ambigua for other nectar resources, to the detriment of the plant. It is interesting that in this case, the exploiter is an introduced species. Will this plant, or at least its mutualism with native pollinators, be able to persist over the long term? This is more than an abstract evolutionary question. It highlights that an understanding of competitive hierarchies among native and introduced species may shed light on the conditions under which mutualisms will be able to persist and evolve in the face of anthropogenic change.34

Figure 2C may thus seem to be an ecologically and evolutionarily fragile situation for mutualism. However, close study of several mutualist–exploiter interactions has revealed that the shared partner has some ability to control the exploiter in a way that shifts the competitive advantage toward the mutualistic partner. We illustrate this general situation in Figure 2D. As a biological example, Kiers and colleagues have elegantly demonstrated that plants are able to discriminate among and differentially deliver resources to symbiotic Rhizobium bacteria that produce relatively more fixed nitrogen for them;35,36 similar control mechanisms may exist within other plant rhizosphere mutualisms.37 A wide variety of control mechanisms have been suggested under various names (e.g., sanctions, punishment, and partner choice). Given the potential importance of these mechanisms in allowing mutualism to persist in the face of exploitation, a large body of theory has been developed to examine when each mechanism is likely to evolve and how it would function (e.g., Refs. 27 and 38–40). We consider this issue in more depth below.

It is clear, however, that partner control mechanisms are not always necessary to explain how competing mutualists and exploiters are able to coexist. One obvious case is when it is the mutualist rather than the exploiter that holds an innate competitive advantage. This situation is illustrated in Figure 2E. Good empirical evidence comes from mutualisms between certain tropical plants and the highly specialized ants that inhabit them. Some of these ants are mutualistic, aggressively defending their plants from herbivore attack, whereas others occupy the plant and provide no defense. Exploiter ants have in several cases been reported to be competitively inferior to mutualistic ants; when mutualists invade a plant that exploiters occupy, it is commonly the exploiters that are displaced.41,42 Their superior ability to locate unoccupied plants results in a competition–colonization trade-off that allows them to persist even in the face of their evident disadvantage when challenged.41,42 Furthermore, certain mutualistic ants possess dietary specializations that allow them to more efficiently use the food that plants provide them.29,31 Of course, it is possible that the chemical makeup of this resource has evolved as a partner-control mechanism that shifts the competitive balance toward mutualists, illustrating that it can be difficult to empirically distinguish interaction networks as similar as those shown in Figure 2D and E.

Thus, to understand when we would expect to see the evolution of sanctions and punishments in mutualisms afflicted with exploitation, it is critical to examine whether exploiters hold a competitive advantage over the mutualists with which they share a resource, or vice versa. This has only rarely been investigated. The usual assumption has been that control mechanisms are always essential for mutualism to persist in the face of exploitation.

Competition between mutualists

In the previous two sections, we have considered the two best understood ways in which competition and mutualism interact: when individuals or species compete for resources provided by a shared mutualist and when mutualists and exploiters compete for resources from a shared partner. A much less studied phenomenon is when mutualistic partners are also competitors for resources. When mutualists occupy different trophic levels, as is generally the case,2 resource sharing is not expected. Thus, for instance, plants and pollinators do not share and compete for resources, nor do ants and the plants they defend. However, a number of less well-known mutualisms involve species that occupy the same trophic level and thus are likely to compete for access to shared resources.43 Müllerian mimicry in butterflies provides a good illustration. In these cases, mutual benefit is derived by a shared resemblance that “trains” predators to recognize them and, because they are distasteful or toxic, to avoid consuming them (e.g., Ref. 44). These individuals are likely to compete for food and other resources, however. A similar situation can be found in interspecific group foraging: individuals benefit either by shared predator vigilance or by increased access to food.45,46 However, they also may compete for the food they locate.47

We know of no standard way of illustrating these relationships via net effects arrows as in Figures 1A and 2A. We attempt to do this in Figure 3A. Here, the arrows are labeled +/– because the partners are simultaneously competing (hence, are in a minus/minus interaction) and benefiting each other (hence, are in a plus/plus interaction). This is not very satisfying. The difficulty of finding a way to illustrate these interactions is symptomatic of a general problem with using net effects to capture them: mutualism and competition occur simultaneously, and whether they add up to net effects that are positive for one, both, or neither partner is likely dependent on many system-specific and context-dependent factors.48 Path coefficients could be used to quantify the net effects;16 however, the individual contributions of mutualism and competition would be lost, making it difficult to translate the relationship into a mechanistic model.

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Figure 3. Competition between mutualists. (A) A net effects diagram. M1 and M2 are simultaneously engaged in mutualism (+/+) and competition (–/–). The true net effects could be either positive or negative, depending on whether mutualism or competition dominates, respectively. (B) A resource-based diagram. The core mutualism is the same as in Figure 1B. There is now also a third resource (R3) that is consumed by both M1 and M2. (C) Asymmetric competition between mutualists. M1 is a better competitor for the shared resource and interferes with consumption of R3 by M2. While not explicitly shown, competition for R3 could change production of the mutualistic resources, R1 and R2. For the resource-based diagrams, (B, C), arrows represent resource production (black arrows), resource consumption (red arrows), increased resource consumption (thick arrow), and interference with resource consumption (dashed inhibition arrow).

