INTERGENOMIC EPISTASIS AND COEVOLUTIONARY CONSTRAINT IN PLANTS AND RHIZOBIA

Studying how the fitness benefits of mutualism differ among a wide range of partner genotypes, and at multiple spatial scales, can shed light on the processes that maintain mutualism and structure coevolutionary interactions. Using legumes and rhizobia from three natural populations, I studied the symbiotic fitness benefits for both partners in 108 plant maternal family by rhizobium strain combinations. Genotype‐by‐genotype (G × G) interactions among local genotypes and among partner populations determined, in part, the benefits of mutualism for both partners; for example, the fitness effects of particular rhizobium strains ranged from uncooperative to mutualistic depending on the plant family. Correlations between plant and rhizobium fitness benefits suggest a trade off, and therefore a potential conflict, between the interests of the two partners. These results suggest that legume–rhizobium mutualisms are dynamic at multiple spatial scales, and that strictly additive models of mutualism benefits may ignore dynamics potentially important to both the maintenance of genetic variation and the generation of geographic patterns in coevolutionary interactions.     

Nutrient loading alters the performance of key nutrient exchange mutualisms

Nutrient exchange mutualisms between phototrophs and heterotrophs, such as plants and mycorrhizal fungi or symbiotic algae and corals, underpin the functioning of many ecosystems. These relationships structure communities, promote biodiversity and help maintain food security. Nutrient loading may destabilise these mutualisms by altering the costs and benefits each partner incurs from interacting. Using meta‐analyses, we show a near ubiquitous decoupling in mutualism performance across terrestrial and marine environments in which phototrophs benefit from enrichment at the expense of their heterotrophic partners. Importantly, heterotroph identity, their dependence on phototroph‐derived C and the type of nutrient enrichment (e.g. nitrogen vs. phosphorus) mediated the responses of different mutualisms to enrichment. Nutrient‐driven changes in mutualism performance may alter community organisation and ecosystem processes and increase costs of food production. Consequently, the decoupling of nutrient exchange mutualisms via alterations of the world's nitrogen and phosphorus cycles may represent an emerging threat of global change.     

Perspectives on allelopathic disruption of plant mutualisms: a framework for individual- and population-level fitness consequences

Mutualisms with mycorrhizal fungi, pollinators, and seed dispersers are critical for plant survival and reproduction. However, mutualism effectiveness is highly sensitive to disturbance by environmental stressors. Allelopathy is often overlooked, yet likely important, as a potential stress on plant mutualism function. Allelochemicals can affect plant mutualisms by either directly interfering with the plant’s ability to produce resources and rewards for its mutualistic partners or by directly or indirectly altering the non-plant mutualist’s behavior. Here we explore the potential effects of allelochemicals on plant mutualisms. Since allelochemicals can reduce plant growth and carbon acquisition, we suggest that allelopathy could directly diminish: (1) carbon provisioning to mycorrhizal fungi, (2) flower, pollen, and nectar production for pollinators, and (3) fruit attractiveness to seed dispersers. Similarly, allelochemicals that directly affect mycorrhizal fungi functioning can reduce the flow of soil resources to their plant partner. Further, volatile allelochemicals or uptake of allelochemicals from the soil by the plant could alter pollen/nectar or fruit attractiveness and indirectly influence pollinator and seed disperser behavior. Finally, we explore the extent to which plant-produced chemicals could have a direct or indirect positive effect on plant mutualisms. We end using these questions to frame future avenues of research that could help to move studies of allelopathy into the broader ecological context of mutualisms.     

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

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

Decreasing water availability across the globe improves the effectiveness of protective ant–plant mutualisms: a meta‐analysis

Abiotic conditions can increase the costs of services and/or the benefits of rewards provided by mutualistic partners. Consequently, in some situations, the outcome of mutualisms can move from beneficial to detrimental for at least one partner. In the case of protective mutualisms between ant bodyguards and plants bearing extrafloral nectaries (EFNs), plants from arid environments face a trade‐off between EFN production and maintenance and water and carbon economy. This trade‐off may increase EFN costs and decrease their value as a defensive strategy to plants in such environments. Despite this, the presence of EFNs is an ubiquitous trait in plants from arid environments, suggesting that they provide greater benefits to plants in these environments to compensate for their higher costs. We used a meta‐analysis to investigate if such benefits do increase with decreasing water availability and the possible underlying causes (such as ant behaviour or ant diversity). As predicted, ant effect on EFN plants performance increased as mean annual precipitation decreased. We also found that the frequency of dominant ants on EFN plants increased in drier areas. Due to the more aggressive behaviour of dominant ants, we suggest that they represent an important factor shaping the adaptive value of EFNs to plants in arid environments.     

