The evolution of mutualism

Like altruism, mutualism, cooperation between species, evolves only by enhancing all participants' inclusive fitness. Mutualism evolves most readily between members of different kingdoms, which pool complementary abilities for mutual benefit: some of these mutualisms represent major evolutionary innovations. Mutualism cannot persist if cheating annihilates its benefits. In long-term mutualisms, symbioses, at least one party associates with the other nearly all its life. Usually, a larger host harbours smaller symbionts. Cheating is restrained by vertical transmission, as in Buchnera; partner fidelity, as among bull-thorn acacias and protective ants; test-based choice of symbionts, as bobtail squid choose bioluminescent bacteria; or sanctioning nonperforming symbionts, as legumes punish nonperforming nitrogen-fixing bacteria. Mutualisms involving brief exchanges, as among plants and seed-dispersers, however, persist despite abundant cheating. Both symbioses and brief-exchange mutualisms have transformed whole ecosystems. These mutualisms may be steps towards ecosystems which, like Adam Smith's ideal economy, serve their members' common good.     

Mutualism variation in the nodulation response to nitrate

The evolution of mutualisms under novel selective pressures will play a key role in ecosystem responses to environmental change. Because fixed nitrogen is traded in plant–rhizobium mutualisms, increasing N availability in the soil is predicted to alter coevolution of these interactions. Legumes typically decrease the number of associations (nodules) with rhizobia in response to nitrate, but the evolutionary dynamics of this response remain unknown. We grew plant and rhizobium genotype combinations in three N environments to assess the coevolutionary potential of the nodule nitrate response in natural communities of plants and rhizobia. We found evidence for coevolutionary genetic variation for nodulation in response to nitrate (G × G × E interaction), suggesting that the mutualism response to N deposition will depend on the combination of partner genotypes. Thus, the nitrate response is not a fixed mechanism in plant–rhizobium symbioses, but instead is potentially subject to natural selection and dynamic coevolution.     

Plant lock and ant key: pairwise coevolution of an exclusion filter in an ant-plant mutualism

Although observations suggest pairwise coevolution in specific ant-plant symbioses, coevolutionary processes have rarely been demonstrated. We report on, what is to the authors' knowledge, the strongest evidence yet for reciprocal adaptation of morphological characters in a species-specific ant-plant mutualism. The plant character is the prostoma, which is a small unlignified organ at the apex of the domatia in which symbiotic ants excavate an entrance hole. Each myrmecophyte in the genus Leonardoxa has evolved a prostoma with a different shape. By performing precise measurements on the prostomata of three related myrmecophytes, on their specific associated ants and on the entrance holes excavated by symbiotic ants at the prostomata, we showed that correspondence of the plant and ant traits forms a morphological and behavioural filter. We have strong evidence for coevolution between the dimensions and shape of the symbiotic ants and the prostoma in one of the three ant-Leonardoxa associations.     

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.     

Algal switching among lichen symbioses

Lichens are intimate and long-term symbioses of algae and fungi. Such intimate associations are often hypothesized to have undergone long periods of symbiotic interdependence and coevolution. However, coevolution has not been rigorously tested for lichen associations. In the present study we compared the nuclear internal transcribed spacer (ITS) phylogenies of algal and fungal partners from 33 natural lichen associations to test two aspects of coevolution, cospeciation and parallel cladogenesis. Since statistically significant incongruence between symbiont phylogenies rejected parallel cladogenesis and minimized cospeciation events, we conclude that switching of highly selected algal genotypes occurs repeatedly among these symbiotic lichen associations.     