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These interactions are much more effectively captured once resources are illustrated explicitly, as seen in Figure 3B. Now it is clear that M1 and M2 interact mutualistically via resources R1 and R2, exactly as in Figures 1B and 2B. What is different here is that there is a third resource, R3, for which M1 and M2 compete. To frame the group foraging example described above in these terms, investment of time and energy into predator vigilance might be the resource of exchange. Indeed, the resources R1 and R2 are in this case the same thing. R3 in this example might be a shared food resource.

The central question for understanding the persistence of mutualism in this scenario is when the magnitude of competition will outweigh the magnitude of mutualism or vice versa, and, if competition is stronger, what the fate of mutualism is likely to be. Clearly, we cannot project the evolutionary consequences for mutualism in an interaction network like this without explicitly considering and measuring competition.

Figure 3C illustrates one way in which competition could be manifest. In this case, M1 is the superior competitor for the shared resource, suppressing M2's use of it. When framed this way, the question about the persistence of mutualism becomes refocused as a question about the persistence of M2. Will the detriment M2 experiences from its reduced access to R3 outweigh the benefit it receives from M1, via the mutualistic component of their interaction? And, how will these combined effects feed back on M1? Competition could logically lead loose mutualisms of this type to dissolve as predicted in a model of Ranta et al.48

Relevant empirical data on these questions are few. Hino found that five of six bird species studied changed their foraging behavior when in mixed-species flocks compared to when foraging alone.49 Interestingly, feeding rates were higher in mixed flocks. Although this may indicate an absence of competition for food, and in fact an increase in food availability, the authors point out that it could also be an effect of kleptoparasitism or social learning, either of which could be the result of intense competition among species.

As in all previous cases we have described, our figures capture some but not all of the complexity of how competition and mutualism can interact. In Figure 3B, competition is for a resource extrinsic to mutualism (R3). However, competition may also occur between M1 and M2 for mutualistic resources (R1 and R2). For example, two studies in marine habitats have found that two fish species collaborate to locate food, but then appear to compete to consume it.47,50 To capture these and other complex competition–mutualism interactions (e.g., Ref. 51), some important modifications to our figures would be required. The ones we show, however, provide a starting point for how to conceptualize these phenomena.

Competitive advantage as a benefit of mutualism

The best studied benefits of mutualism are transportation (e.g., of pollen by pollinators), protection (e.g., of aphids by ants), and nutrition (e.g., of plants by Rhizobium bacteria). However, other mutualistic benefits are well documented. Among these are beneficial alterations of a partner's competitive environment, and this is the final intersection of mutualism and competition that we will consider. Here are two empirical examples. Hartnett et al. explored how competitive interactions among prairie plants might be mediated by mutualistic mycorrhizal fungi.52 They demonstrated that competitive dominance of one grass species, Andropogon gerardii, depends on it having access to mycorrhizae. Thus, in this case, a mutualist confers traits that give its partner a competitive advantage. As another example, Stachowicz and Hay studied interactions between herbivorous crabs and the coralline algae upon which they live.53 They showed that crabs feed upon fouling seaweeds that, if unchecked, would overgrow the coralline algae; the algae provide a place for crabs to live. In this case, then, a mutualist actively interferes with a competitor to the partner's advantage.

The net effects figure shown in Figure 4A summarizes interactions of this general type. Note that in this case, there might or might not be a mutualism between M1 and M2 in the absence of the competitor C. With reference to the two examples above, plants and mycorrhizae are likely to be mutualists even in the absence of competitors as there are other benefits of this interaction. However, the crabs and algae studied by Stachowicz and Hay would likely not be.53 Such context dependency—that is, a mutualistic outcome that occurs only in a limited set of environments—is almost impossible to capture in a net effects-based figure such as Figure 4A. A resource-based figure permits us to do this. Furthermore, it allows us to recognize important differences between phenomena exemplified in these two empirical cases and to consider how competition may function in each of them. For this reason, we treat them separately below.

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Figure 4. Competitive advantage as a benefit of mutualism. (A) A net effects diagram. The core mutualism is the same as in Figure 1A. A third species (C) has been added that competes (–/–) with M1. M2 interferes (–) with C, thus giving an indirect benefit to M1, in addition to any direct benefits of the core mutualism. (B) A resource-based diagram. The core mutualism is the same as in Figure 1B. Additionally, M1 consumes a resource (R3) that is also consumed by C. (C) Competitive advantage is a secondary benefit of mutualism. By consuming R2, M1 becomes a superior competitor for R3 and is able to interfere with consumption of R3 by C. (D) A resource-based diagram of context-dependent mutualism. M1 produces R1, which is consumed by M2. However, M2 does not produce any resource that can be consumed directly by M1 (R2 has been removed from the core mutualism). Instead, the benefit provided by M2 is context-dependent and requires the presence of C. (E) Competitive advantage is the only benefit of mutualism. M2 is an antagonist of C and interferes with its consumption of R3. Consequently, M1 is able to increase consumption of R3. For the resource-based diagrams, (B–E), arrows represent resource production (black arrows), resource consumption (red arrows), increased resource production or consumption (thick arrows), and interference with resource consumption (dashed inhibition arrows).