A selection mosaic in the facultative mutualism between ants and wild cotton

In protection mutualisms, one mutualist defends its partner against a natural enemy in exchange for a reward, usually food or shelter. For both partners, the costs and benefits of these interactions often vary considerably in space because the outcome (positive, negative or neutral) depends on the local abundance of at least three species: the protector, the beneficiary of protection and the beneficiary's natural enemy. In Gossypium thurberi (wild cotton), ants benefit nutritionally from the plant's extrafloral nectaries and guard plants from herbivores. Experimentally altering the availability of both ants and extrafloral nectar in three populations demonstrated that the mutualism is facultative, depending, in part, on the abundance of ants and the level of herbivore damage. The species composition of ants and a parasitic alga that clogs extrafloral nectaries were also implicated in altering the outcome of plant-ant interactions. Furthermore, experimental treatments that excluded ants (the putative selective agents) in combination with phenotypic selection analyses revealed that selection on extrafloral nectary traits was mediated by ants and, importantly, varied across populations. This work is some of the first to manipulate interactions experimentally across multiple sites and thereby document that geographically variable selection, mediated by a mutualist, can shape the evolution of plant traits.     

Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia

Mutualistic interactions are widespread and obligatory for manyorganisms, yet their evolutionary persistence in the face ofcheating is theoretically puzzling. Nutrient-acquisition symbiosesbetween plants and soil microbes are critically important toplant evolution and ecosystem function, yet we know almost nothingabout the evolutionary dynamics and mechanisms of persistenceof these ancient mutualisms. Partner-choice and partner-fidelityare mechanisms for dealing with cheaters, and can theoreticallyallow mutualisms to persist despite cheaters. Many models of cooperative behavior assume pairwise interactions,while most plant-microbe nutrient-acquisition symbioses involvea single plant interacting with numerous microbes. Market models,in contrast, are well suited to mutualisms in which single plantsattempt to conduct mutually beneficial resource exchange withmultiple individuals. Market models assume that one partnerchooses to trade with a subset of individuals selected froma market of potential partners. Hence, determining whether partner-choiceoccurs in plant-microbe mutualisms is critical to understandingthe evolutionary persistence and dynamics of these symbioses.The nitrogen-fixation/carbon-fixation mutualism between leguminousplants and rhizobial bacteria is widespread, ancient, and importantfor ecosystem function and human nutrition. It also involvessingle plants interacting simultaneously with several to manybacterial partners, including ineffective ("cheating") strains.We review the existing literature and find that this mutualismdisplays several elements of partner-choice, and may match therequirements of the market paradigm. We conclude by identifyingprofitable questions for future research.     

EXPLAINING MUTUALISM VARIATION: A NEW EVOLUTIONARY PARADOX?

The paradox of mutualism is typically framed as the persistence of interspecific cooperation, despite the potential advantages of cheating. Thus, mutualism research has tended to focus on stabilizing mechanisms that prevent the invasion of low‐quality partners. These mechanisms alone cannot explain the persistence of variation for partner quality observed in nature, leaving a large gap in our understanding of how mutualisms evolve. Studying partner quality variation is necessary for applying genetically explicit models to predict evolution in natural populations, a necessary step for understanding the origins of mutualisms as well as their ongoing dynamics. An evolutionary genetic approach, which is focused on naturally occurring mutualist variation, can potentially synthesize the currently disconnected fields of mutualism evolution and coevolutionary genetics. We outline explanations for the maintenance of genetic variation for mutualism and suggest approaches necessary to address them.     

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

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

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

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

Selection for cheating across disparate environments in the legume‐rhizobium mutualism

The primary dilemma in evolutionarily stable mutualisms is that natural selection for cheating could overwhelm selection for cooperation. Cheating need not entail parasitism; selection favours cheating as a quantitative trait whenever less‐cooperative partners are more fit than more‐cooperative partners. Mutualisms might be stabilised by mechanisms that direct benefits to more‐cooperative individuals, which counter selection for cheating; however, empirical evidence that natural selection favours cheating in mutualisms is sparse. We measured selection on cheating in single‐partner pairings of wild legume and rhizobium lineages, which prevented legume choice. Across contrasting environments, selection consistently favoured cheating by rhizobia, but did not favour legumes that provided less benefit to rhizobium partners. This is the first simultaneous measurement of selection on cheating across both host and symbiont lineages from a natural population. We empirically confirm selection for cheating as a source of antagonistic coevolutionary pressure in mutualism and a biological dilemma for models of cooperation.     

