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

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

Host discrimination in modular mutualisms: a theoretical framework for meta-populations of mutualists and exploiters

Plants in multiple symbioses are exploited by symbionts that consume their resources without providing services. Discriminating hosts are thought to stabilize mutualism by preferentially allocating resources into anatomical structures (modules) where services are generated, with examples of modules including the entire inflorescences of figs and the root nodules of legumes. Modules are often colonized by multiple symbiotic partners, such that exploiters that co-occur with mutualists within mixed modules can share rewards generated by their mutualist competitors. We developed a meta-population model to answer how the population dynamics of mutualists and exploiters change when they interact with hosts with different module occupancies (number of colonists per module) and functionally different patterns of allocation into mixed modules. We find that as module occupancy increases, hosts must increase the magnitude of preferentially allocated resources in order to sustain comparable populations of mutualists. Further, we find that mixed colonization can result in the coexistence of mutualist and exploiter partners, but only when preferential allocation follows a saturating function of the number of mutualists in a module. Finally, using published data from the fig–wasp mutualism as an illustrative example, we derive model predictions that approximate the proportion of exploiter, non-pollinating wasps observed in the field.     

Interspecific competition in perennial sedentary organisms: An individual-based model

We investigated a mathematical model of the dynamics of the ecological system consisting of two competing perennial species, each of which leads a sedentary life. It is an individual-based model, in which the growth of each individual is described. The rate of this growth is weakened by competition from neighboring individuals. The strength of the competitors' influence depends on their size and distance to them. The conditions, in which the competitive exclusion of one of the competitors and the coexistence of both competitors take place are provided. The influence of the parameters responsible for the strength of competition, the degree of competitive asymmetry, and consideration of the importance of specific elements of the spatial structure of this ecological system on the results of the competition were analyzed. Both species co-exist when they are equal competitors. Permanent coexistence is possible only when interspecific competition is weaker than intraspecific. When interspecific competition is stronger, the coexistence of equal interspecific competitors is random. Both species have equal probability of extinction. If species are not equal competitors, the stronger one wins. This result can be modified by different strengths of intraspecific competition. The weaker interspecific competitor can permanently coexist with stronger one, when its individuals suffer stronger intraspecific competition.     

非传粉小蜂的食性及其对榕树-传粉小蜂系统稳定性的影响

榕树与其传粉小蜂形成了高度专一的互惠共生系统。非传粉小蜂则是该系统的资源掠夺者,但它与该系统共存的机制仍不清楚。于2003年12月-2004年4月在西双版纳以聚果榕（Ficus racemosa L．）为材料,研究了寄生在聚果榕榕果内的5种非传粉小蜂的食性及相互关系,以探讨非传粉小蜂与榕树-传粉小蜂系统共存的机制。结果表明：寄生在聚果榕榕果内的5种非传粉小蜂中,仅Platyneura testacea Motschulsky和Platyneura,mayri Rasplus能刺激子房发育成瘿花,是造瘿者;Apocrypta sp．,Apocrypta westwoodi Grandi和Platyneura agraensis Joseph不能刺激子房发育成瘿花,是拟寄生者。传粉小蜂的拟寄生者和造瘿者对传粉小蜂有负的影响。但在蚂蚁和造瘿者的拟寄生蜂作用下,这种负面影响并不显著,而且它们对榕树繁殖没有显著影响。对小蜂自然种群的分析表明,传粉小蜂处于优势地位。说明在自然情况下传粉小蜂的拟寄生者和造瘿者的种群维持在一个较低水平,对榕树一传粉小蜂系统稳定性影响较小,故能与之长期共存。     

Cheating and the evolutionary stability of mutualisms

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

Persistence of mutualisms with bidirectional interactions in a two-species system

In Lotka–Volterra equations (LVEs) of mutualisms, population densities of mutualists will increase infinitely if the mutualisms between them are strong, which is called the divergence problem. In order to avoid the problem, a mutualism system of two species is analyzed in this work. The model is derived from reactions on lattice and has a form similar to that of LVEs. Population densities of species will not increase infinitely because of spatial limitation on the lattice. Stability analysis of the model demonstrates basic mechanisms by which the mutualisms lead to coexistence/extinction of the species. When in coexistence, intermediate mutualistic effect is shown to lead to the maximal density in certain parameter ranges, while a strong or weak mutualistic effect is not so good. Furthermore, the stability analysis exhibits that extremely strong/weak mutualisms will result in extinction of one/both species.     