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Figures 4B and C illustrate the case in which one, but not the only, benefit of mutualism is the suppression of competitors. In Figure 4B, we again see the same core mutualism as in Figures 1B, 2B, and 3B. Added to it is a competitor (C) that shares a different resource (R3) with mutualist M1. (If C shared R1 or R2 with a mutualist, we would consider it to be an exploiter of the M1–M2 mutualism, and the scheme shown in Fig. 2B would be more appropriate.) As in Figures 1B, 2B, and 3B, mutualist M1 gains a direct benefit from consuming R2. In addition, as illustrated in Figure 4C, consuming R2 gives M1 a competitive advantage over C for the shared resource R3. The example provided by Hartnett et al.,52 described above, fits this scenario. Note again that it is not M2 (mycorrhizae) that suppress the competitor; M1 (the plant) does this, but only when their mutualists M2 are present. Competitive suppression is thus an indirect benefit provided by mycorrhizae accompanying the direct benefits of nutrient provision. Evidently, it can be extremely important in its own right, however. For example, Wilson and Hartnett show that community-scale plant diversity may be increased if mycorrhizae augment a subordinate species’ performance in competition with a dominant one.54

Figure 4D illustrates the case when an interaction is mutualistic only in the presence of a competitor, that is, when alteration of the competitive environment is the only benefit of a mutualism. In this case, there is no core mutualism resembling those in Figures 1B, 2B, and 3B. Here, one species (M2) consumes a resource (R1) provided by a partner (M1), but there is no reciprocal benefit (i.e., there is no resource R2). As in Figure 4B, the resource-providing partner M1 competes for another resource (R3) with a competitor C. In Figure 4D, the relationship between M1 and M2 is not mutualistic: these interactions are often referred to as commensal (i.e., +0 rather than ++) or facilitative, or sometimes more generically as “positive interactions” (e.g., Refs. 55 and 56). Alternatively, if R1 is costly to produce and no benefit is returned for its provision, then this interaction could be antagonstic (+–). It can become mutualistic, however, via the mechanism illustrated in Figure 4E. Here, M2 alters the environment in a way that shifts the balance of competition between M1 and C in favor of M1. This scenario matches that described by Stachowicz and Hay,53 in which crabs benefit from coralline algae (they are provided with a substrate on which to live and feed), but algae only benefit from the crabs when fouling seaweeds are present and crabs remove them.

Context-dependent outcomes like this one are now widely recognized as one of the most ubiquitous ecological features of mutualism, regardless of their natural history.3 The evolutionary implications of context dependency, in contrast, have barely been considered (but see Ref. 57). Figure 4 clearly suggests that understanding when mutualisms and mutualistic outcomes arise may depend upon documenting the competitive environment in which they occur.

Mechanisms of competitive asymmetry among mutualists: the cooperation–competition trade-off

  1. Top of page
  2. Abstract
  3. Introduction
  4. Competition and mutualism: empirical phenomena
  5. Mechanisms of competitive asymmetry among mutualists: the cooperation–competition trade-off
  6. Mutualism and competition: evolutionary implications
  7. Conclusions
  8. Acknowledgments
  9. Conflicts of interest
  10. References

In the previous section, we showed that competition for resources is a common feature of mutualisms. Additionally, we discussed how competition is often between individuals or species that vary in their quality as mutualist partners (Fig. 1C and D), and in the extreme case are exploiters that do not reciprocate any benefits (Fig. 2). This variation in partner quality raises fundamental evolutionary questions: how is the variation in partner quality maintained and how can mutualisms persist despite low-quality partners and exploiters? If low-quality mutualists and exploiters have a competitive advantage, evolution should lead to the loss of mutualism. Thus, the question becomes: what mechanisms favor high-quality mutualists? Below, we demonstrate how considering the details of competition described above is crucial for understanding how investment in mutualism is maintained evolutionarily.

Although evidence is lacking, it has generally been assumed that individuals can gain a competitive advantage by investing less in rewarding partners (e.g., Figs. 1C, 2C, and 5A).58,59 In this case, or even when individuals that contribute less to the partner are equal in direct competition, the mutualism is expected to evolve to extinction.11 This occurs as a result of a “tragedy of the commons”60: lower-quality mutualists can invest more in survival and reproduction while retaining full benefits from partners, with an ever-growing numerical advantage as a consequence.

image

Figure 5. Possible relationships between mutualist quality (investment in producing mutualistic resources) and competitive ability (access to mutualistic resources produced by the partner). (A) Competitive ability decreases with investment in producing mutualistic resources. This decrease can be linear (solid line), accelerating (dashed line), or decelerating (dotted line). (B) Competitive ability increases with mutualist quality. This increase can be linear (solid line), “punishing” (marginal increases in competitive ability become smaller as mutualist quality increases; dashed line), or “rewarding” (marginal increases in competitive ability become larger as mutualist quality increases; dotted line). (C) Competitive ability is maximized at intermediate mutualist quality (concave, dashed line) or is minimized at intermediate mutualist quality (convex, dotted line).