Trait‐based partner selection drives mycorrhizal network assembly

Plants and their microbial symbionts are often found to interact non‐randomly in nature, but we have yet to understand the mechanisms responsible for such preferential species associations. Theory predicts that host plants should select symbiotic partners bearing traits complementary to their own, as this should favor cooperation and evolutionary stability of mutualisms. Here, we present the first field‐based empirical test for this hypothesis using arbuscular mycorrhizas (AM), the oldest and most widespread plant symbiosis. Preferential associations occurring within a local plant–AM fungal community could not be predicted by the spatial distributions of interacting partners, nor by gradients in soil properties. Rather, plants with similar traits preferentially hosted similar AM fungi and, likewise, phylogenetically related AM fungi (assumed to have similar functional traits) interacted with similar plants. Our results suggest that trait‐based partner selection may have been a strong force in maintaining plant–AM fungal symbioses since the evolution of land plants.     

Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity

Brood pollination mutualisms—interactions in which specialized insects are both the pollinators (as adults) and seed predators (as larvae) of their host plants—have been influential study systems for coevolutionary biology. These mutualisms include those between figs and fig wasps, yuccas and yucca moths, leafflowers and leafflower moths, globeflowers and globeflower flies, Silene plants and Hadena and Perizoma moths, saxifrages and Greya moths, and senita cacti and senita moths. The high reciprocal diversity and species‐specificity of some of these mutualisms have been cited as evidence that coevolution between plants and pollinators drives their mutual diversification. However, the mechanisms by which these mutualisms diversify have received less attention. In this paper, we review key hypotheses about how these mutualisms diversify and what role coevolution between plants and pollinators may play in this process. We find that most species‐rich brood pollination mutualisms show significant phylogenetic congruence at high taxonomic scales, but there is limited evidence for the processes of both cospeciation and duplication, and there are no unambiguous examples known of strict‐sense contemporaneous cospeciation. Allopatric speciation appears important across multiple systems, particularly in the insects. Host‐shifts appear to be common, and widespread host‐shifts by pollinators may displace other pollinator lineages. There is relatively little evidence for a “coevolution through cospeciation” model or that coevolution promotes speciation in these systems. Although we have made great progress in understanding the mechanisms by which brood pollination mutualisms diversify, many opportunities remain to use these intriguing symbioses to understand the role of biotic interactions in generating biological diversity.     

Plant-ants feed their host plant, but above all a fungal symbiont to recycle nitrogen

In ant-plant symbioses, plants provide symbiotic ants with food and specialized nesting cavities (called domatia). In many ant-plant symbioses, a fungal patch grows within each domatium. The symbiotic nature of the fungal association has been shown in the ant-plant Leonardoxa africana and its protective mutualist ant Petalomyrmex phylax. To decipher trophic fluxes among the three partners, food enriched in (13)C and (15)N was given to the ants and tracked in the different parts of the symbiosis up to 660 days later. The plant received a small, but significant, amount of nitrogen from the ants. However, the ants fed more intensively the fungus. The pattern of isotope enrichment in the system indicated an ant behaviour that functions specifically to feed the fungus. After 660 days, the introduced nitrogen was still present in the system and homogeneously distributed among ant, plant and fungal compartments, indicating efficient recycling within the symbiosis. Another experiment showed that the plant surface absorbed nutrients (in the form of simple molecules) whether or not it is coated by fungus. Our study provides arguments for a mutualistic status of the fungal associate and a framework for investigating the previously unsuspected complexity of food webs in ant-plant mutualisms.     

Dynamics of the association between a long-lived understory myrmecophyte and its specific associated ants

Myrmecophytic symbioses are widespread in tropical ecosystems and their diversity makes them useful tools for understanding the origin and evolution of mutualisms. Obligate ant–plants, or myrmecophytes, provide a nesting place, and, often, food to a limited number of plant–ant species. In exchange, plant–ants protect their host plants from herbivores, competitors and pathogens, and can provide them with nutrients. Although most studies to date have highlighted a similar global pattern of interactions in these systems, little is known about the temporal structuring and dynamics of most of these associations. In this study we focused on the association between the understory myrmecophyte Hirtella physophora (Chrysobalanaceae) and its obligate ant partner Allomerus decemarticulatus (Myrmicinae). An examination of the life histories and growth rates of both partners demonstrated that this plant species has a much longer lifespan (up to about 350 years) than its associated ant colonies (up to about 21 years). The size of the ant colonies and their reproductive success were strongly limited by the available nesting space provided by the host plants. Moreover, the resident ants positively affected the vegetative growth of their host plant, but had a negative effect on its reproduction by reducing the number of flowers and fruits by more than 50%. Altogether our results are important to understanding the evolutionary dynamics of ant–plant symbioses. The highly specialized interaction between long-lived plants and ants with a shorter lifespan produces an asymmetry in the evolutionary rates of the interaction which, in return, can affect the degree to which the interests of the two partners converge.     