Interference competition and species coexistence

Interference competition is ubiquitous in nature. Yet its effects on resource exploitation remain largely unexplored for species that compete for dynamic resources. Here, I present a model of exploitative and interference competition with explicit resource dynamics. The model incorporates both biotic and abiotic resources. It considers interference competition both in the classical sense (i.e. each species suffers a net reduction in per capita growth rate via interference from, and interference on, the other species) and in the broad sense (i.e. each species suffers a net reduction in per capita growth rate via interference from, but can experience an increase in growth rate via interference on, the other species). Coexistence cannot occur under classical interference competition even when the species inferior at resource exploitation is superior at interference. Such a trade-off can, however, change the mechanism of competitive exclusion from dominance by the superior resource exploiter to a priority effect. Now the inferior resource exploiter can exclude the superior resource exploiter provided it has a higher initial abundance. By contrast, when interference is beneficial to the interacting species, coexistence is possible via a trade-off between exploitation and interference. These results hold regardless of whether the resource is biotic or abiotic, indicating that the outcome of exploitative and interference competition does not depend on the exact nature of resource dynamics. The model makes two key predictions. First, species that engage in costly interference mechanisms (e.g. territoriality, overgrowth or undercutting, allelopathy and other forms of chemical competition) should not be able to coexist unless they also engage in beneficial interference mechanisms (e.g. predation or parasitism). Second, exotic invasive species that displace native biota should be superior resource exploiters that have strong interference effects on native species with little or negative cost. The first prediction provides a potential explanation for patterns observed in several natural systems, including plants, aquatic invertebrates and insects. The second prediction is supported by data on invasive plants and vertebrates.     

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

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

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

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

The exploitation of mutualisms

Mutualisms (interspecific cooperative interactions) are ubiquitously exploited by organisms that obtain the benefits mutualists offer, while delivering no benefits in return. The natural history of these exploiters is well-described, but relatively little effort has yet been devoted to analysing their ecological or evolutionary significance for mutualism. Exploitation is not a unitary phenomenon, but a set of loosely related phenomena: exploiters may follow mixed strategies or pure strategies at either the species or individual level, may or may not be derived from mutualists, and may or may not inflict significant costs on mutualisms. The evolutionary implications of these different forms of exploitation, especially the threats they pose to the stability of mutualism, have as yet been minimally explored. Studies of this issue are usually framed in terms of a "temptation to defect" that generates a destabilizing conflict of interest between partners. I argue that this idea is in fact rather inappropriate for interpreting most observed forms of exploitation in mutualisms. I suggest several alternative and testable ideas for how mutualism can persist in the face of exploitation.     

Pollination outcomes reveal negative density‐dependence coupled with interspecific facilitation among plants

Pollination is thought to be under positive density‐dependence, destabilising plant coexistence by conferring fitness disadvantages to rare species. Such disadvantage is exacerbated by interspecific competition but can be mitigated by facilitation and intraspecific competition. However, pollinator scarcity should enhance intraspecific plant competition and impose disadvantage on common over rare species (negative density‐dependence, NDD). We assessed pollination proxies (visitation rate, pollen receipt, pollen tubes) in a generalised plant community and related them to conspecific and heterospecific density, expecting NDD and interspecific facilitation due to the natural pollinator scarcity. Contrary to usual expectations, all proxies indicated strong intraspecific competition for common plants. Moreover interspecific facilitation prevailed and was stronger for rare than for common plants. Both NDD and interspecific facilitation were modulated by specialisation, floral display and pollinator group. The combination of intraspecific competition and interspecific facilitation fosters plant coexistence, suggesting that pollination can be a niche axis maintaining plant diversity.     

Variation in mycorrhizal growth response influences competitive interactions and mechanisms of plant species coexistence

Plant species vary in their growth response to arbuscular mycorrhizal (AM) fungi, with responses ranging from negative to positive. Differences in response to AM fungi may affect competition between plant species, influencing their ability to coexist. We hypothesized that positively responding species, whose growth is stimulated by AM fungi, will experience stronger intraspecific competition and weaker interspecific competition in soil containing AM fungi, while neutrally or negatively responding species should experience weaker intraspecific and stronger interspecific competition. We grew Plantago lanceolata, which responds positively to AM fungi, and Bromus inermis, which responds negatively to AM fungi, in an additive response surface competition experiment that varied the total density and relative frequency of each species. Plants were grown in sterilized background soil that had been inoculated with whole soil biota, which includes AM fungi, or a microbial wash, that contained other soil microbes but no AM fungi, or in sterilized soil that contained no biota. The positively responding P. lanceolata was more strongly limited by intraspecific than interspecific competition when AM fungi were present. By contrast, the presence of AM fungi decreased the strength of intraspecific competition experienced by the negatively responding B. inermis. Because AM fungi are almost always present in soil, strong intraspecific competition in positively responding species would prevent them from outcompeting species that respond neutrally or negatively to AM fungi. The potential for increased intraspecific competition to offset growth benefits of AM fungi could, therefore, be a stabilizing mechanism that promotes coexistence among plant species.     

Competition and coexistence in plant communities: intraspecific competition is stronger than interspecific competition

Theory predicts that intraspecific competition should be stronger than interspecific competition for any pair of stably coexisting species, yet previous literature reviews found little support for this pattern. We screened over 5400 publications and identified 39 studies that quantified phenomenological intraspecific and interspecific interactions in terrestrial plant communities. Of the 67% of species pairs in which both intra‐ and interspecific effects were negative (competitive), intraspecific competition was, on average, four to five‐fold stronger than interspecific competition. Of the remaining pairs, 93% featured intraspecific competition and interspecific facilitation, a situation that stabilises coexistence. The difference between intra‐ and interspecific effects tended to be larger in observational than experimental data sets, in field than greenhouse studies, and in studies that quantified population growth over the full life cycle rather than single fitness components. Our results imply that processes promoting stable coexistence at local scales are common and consequential across terrestrial plant communities.     