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Evolutionary models of mutualism have invoked several mechanisms that shift the balance in favor of higher-quality mutualists. What these mechanisms share in common is that they enable selection for increased investment in mutualism by offseting the cost of investment with the benefit of a competitive advantage. How the competitive advantage arises depends on the mechanism. We discuss the most prominent of these mechanisms below, along with empirical examples. For each mechanism, we describe how it functions and how it affects competition. As we shall see, the cooperation–competition trade-off shaped by these mechanisms is key to understanding several important aspects of the evolution of mutualisms.

Competitive asymmetry caused by partner choice

Interactions with inferior partners can be costly and reduce the potential for interactions with better partners. Mutualists can escape these costs by using “partner choice” mechanisms to restrict interactions to the best available partners.38,61 In turn, partner choice alters the competitive and adaptive landscape by conferring an advantage to better mutualists (e.g., Figs. 1D, 2D, and 5B).

Partner choice mechanisms may be based on a comparison of available partners. This “active partner choice” is common for animals such as pollinators and fruit dispersers that can choose partners based on reliable cues of reward quality,16 and is also well-described in clients of cleaner fish.62 Since high-quality partners are given preferential access to rewards their mutualists provide, they gain a competitive advantage over any lower-quality partners.

Alternatively, partner choice mechanisms may be based on static criteria that prospective partners must meet. Examples include legumes whose roots can only be nodulated by specific nitrogen-fixing rhizobia through a “lock-and-key” recognition system,63 and bobtail squid whose light organs can only be detoxified and colonized by bioluminescent Vibrio fischeri bacteria.64 In this case, only individuals that meet the choice criteria can successfully compete for mutualist rewards.

Partner choice mechanisms may be costly to implement, but they are predicted to evolve as long as there is sufficient variation in partner quality.65,66 The type of partner choice that evolves is likely to depend on both the capabilities of the choosing species (e.g., whether they have the cognitive ability to compare and make choices) and the pattern of variation in partner quality.16 Interestingly, being choosy may itself confer an advantage in competition for partners, as choosy client fish have been found to be given priority by cleaners.67 Partner choice has also been suggested to alter the community of competitors by favoring specialization and reducing the diversity of competing species in mutualist guilds.15

Competitive asymmetry caused by conditional rewards

It is frequently impossible for the quality of a potential partner to be recognized before an interaction takes place.68 When there are no reliable signals of mutualist quality, or when such signals cannot be acted upon in the short term, each partner must take a risk when initiating an interaction. One mechanism that has been proposed to limit this risk is conditional investment in the partner. By adjusting investment based on the amount received from the partner, mutualists can reduce the cost of being cheated and encourage cooperation by the partner. As with partner choice, conditional investment gives high-quality mutualists preferential access to rewards, and thus a competitive advantage over low-quality mutualists and exploiters (e.g., Figs. 1D, 2D, and 5B) that can favor the evolution of increased mutualist qualtiy.

The strategy of gradually investing more in cooperative partners has been termed “raising the stakes”69,70 and “negotiation.”71 The reverse strategy, decreasing investment toward low-quality partners, is often referred to as a type of “sanction” (sanctions are described below). Conditional investment in which rewards are directed toward the most cooperative partners has been found between plants and their mycorrhizal fungi and rhizobia.72,73 The form that conditional investment takes is likely to depend on the opportunities for exploiting and switching partners.74 For example, cleaner fish have the ability to cheat their clients whereas the clients often have the ability to switch cleaners. Since cleaners must compete for clients and high-quality cleaners (those that do not cheat) have a competitive advantage, cleaners build up relationships with their clients through initially higher than average investment.74

Competition between potential partners is not necessary for conditional investment mechanisms to provide a benefit, since conditional investment links the benefits received to the benefits given. However, negotiation has been found to work best when there are multiple prospective partners that can engage in “outbidding competition.”75 Competition between potential partners improves the bargaining position of the other species and increases its benefit from the mutualism.71,76 On the other hand, competition may not always be intensified by the presence of many potential partners. When the benefits of mutualism can be shared without being diminished, potential partners do not need to compete for attention from the mutualist; instead, they may in fact decrease their investment in these conditions. For example, lycaenid larvae have been found to offer higher quantities of nutritious glandular secretions to ant defenders when alone than when aggregated, since ants tending other larvae in the aggregation will deter predators and parasitoids from the entire group.77

Competitive asymmetry caused by sanctions

Instead of rewarding high-quality partners, mutualists may punish low-quality partners by imposing “sanctions”: terminating the interaction or reducing the net benefit conferred during continuing interactions.65 The net benefit given to low-quality partners can be reduced either by providing fewer rewards (as in conditional investment, discussed above) or by inflicting an additional cost. Sanctions provide a competitive and selective advantage to high-quality mutualists that can avoid punishment and thus get a higher net benefit from the interaction (e.g., Figs. 1D, 2D, and 5B).

In many cases, mutualists may not have control over which interactions are initiated, but may be able to end interactions that are not favorable. For example, yuccas can abort fruits when yucca moths lay too many eggs (which would hatch into seed-eating larvae) or do not pollinate sufficiently.78 Thus, the larvae of the yucca moths are killed when the costs of growing the fruit are too high compared to the benefit that would be received from any surviving seeds. (Note that such sanctions may have originally evolved as defenses against antagonists or as responses to the absence of mutualists; nevertheless, they can now be utilized to control partners.)