Ants suppressing plant pathogens: a review

Ant–plant mutualisms are usually regarded as driven by ants defending plants against herbivores in return for plant‐produced food rewards and housing. However, ants may provide additional services. In a review of published studies on ant–pathogen–plant interactions, we investigated whether ants’ extensive hygiene measures, including the use of ant‐produced antibiotics, extend to their host plants and reduce plant pathogen loads. From 30 reported species combinations, we found that the presence of ants lead to reduced pathogen levels in 18 combinations and to increased levels in 6. On average, ants significantly reduced pathogen incidence with 59%. This effect size did not differ significantly from effect sizes reported from meta‐analyses on herbivore protection. Thus, pathogen and herbivore protection could be of equal importance in ant–plant mutualisms. Considering the abundance of these interactions, ecological impacts are potentially high. Furthermore, awareness of this service may stimulate the development of new measures to control plant diseases in agriculture. It should be noted, though, that studies were biased toward tropical ant–plant symbioses and that the literature in the field is limited at present. Future research on plant pathogens is needed to enhance our understanding of ant–plant mutualisms and their evolution.     

Multiple effects of mutualistic ants improve the performance of a neotropical ant-plant: A long-term study with the Cecropia-Azteca system

Comprehension of the benefits involved in mutualisms is crucial to disentangle the role of interactions in the structure and functioning of populations, communities and ecosystems. In ant-plant mutualisms, benefits provided by plants to ants are immediately recognizable, but reverse benefits are less obvious, conditional and accumulate over longer time spans. Here we tested the hypothesis that the ant Azteca muelleri simultaneously provides multiple benefits to its host plant (Cecropia glaziovii), ultimately increasing plant performance. We planted seedlings and experimentally prevented ant colonization for half of them. Over 4.5 years we quantified the effects of ant presence or absence on plant growth, herbivory levels, fungal infection, fertilization via ant debris and changes in defense strategies. Ant colonization increased plant height by 125% compared to ant-free plants. Such an improvement in plant performance can be explained because plants with ants faced less herbivory, lower prevalence of pathogenic fungi, invested less in foliar trichomes and had more foliar nitrogen. We thus confirmed that ant mutualists provide cumulative benefits including nutritional benefits, effective defense and lower investment into other defenses – which result in increased plant growth. We highlight the importance of long-term experiments that simultaneously evaluate a multiplicity of potential ant effects to better understand their relative contribution to the performance of the mutualistic partner.     

Standing genetic variation in host preference for mutualist microbial symbionts

Many models of mutualisms show that mutualisms are unstable if hosts lack mechanisms enabling preferential associations with mutualistic symbiotic partners over exploitative partners. Despite the theoretical importance of mutualism-stabilizing mechanisms, we have little empirical evidence to infer their evolutionary dynamics in response to exploitation by non-beneficial partners. Using a model mutualism—the interaction between legumes and nitrogen-fixing soil symbionts—we tested for quantitative genetic variation in plant responses to mutualistic and exploitative symbiotic rhizobia in controlled greenhouse conditions. We found significant broad-sense heritability in a legume host''s preferential association with mutualistic over exploitative symbionts and selection to reduce frequency of associations with exploitative partners. We failed to detect evidence that selection will favour the loss of mutualism-stabilizing mechanisms in the absence of exploitation, as we found no evidence for a fitness cost to the host trait or indirect selection on genetically correlated traits. Our results show that genetic variation in the ability to preferentially reduce associations with an exploitative partner exists within mutualisms and is under selection, indicating that micro-evolutionary responses in mutualism-stabilizing traits in the face of rapidly evolving mutualistic and exploitative symbiotic bacteria can occur in natural host populations.     