Active dispersal is differentially affected by inter‐ and intraspecific competition in closely related nematode species

Competition is one of the main drivers of dispersal, which can be an important mechanism to achieve permanent or temporal coexistence of multiple species. This coexistence can be achieved by a dispersal‐competition tradeoff, spatial store effects or neutral dynamics. Here we test the effect of inter‐ and intraspecific competition on dispersal of four species of the marine nematode species complex Litoditis marina. A previous study in closed microcosms without a possibility for dispersal had demonstrated pronounced interspecific competition, leading to the exclusion of one species. We now investigated whether 1) the dispersal is affected by interspecific interactions, by intraspecific competition (density) or by food availability, 2) the dispersal dynamics influence assemblage composition and can lead to co‐occurrence of the species, and 3) the abiotic environment (here salinity) can affect these dynamics. We show that density is the main driver for dispersal in two of the four species. Dispersal of a third species always started at the same time irrespective of density, whereas in the fourth species interspecific interactions accelerated dispersal. Remarkably, this fourth species was not a strong competitor, suggesting that a dispersal–competition tradeoff does not explain the observed coexistence. Salinity did not alter the timing of dispersal when interspecific interactions were present but did affect assemblage composition. Consequently, spatial store effects may influence coexistence. All four species co‐occurred in fairly stable abundances throughout the present experiment indicating the importance of species specific dispersal strategies for coexistence. Co‐occurrence can be facilitated because competition is postponed or avoided by dispersal. Neutral dynamics also played a role as intra‐ and interspecific competition were of similar importance in three of the four species. We conclude that dispersal is a driver of the coexistence of closely related nematode species, and that population density and interspecific interactions shape these dynamics.     

Global stability of obligate mutualism in community modules with facultative mutualists

Mutualism is a fundamental building block of ecological communities and an important driver of biotic evolution. Classic theory suggests that a pairwise two‐species obligate mutualism is fragile, with a large perturbation potentially driving both mutualist populations into extinction. In nature, however, there are many cases of pairwise obligate mutualism. Such pairwise obligate mutualisms are occasionally associated with additional interactions with facultative mutualists. Here, we use a mathematical model to show that when a two‐species obligate mutualism has a single additional link to a third facultative mutualist, the obligate mutualism can become permanently persistent. In the model, a facultative mutualist interacts with one of two inter‐dependent obligate mutualists, and the facultative mutualist enhances the persistence not only of its directly interacting obligate mutualist, but also that of the other obligate mutualist indirectly, enabling the permanent coexistence of the three mutualist species. The effect of the facultative mutualist is strong; it can allow a three‐species permanent coexistence even when two obligate mutualists by themselves are not sustainable (i.e. not locally stable). These results suggest that facultative mutualists can play a pivotal role for the persistence of obligate mutualisms, and contribute to a better understanding on the mechanisms maintaining more complex mutualistic networks of multiple species.     

Proteases hold the key to an exclusive mutualism

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

Competition and coexistence with multiple life-history stages

Do complex life histories affect the conditions under which competitors can coexist? We investigated this using a two-species, two-stage Ricker model. With complex life cycles, the competition coefficients associated with each life-history stage suggest one of three competitive outcomes-coexistence, alternate stable states, or competitive exclusion-that depend on the relative magnitudes of intraspecific and interspecific competition. When the two stages suggest the same outcome, only that outcome can occur. When the stages suggest different outcomes, either one may prevail. It is also possible to have emergent outcomes, in which the outcome is not suggested by either stage. This can occur when the two stages suggest competitive exclusion by opposite species or when one stage suggests alternate stable states and the other suggests coexistence. Therefore, determining the mechanisms of coexistence in species with complex life histories may require consideration of competitive interactions within all life-history stages.     

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

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

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

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

Competition and evolutionary stability of plants in a spatially structured habitat

We modelled the population dynamics of two types of plants with limited dispersal living in a lattice structured habitat. Each site of the square lattice model was either occupied by an individual or vacant. Each individual reproduced to its neighbors. We derived a criterion for the invasion of a rare type into a population composed of a resident type based on a pair-approximation method, in which the dynamics of both average densities and the nearest neighbor correlations were considered. Based on this invasibility criterion, we showed that, when there is a tradeoff between birth and death rates, the evolutionarily stable type is the one that has the highest ratio of birth rate to mortality. If these types are different species, they form segregated spatial patterns in the lattice model in which intraspecific competitive interactions occur more frequently than interspecific interactions. However, stable coexistence is not possible in the lattice model contrary to results from completely mixed population models. This clearly shows that the casual conclusion, based on traditional well mixed population models, that different species can coexist if intraspecific competition is stronger than interspecific competition, does not hold for spatially structured population models.