Competition between potential partners makes terminating an interaction a viable option; in the absence of alternative partners, even a low-quality mutualist could be better than no mutualist. The sanctions that clients of cleaner fish use depend on the client's ability to travel to other cleaners; clients with large ranges sanction by terminating the interaction and switching to another cleaner, whereas clients with small ranges sanction by chasing the cleaner.79 Interestingly, cleaners are significantly more cooperative with predatory clients, presumably because of the more severe sanctions predators could employ.74

Sanction severity can also vary quantitatively with partner investment. Legumes have been found to decrease the oxygen supply to nodules that fix less nitrogen,35,80 and the level of such sanctions can depend on how much nitrogen is fixed.36 As with partner choice, the consequences for competition between partners of different quality depends on whether partner quality is evaluated by a direct comparison of partners or by static criteria. For example, if legumes withhold oxygen based on a comparison of nitrogen fixation among nodules, rhizobia in a nodule need only fix more nitrogen than the rhizobia in the other nodules in order to gain a competitive advantage. Alternatively, if the amount of oxygen that legumes supply depends on the absolute amount of nitrogen provided by a nodule, rhizobia can always increase their competitive advantage by fixing more nitrogen. Furthermore, the scale at which sanctions occur is important. For instance, if multiple strains of rhizobia coinfect nodules, sanctions against entire nodules may not give a competitive advantage to the best rhizobia.81

Competition for partners can affect the strength of sanctions. When the sanctioning species is the limiting partner, stronger sanctions are predicted to be favored.82 Competition for partners can also affect the likelihood of sanctions. This may be the case when, as in the yucca fruit abortion example above, an overabundance of partners makes the interaction too costly.83,84 Competition for rewards can lead to increased mortality even when a severe action such as fruit abortion does not occur, as has been found for the seed-eating larvae of yucca, globeflower (Trollius) and fig pollinators.84–86 Consequently, there is evidence that some species have evolved to avoid mutualists that already have partners. For example, yucca moths and senita moths use pheromone signals deposited during oviposition to avoid laying eggs in flowers that competitors have already used.87,88 Furthermore, it has been suggested that mutualists can evolve mechanisms to intensify this competition.89–91 One example is globeflowers whose tightly closed flower structure is thought to intensify competition between the seed-consuming larvae of pollinators.89

Mutualism and competition: evolutionary implications

  1. Top of page
  2. Abstract
  3. Introduction
  4. Competition and mutualism: empirical phenomena
  5. Mechanisms of competitive asymmetry among mutualists: the cooperation–competition trade-off
  6. Mutualism and competition: evolutionary implications
  7. Conclusions
  8. Acknowledgments
  9. Conflicts of interest
  10. References

Above, we discussed how incorporating competition and its underlying mechanisms into our understanding of mutualism helps to illuminate ecological phenomena: how species engaged in different aspects of mutualism (i.e., as mutualists, exploiters of mutualists, or competitors of mutualists) interact, as well as what the outcomes of these interactions will be. We then reviewed the mechanisms that have been proposed to select for high-quality mutualists by giving a competitive advantage to the best partners. As we take an evolutionary perspective on mutualistic and competitive traits, many more questions arise. Are these interactions evolutionarily stable, or will one or more species abandon the mutualism or even go extinct? What roles have mutualisms played in generating macroevolutionary patterns, and how can incorporating competition help us understand these? How do the mechanisms generating the different competitive hierarchies described above influence these outcomes? Below, we discuss the implications of competition for the evolution of mutualisms.

The origins of mutualism and obligate endosymbiosis

Novel mutualisms can provide an escape from competition by extending the range of resources or services available to a species. For example, a species could gain an advantage over its competitors by engaging in a novel mutualism (Fig. 4). Alternatively, the benefits of a mutualism between competitors (Fig. 3) could compensate for the costs of competition and enable coexistence. Thus, intense competition should favor the evolution of novel mutualisms.92 However, unless partners can produce commodities without entailing a cost (“by-product” mutualism), conflicts between the partners will remain.39

These conflicts can be ameliorated if current investment in a mutualist gives a competitive advantage for access to future rewards through “partner fidelity feedback.”38,39,92 Investment in a mutualist can increase that mutualist's survival, reproductive success, and ability to produce rewards. These increased rewards can feed back to the original partner, or its progeny, when interactions are extended over long time periods or are repeated with little movement (i.e., there is a “viscous” community). Models have found that partner fidelity feedback can select for mutualism,93–95 even between a parasite and its host,96 since parasite evolution is also strongly directed by competition for hosts.

The most striking form of partner fidelity is when independent species become a single organism, as occurred during the development of the eukaryotic cell.97 Similar transitions are thought to have produced the lichens and the vertically transmitted bacterial endosymbionts of many insects,98,99 and the evolutionary transition to cotransmission has even been observed experimentally in bacteriophage.100 In these transitions, the species have reached a solution that guarantees that the best mutualists are the best competitors for partners, as the best mutualists are also the most successful at producing future partners.