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.     

The Evolution of Insect-Fungus Associations: From Contact to Stable Symbiosis

Insect-fungus interactions range from agonistic to mutualistic,and include several spectacular examples of complex symbioses.A potential benefit of mycophagy (the ingestion of fungal tissue)is the augmentation of digestive capacity by the ingestion offungal enzymes that remain active in the gut following ingestion.Cellulose digestion is mediated by ingested fungal enzymes inthe wood-boring larvae of cerambycid beetles and siricid woodwasps,in detritus-feeding stonefly nymphs, and in the workers of fungus-growingtermites. In this paper I discuss a plausible scenario for theevolution of stable symbiotic insect-fungus associations, inwhich the augmentation of digestive capacity through the ingestionof fungal enzymes is an important factor leading to the establishmentof interdependence between the interacting partners in a mutualism.Ingested fungal enzymes play a different role in the mutualisticassociation of the attine ants and their symbiotic fungi. Analyses of the associations of the siricid woodwasps, fungus-growingtermites, and fungus-growing ants with their symbiotic fungipermit the testing of Law's (1985) predictions concerning theconsequences of evolution in a mutualistic environment. As predicted,the rate of speciation has been slower in the protected partnerthan in the host partner, selection has favored asexual reproductionin the protected partner, and, at least in the attine ant-fungussymbiosis, the protected partner exhibits a low degree of specificitytoward different host species. Insect-fungus interactions provide rich material for the studyof both mechanistic and theoretical aspects of mutualism.     

Evolutionary stability in a 400-million-year-old heritable facultative mutualism

Many eukaryotes interact with heritable endobacteria to satisfy diverse metabolic needs. Some of these interactions are facultative symbioses, in which one partner is not essential to the other. Facultative symbioses are expected to be transitional stages along an evolutionary trajectory toward obligate relationships. We tested this evolutionary theory prediction in Ca. Glomeribacter gigasporarum, nonessential endosymbionts of arbuscular mycorrhizal fungi (Glomeromycota). We found that heritable facultative mutualisms can be both ancient and evolutionarily stable. We detected significant patterns of codivergence between the partners that we would only expect in obligate associations. Using codiverging partner pairs and the fungal fossil record, we established that the Glomeromycota-Glomeribacter symbiosis is at least 400 million years old. Despite clear signs of codivergence, we determined that the Glomeribacter endobacteria engage in recombination and host switching, which display patterns indicating that the association is not evolving toward reciprocal dependence. We postulate that low frequency of recombination in heritable endosymbionts together with host switching stabilize facultative mutualisms over extended evolutionary times.     

Evolutionary Dynamics of Nitrogen Fixation in the Legume–Rhizobia Symbiosis

The stabilization of host–symbiont mutualism against the emergence of parasitic individuals is pivotal to the evolution of cooperation. One of the most famous symbioses occurs between legumes and their colonizing rhizobia, in which rhizobia extract nutrients (or benefits) from legume plants while supplying them with nitrogen resources produced by nitrogen fixation (or costs). Natural environments, however, are widely populated by ineffective rhizobia that extract benefits without paying costs and thus proliferate more efficiently than nitrogen-fixing cooperators. How and why this mutualism becomes stabilized and evolutionarily persists has been extensively discussed. To better understand the evolutionary dynamics of this symbiosis system, we construct a simple model based on the continuous snowdrift game with multiple interacting players. We investigate the model using adaptive dynamics and numerical simulations. We find that symbiotic evolution depends on the cost–benefit balance, and that cheaters widely emerge when the cost and benefit are similar in strength. In this scenario, the persistence of the symbiotic system is compatible with the presence of cheaters. This result suggests that the symbiotic relationship is robust to the emergence of cheaters, and may explain the prevalence of cheating rhizobia in nature. In addition, various stabilizing mechanisms, such as partner fidelity feedback, partner choice, and host sanction, can reinforce the symbiotic relationship by affecting the fitness of symbionts in various ways. This result suggests that the symbiotic relationship is cooperatively stabilized by various mechanisms. In addition, mixed nodule populations are thought to encourage cheater emergence, but our model predicts that, in certain situations, cheaters can disappear from such populations. These findings provide a theoretical basis of the evolutionary dynamics of legume–rhizobia symbioses, which is extendable to other single-host, multiple-colonizer systems.     