Phenological shifts and the fate of mutualisms

Climate change is altering the timing of life history events in a wide array of species, many of which are involved in mutualistic interactions. Because many mutualisms can form only if partner species are able to locate each other in time, differential phenological shifts are likely to influence their strength, duration and outcome. At the extreme, climate change‐driven shifts in phenology may result in phenological mismatch: the partial or complete loss of temporal overlap of mutualistic species. We have a growing understanding of how, when, and why phenological change can alter one type of mutualism–pollination. However, as we show here, there has been a surprising lack of attention to other types of mutualism. We generate a set of predictions about the characteristics that may predispose mutualisms in general to phenological mismatches. We focus not on the consequences of such mismatches but rather on the likelihood that mismatches will develop. We explore the influence of three key characteristics of mutualism: 1) intimacy, 2) seasonality and duration, and 3) obligacy and specificity. We predict that the following characteristics of mutualism may increase the likelihood of phenological mismatch: 1) a non‐symbiotic life history in which co‐dispersal is absent; 2) brief, seasonal interactions; and 3) facultative, generalized interactions. We then review the limited available data in light of our a priori predictions and point to mutualisms that are more and less likely to be at risk of becoming phenologically mismatched, emphasizing the need for research on mutualisms other than plant–pollinator interactions. Future studies should explicitly focus on mutualism characteristics to determine whether and how changing phenologies will affect mutualistic interactions.     

Life-history differences among coral reef sponges promote mutualism or exploitation of mutualism by influencing partner fidelity feedback

Mutualism can be favored over exploitation of mutualism when interests of potential heterospecific partners are aligned so that individual organisms are beneficial to each others' continued growth, survival, and reproduction, that is, when exploitation of a particular partner individual is costly. A coral reef sponge system is particularly amenable to field experiments probing how costs of exploitation can be influenced by life-history characteristics. Pairwise associations among three of the sponge species are mutually beneficial. A fourth species, Desmapsamma anchorata, exploits these mutualisms. Desmapsamma also differs from the other species by growing faster, fragmenting more readily, and suffering higher mortality rates. Evaluating costs and benefits of association in the context of the complex life histories of these asexually fragmenting sponges shows costs of exploitation to be high for the mutualistic species but very low for this essentially weedy species. Although it benefits from association more than the mutualist species, by relying on their superior tensile strength and extensibility to reduce damage by physical disturbance, exploitation is favored because each individual host is of only ephemeral use. These sponges illustrate how life-history differences can influence the duration of association between individuals and, thus, the role of partner fidelity in promoting mutualism.     

The evolution of plant-insect mutualisms

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

Context dependence in the coevolution of plant and rhizobial mutualists

Several mechanisms are expected to rapidly rid mutualisms of genetic variation in partner quality. Variation for mutualist quality, however, appears to be widespread. We used a model legume-rhizobium mutualism to test for evidence that context-dependent selection may maintain variation in partner quality. In a greenhouse experiment using 10 natural populations of Medicago truncatula and two strains of Sinorhizobium medicae, we detected significant genotype x genotype (G x G) interactions for plant fitness, indicating that the most beneficial rhizobium strain depends on the host genotype. In a second experiment using a subset of the plant populations used in the first experiment, we detected significant G x G interactions for both plant and rhizobium fitness. Moreover, the plant population with which rhizobium strains gained the greatest benefit depended on the nitrogen environment. Finally, we found that in a high nitrogen environment, all plant populations had lower fitness when inoculated with a 1:1 mixture of strains than with the worse single strain alone, suggesting that nitrogen shifts the exchange of benefits in favour of rhizobia. Our data suggest that genotype, nitrogen and biotic dependency might contribute to the maintenance of genetic variation in mutualist quality when coupled with spatial or temporal heterogeneity in the environment.     

Plant chemical defence: a partner control mechanism stabilising plant - seed-eating pollinator mutualisms

Background  

Mutualisms are inherently conflictual as one partner always benefits from reducing the costs imposed by the other. Despite the widespread recognition that mutualisms are essentially reciprocal exploitation, there are few documented examples of traits that limit the costs of mutualism. In plant/seed-eating pollinator interactions the only mechanisms reported so far are those specific to one particular system, such as the selective abortion of over-exploited fruits.     

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.     

A general framework for effectiveness concepts in mutualisms

A core interest in studies of mutualistic interactions is the ‘effectiveness’ of mutualists in providing benefits to their partners. In plant‐animal mutualisms it is widely accepted that the total effect of a mutualist on its partner is estimated as (1) a ‘quantity’ component multiplied by (2) a ‘quality’ component, although the meanings of ‘effectiveness,’ ‘quantity,’ and ‘quality’ and which terms are applied to these metrics vary greatly across studies. In addition, a similar quantity × quality = total effect approach has not been applied to other types of mutualisms, although it could be informative. Lastly, when a total effect approach has been applied, it has invariably been from a phytocentric perspective, focussing on the effects of animal mutualists on their plant partner. This lack of a common framework of ‘effectiveness’ of mutualistic interactions limits generalisation and the development of a broader understanding of the ecology and evolution of mutualisms. In this paper, we propose a general framework and demonstrate its utility by applying it to both partners in five different types of mutualisms: pollination, seed dispersal, plant protection, rhizobial, and mycorrhizal mutualisms. We then briefly discuss the flexibility of the framework, potential limitations, and relationship to other approaches.     

Kin selection and the Evolution of Mutualisms between Species

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