Persistence of mutualist lineages: the evolutionary paradox of specialization

Mutualism can increase the competitive ability of mutualists relative to that of other community members (Fig. 4). This competitive advantage, particularly when it results in an expansion of realized niche breadth, is expected to contribute to the persistence of the mutualist lineage.101

On the other hand, competition for partners (Figs. 1 and 2) may favor specialization on a subset of potential partners,15,102 which narrows niche breadth and may represent an evolutionary dead-end.103 Such specialization is expected to increase a mutualist species’ susceptibility to extinction when there is loss of habitat (e.g., Ref. 104; but see Ref. 105) or of the partner species.106 Whereas many mutualisms remain facultative and are thus unlikely to be affected greatly by the loss of any one partner species,58 the case of obligate mutualisms is more complex. There is evidence that many obligate mutualisms have relatively recent origins, which suggests that these mutualisms are prone to extinction.107 However, specialized, obligate mutualists can persist for millions of years,108,109 and may have life history traits that promote persistence in the (temporary) absence of partners.106,110

Mathematical models have shed light on the evolutionary problem of specialization, showing that competition for partners and rewards is critical for determining whether an obligate mutualism is evolutionarily stable, or on an evolutionarily trajectory toward extinction.11 One of the ways in which a mutualist species, and thus its specialized partner, can be lost is as a result of invasion by competitively superior exploiters (e.g., Fig. 2C). Interestingly, exposure of an obligate mutualism to exploiters at an early stage of the mutualism evolutionary history can influence the mutualists’ coevolutionary trajectories in ways that “immunize” the mutualism against modern exploiters.13 The consequences of coevolution between mutualists and exploiters are also determined by the intensity of competition among mutualists for partner rewards, that is, extinction of the exploiter under weak competition, stable coexistence at intermediate levels of competition, or global extinction of the mutualism and exploiter under strong competition.111

Persistence of mutualist lineages: evolution of mutualist quality

Species can be driven to abandon mutualism or to extinction if partners fail to provide a sufficient benefit. The mechanisms that mutualists use to control their partners and ensure a benefit are described above. By giving a competitive advantage to high-quality mutualists, these partner control mechanisms play an important role in the evolution of mutualist quality. The way that mutualist quality evolves depends on the details of the control mechanism used.

Models of partner choice (described above) have generally predicted the evolution of higher-quality mutualists.11,13,95 In addition, partner choice by legumes has been found to successfully select for more productive rhizobia.112 However, since active partner choice requires direct competition between potential partners, lower-quality mutualists may still have a growth advantage whenever better mutualists are not available for comparison.113 Thus, active partner choice is most likely to lead to a fair exchange of resources when there is a large group of competing partners.114,115 Static choice criteria may ensure that prospective partners must always (appear to) be of a certain quality. However, partner choice does not eliminate all low-quality mutualists and exploiters if the choice criteria are not reliable indicators of mutualist quality,66,68 as has been observed in the legume-rhizobium system.63

Instead of increasing their investment in mutualism to compete with high-quality mutualists, low-quality mutualists could abandon the mutualism. It has recently been suggested that partner choice mechanisms could select for low-quality partners to avoid the interaction, if being rejected is costly.116 Rejection may be particularly costly for endosymbionts, which are unlikely to escape after a failed attempt to colonize a host.

Similar to partner choice, conditional investment strategies (see above) can result in increased mutualist quality. These strategies can even maximize the partners’ joint benefit from the interaction.71 However, also in parallel to partner choice, conditional investment may not be able to exclude all low-quality partners, which still experience an advantage when not in direct competition.76 Moreover, conditional investment may not be able to maintain mutualism in the absence of other factors (such as spatial structure).93

The use of sanctions against low-quality partners is also predicted to select for higher-quality partners.117,118 However, there may be strategies that allow low-quality partners to escape sanctions without investing more in mutualism, such as shallow oviposition by yucca moths that avoids triggering fruit abortion.119 As described above, competition among mutualists for rewards can be costly and these costs may be intensified by partner traits as a response to overexploitation. In such cases, which include the yucca-yucca moth,87 senita-senita moth,88 and globeflower-fly mutualisms,89 trade-offs between competitive dominance and other traits, such as fecundity, can select for partners that provide a higher net benefit.89,111 Thus, details of the sanction process, its relation with competition, and trade-offs with other traits, are critical for the evolution of mutualist quality.

In general, the evolutionary implications of partner control for mutualist quality depend on the relationship between mutualist quality and competitive ability (Fig. 5). The parallel evolution of large investments by mutualist partners is expected if competition for partners is strongly asymmetrical in both mutualists, that is, if the competitive advantage to better mutualists is high.11 This means that there is a “cooperation–competition” trade-off between the direct cost of mutualistic investment and the direct benefit of competitive advantage (Fig. 5); and that the slope of the trade-off is steep. This prediction is robust to the inclusion of (nonevolving) exploiters.13 However, mutualist–exploiter coevolution tends to degrade the mutualist's quality.111 A clear-cut prediction is that mutualist and exploiter converge, resulting in relatively benign exploitation, if mutualists experience strong competition for partners; they diverge, leading to severe exploitation, if competition for partners is weak.111

Evolutionary patterns of convergence and divergence

Mutualists’ traits may be expected to coevolve to match in order to maximize the exchange of rewards (e.g., Refs. 120 and 121, but see Ref. 122), and convergent evolution has been found between species that share mutualist partners.123 Furthermore, there can be “advergent” evolution, such as when exploiters (e.g., nectarless orchids) evolve mimicry of a mutualist species.124