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.     

The resource-mediated modular structure of a non-symbiotic ant–plant mutualism

1. Plant–animal mutualisms are key processes that influence community structure, dynamics, and function. They reflect several neutral and niche-based mechanisms related to plant–animal interactions. 2. However, the strength with which these processes influence community structure depends on functional traits that influence the interactions between mutualistic partners. In mutualisms involving plants and ants, nectar is the most common reward, and traits such as quantity and quality can affect ant species' responses by influencing their recruitment rates and aggressiveness. 3. In this study, nectar traits that mediate ant–plant defensive mutualisms were manipulated to test whether resource quantity and quality affect the structure of ant–plant interaction networks. A downscaling approach was used to investigate the interaction network between ant species and individual plants of the extrafloral nectary-bearing terrestrial orchid Epidendrum secundum. 4. We found a short-term reorganization of the ant assemblage that caused the interaction networks to become more specialised and modular in response to a more rewarding nectar gradient. Furthermore, the ant species tended to narrow their foraging range by limiting their associations to one or a few individual plants. 5. This study shows that ant species' responses to variable resource traits play an important role in the structure of the ant–plant interaction network. We suggest that more rewarding nectar enhanced aggressiveness and a massive recruitment of some ant species, leading to lower niche overlap and thus a less connected and more specialised network.     

The Evolution of Communication in Two Ant-Plant Mutualisms

Myrmecophytes are plants that provide nesting sites and food to ants that protect them against herbivores. Plant signals function to synchronize ant patrolling with the probability of herbivory. We compared the communication signals in two symbioses involving ant and plant pairs that are closely related. The two plants emitted the same volatile compounds upon damage. These compounds are simple molecules common in the plant kingdom. Electroantennography revealed that the two symbiotic ants, as well as several other ant species, were able to perceive these compounds. However, workers of one species responded only to hexanal, while those of the other species responded mostly to methyl salicylate. The two signals involved in the focal symbioses are ‘cheap’ (low metabolic cost), which is consistent with theoretical predictions for the evolution of signalling between partners with convergent interests. They are also not specific, which is expected between plants and broad-spectrum predators such as ants. The fact that different signals are used in the two sister symbioses suggests different mechanisms underlying similar adaptations in the evolution of communication.     

Conflict, cheats and the persistence of symbioses

Many symbioses are widespread, abundant, and evolutionarily persistent. This is despite unambiguous evidence for conflict between the partners and the existence of cheats that use benefits derived from their partners while providing reduced or no services in return. Evidence from a diversity of associations suggests that symbioses are robust to cheating in several ways. Some symbioses persist despite conflict and cheating because of the selective advantage of cost-free interactions (also known as byproduct mutualistic interactions), which incur no conflict. There is also evidence for the suppression of cheating by sanctions imposed by partners in some symbioses, and vertical transmission has been shown experimentally to promote traits that enhance partner performance. It is argued that these processes contribute to the apparent rarity of evolutionary transitions from symbiosis to parasitism. There is strong phylogenetic evidence for the evolutionary reversion of various symbiotic organisms to free-living lifestyles, but at least some of these transitions can be attributed to selection pressures other than within-symbiosis conflict. The principal conclusion is that, although conflict is common in symbioses, it is generally managed and contained.