Convergence may occur between other aspects of the mutualists’ niches and this is particularly important for understanding mutualism between resource competitors (Fig. 3). In these cases, mutualism is expected to promote coexistence despite overlapping niches, as the benefits of mutualism can compensate for (some of) the costs of competition.125,126 However, competition should still constrain the evolution of mutualism since increasing the partner population decreases resources available.127

In the case of Müllerian mimicry, the benefits of mutualism are enhanced if the mimics overlap in time and space. However, this overlap is likely to increase competition for shared resources. Either mutualism or competition may be the dominant interaction. In neotropical butterflies, mimicry has driven niche convergence between sympatric, unrelated species.128 In contrast, mimicry in catfish occurs almost exclusively between species that are not competitors.129 More research is needed to determine how often and why mutualism is dominant to competition and vice versa.

Divergence between mutualists can be driven by competition for partners. Trade-offs in the ability to exploit different shared resources can select for resource specialization;130 similarly, competition for partners can select for specialization on a subset of potential partner species.15,102 For example, the diversification of floral morphology and phenology within communities has been attributed to competition for partners.131–133 Interestingly, the intensity of competition for partners can be reflected in the degree of diversification; plants competing more for pollinators than for fruit dispersers show higher diversification in flower than in fruit morphology.134 Nevertheless, it has been suggested that, even without specialization, mutualists competing for a shared partner (Fig. 1C and D) should be more likely to coexist than general competitors, since the competing mutualists can increase the density of their shared resource (the partner species).14

Competition can be intense even within specialized interactions, especially when one mutualist partner utilizes competition in partner control. As described above, mutualists may evolve mechanisms that increase the intensity of competition among their partners.89,90 Selection should then act on the partner species to reduce competition. As alternatives to evolving to become better competitors, partners could diversify in their use of shared mutualist commodities,89,135 or abandon the mutualism.58 Even when there are mechanisms that give a competitive advantage to mutualists, intense competition among mutualists has been predicted to enable the coexistence of exploiters,25 as well as to make conditions favorable for exploiters to arise from mutualists.11,89,111,135 If the competitive advantage does not completely compensate for the costs of investment in mutualistic resources, the mutualism may remain susceptible to invasion by low-quality partners.136 Some empirical support for these predictions comes from the pollination/seed-predation mutualisms of globeflowers and yuccas.137–141 In these mutualisms, the pollinators have responded to larval competition by diversifying in timing and location of oviposition, with the later visitors frequently becoming exploiters of the mutualism.

The long-term evolutionary implications of competition for partners critically depend on the shape of the cooperation–competition trade-off.11 One possibility is a rewarding trade-off (Fig. 5B), in which the competitive advantage of being a better mutualist is large while the competitive disadvantage suffered for being an inferior mutualist is small. Sufficiently rewarding trade-offs can result in evolutionary diversification of mutualist quality and maintenance of variation in mutualist quality. In contrast, the trade-off could be punishing (Fig. 5B), in which increasing mutualist quality adds little to competitive ability, whereas there is a large loss of competitive ability with a small decrease in mutualist quality. Punishing trade-offs oppose evolutionary diversification.

We still have only a preliminary understanding of how the cooperation–competition trade-off is shaped by partner control mechanisms, and in particular whether partner choice versus sanctions result in qualitatively different shapes. The difference between rewarding and punishing shapes might not be between partner choice and sanctions, but rather between partner control mechanisms that directly compare partners versus those that compare partners to fixed criteria. For direct comparisons, the advantage comes from being superior to the rest of the potential partners. A small increase in quality in a low-quality mutualist is unlikely to increase its chances of being the best of the available partners. However, the same small increase in quality might move a high-quality mutualist up to the “best partner” rank—thus leading to a rewarding trade-off. On the other hand, if the partners are compared to fixed criteria, all that is necessary is to meet the criteria, and any further increases in mutualist quality should not have much effect on competitive advantage—thus leading to a punishing trade-off. Increases in quality for high-quality mutualists may even lead to a net decrease in competitive ability if the cost of investing in mutualism is taken into account (a concave trade-off, see Fig. 5C). Empirical data are now needed to back up these heuristics.

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Competition and mutualism: empirical phenomena
  5. Mechanisms of competitive asymmetry among mutualists: the cooperation–competition trade-off
  6. Mutualism and competition: evolutionary implications
  7. Conclusions
  8. Acknowledgments
  9. Conflicts of interest
  10. References

Nearly all mutualisms have consumer–resource interactions embedded within them, whereby species on one side of the interaction exploit, and therefore may compete for, a resource (food, service) produced by species on the other side.2 A natural consequence of this principle is that mutualisms set the stage for competitive interactions. As we showed in the section. Competition and mutualism: empirical phenomena, mutualists compete as consumers of their partner-produced resources; the scope of competition may be even broader if, for example, the mutualistic resource influences the outcome of competition for other resources. This leads us to advocate for the importance of competition, both intra- and interspecific, as a critical factor of the ecological and evolutionary dynamics of mutualisms. More generally, to understand mutualism, it is critical to quantify the competitive interactions that lie at its heart.

Our review has highlighted the various form of competition that have been well documented to be associated with mutualistic interactions. We have offered a simple but general classification to unite similar phenomena and distinguish among divergent ones. As we have shown, based on existing theory, the intensity of intra- and interspecific competition for partners, as well as asymmetries in competitive effects on individuals that differ in their mutualistic quality, profoundly affects the ecological stability and evolutionary dynamics of mutualism. Yet, our understanding of the intersection between mutualism and competition is in its infancy. Further studies are necessary to illuminate:

  • • 
    how multiple effects of competition combine to influence the dynamics of the interaction;
  • • 
    how, conversely, the nature of the traded resources/services influences, both ecologically and evolutionarily, the type and intensity of competition and the underlying mechanisms; and
  • • 
    how the structure and diversity of a mutualistic network and the competitive interactions embedded in it may jointly coevolve and influence the short-term persistence of mutualists, the long-term stability of their interaction, and the function of the network in its broader ecosystem context.

To address these broad issues at the interface between competition and mutualism, we advocate a joint empirical–theoretical approach. On the theoretical side, we need to extend modeling approaches that integrate ecological and evolutionary processes, for example, adaptive dynamics and related models.142,143 At the level of individuals, key elements of these models will be the existence and shape of physiological trade-offs between cooperation (i.e., investment in mutualism), competition, and other functional traits; the capacity for individuals to express conditional responses to variation in their mutualistic and competitive environment; the existence of heritable variation for mutualistic and competitive traits and their potentially conditional expression; and the structure of the network of other consumer–resource interactions in which individuals are embedded. Eco-evolutionary models should be designed that integrate knowledge about these individual-level properties and that scale up to gain insights into their ecological and evolutionary consequences. It is thus critical that we deepen such knowledge on the empirical side. To this end, model systems are needed in which multiple forms of competition interact with mutualism.

For a given system, the empirical agenda must start by asking (i) whether partners on at least one side of the interaction compete for mutualistic resources (Fig. 1B); (ii) whether exploiters are present (Fig. 2B), and if so, how costly they are; (iii) whether mutualists also compete for some shared resource (Fig. 3B); and (iv) whether gaining access to mutualists provides one partner with an advantage in competition with its guild members (Fig. 4B).

Observations and manipulative experiments should be performed to weigh, for instance, the strength of competitive effects relative to mutualistic effects and to examine evidence for adaptations that reduce or increase the intensity of competition. The best studied mutualisms from the perspective of the questions raised here are plant—pollinator–nectar-robber and plant—ant–defender—ant–opportunist systems. However, for no system have all four questions been answered conclusively. For example, evidence that competition between pollinators and nectar-robbers inflicts a fitness cost on plants is equivocal.32 A review by Bergstrom et al. provides a useful basis to discuss how other mutualisms position themselves with respect to these four axes of variation and how they could serve the objectives of a joint empirical and theoretical research program on the interplay between mutualism and competition.144

The competition perspective on mutualism opens interesting approaches for further unification of the ecological and evolutionary analysis of interspecific interactions. Particularly promising to explore are parallels with the ecology and evolutionary biology of host–parasite systems. Interactions between hosts and parasites have long been studied as consumer–resource interactions, and the role that competition plays in their ecology and evolution has already received considerable attention. Given the strong conceptual and biological ties that exist between mutualism and parasitism, we anticipate fruitful fertilization of the nascent studies of competition in mutualism from the ongoing theoretical and empirical investigation of competition in parasitism. Taking a competition perspective to parasitism was key to discovering the diverse implications of multiple infection by mixed strains of parasites for virulence.145 This line of inquiry began with simple mathematical models showing how influential within-host competition can be for the evolution of virulence.146–149 This spawned further theoretical and empirical studies that unraveled considerable variation in the relationship between virulence and competitive ability,150–154 and highlighted the complexity of real competitive interactions among parasites for host resources compared to simple resource competition.155 Another exciting parallel between parasitism and mutualism in the context of competition can be drawn from the issue of specialization and diversification. Much theory has been developed to shed light on the evolution of host specificity in parasites and the consequences of specialization for ecological coexistence and evolutionary diversification. Similarly, we expect theoretical advances to shed light on the evolution of mutualistic networks by considering feedbacks with the ecological mixture of trade and competition among partners. This work will help to strengthen our understanding of the structure and diversity of mutualistic networks, as well as to foster our ability to predict their robustness to environmental perturbation.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Competition and mutualism: empirical phenomena
  5. Mechanisms of competitive asymmetry among mutualists: the cooperation–competition trade-off
  6. Mutualism and competition: evolutionary implications
  7. Conclusions
  8. Acknowledgments
  9. Conflicts of interest
  10. References

We thank M. Friesen and two anonymous reviewers for helpful comments on the manuscript. E.I.J. was supported by National Science Foundation Grant DMS-0540524 to R. Gomulkiewicz. R.F. acknowledges support from National Science Foundation Award EF-0623632, the Institut Universitaire de France, and the Agence Nationale de la Recherche.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Competition and mutualism: empirical phenomena
  5. Mechanisms of competitive asymmetry among mutualists: the cooperation–competition trade-off
  6. Mutualism and competition: evolutionary implications
  7. Conclusions
  8. Acknowledgments
  9. Conflicts of interest
  10. References