Parabiotic ants: the costs and benefits of symbiosis

1. Mutualisms are important drivers of co‐evolution and speciation. However, they typically imply costs for one or both partners. Each partner consequently tries to maximise benefits and minimise costs. Mutualisms can therefore develop towards commensalism or parasitism if one partner fails to provide sufficient benefits. This is particularly likely in diffuse interactions, where multiple species can associate with each other. If costs and benefits of a species vary with the identity of the partner species, this may result in a geographical mosaic of co‐evolution. 2. In the present study, inter‐specific interactions in two parabiotic associations of ants were studied (Hymenoptera: Formicidae). One Crematogaster species was associated with one of two closely related Camponotus species. We assessed cost and benefits by studying behavioural interactions, foraging behaviour, and nest defence in the associations. 3. While parabioses had been shown to be mutualistic, evidence was found for exploitation and aggressive competition between species. In spite of apparent costs of being exploited, we found no benefits for one partner (Crematogaster). The magnitude of potential costs to Crematogaster varied between the two Camponotus species. 4. We conclude that the cost/benefit ratio for Crematogaster varies between the two Camponotus partners, and between environmental conditions. Parabiosis can thus fluctuate between mutualism, commensalism, and parasitism, with Crematogaster being the species that may have higher costs than benefits. 5. We suggest that geneflow in the Crematogaster population hinders local adaptation to the resulting mosaic of locally varying selection pressures. This study demonstrates how diffuse interactions and environmental variation can result in a complex of local selection pressures.     

Adapt or disperse: understanding species persistence in a changing world

The majority of studies on environmental change focus on the response of single species and neglect fundamental biotic interactions, such as mutualism, competition, predation, and parasitism, which complicate patterns of species persistence. Under global warming, disruption of community interactions can arise when species differ in their sensitivity to rising temperature, leading to mismatched phenologies and/or dispersal patterns. To study species persistence under global climate change, it is critical to consider the ecology and evolution of multispecies interactions; however, the sheer number of potential interactions makes a full study of all interactions unfeasible. One mechanistic approach to solving the problem of complicated community context to global change is to (i) define strategy groups of species based on life‐history traits, trophic position, or location in the ecosystem, (ii) identify species involved in key interactions within these groups, and (iii) determine from the interactions of these key species which traits to study in order to understand the response to global warming. We review the importance of multispecies interactions looking at two trait categories: thermal sensitivity of metabolic rate and associated life‐history traits and dispersal traits of species. A survey of published literature shows pronounced and consistent differences among trophic groups in thermal sensitivity of life‐history traits and in dispersal distances. Our approach increases the feasibility of unraveling such a large and diverse set of community interactions, with the ultimate goal of improving our understanding of community responses to global warming.     

Effects of parasitoid fecundity and host resistance on indirect interactions among hosts sharing a parasitoid

We examine the effects of fecundity‐limited attack rates and resistance of hosts to parasitism on the dynamics of two‐host–one‐parasitoid systems. We focus primarily on the situation where one parasitoid species attacks two host species that differ in their suitability for parasitism. While all eggs allocated to suitable hosts develop into adult parasitoids, some of the eggs allocated to marginal host do not develop. Marginal hosts can therefore act as a sink for parasitoid eggs. Three‐species coexistence is favoured by low levels of parasitoid fecundity and by low levels of suitability of the marginal host. Our model also produces an indirect (+, ?) interaction in which the suitable host can benefit from the presence of the marginal host, but the marginal host suffers from the presence of the suitable host. The mechanism driving the indirect (+, ?) interaction is egg limitation of parasitoids incurred by allocating eggs to marginal hosts.     

Selective feedback between dispersal distance and the stability of mutualism

The evolution and maintenance of mutually beneficial interactions has been one of the oldest problems for evolutionary theory. For cooperation to be stable, mechanisms such as spatial population structure must exist that prevent non‐cooperative individuals from invading cooperative groups. Selection for certain traits like increased dispersal can erode that structure. Here, I used a spatially explicit individual based dual lattice computer simulation to investigate how the evolution of dispersal interacts with the evolution of mutualism and how this interaction affects the stability of mutualism in the face of non‐mutualists. I ran simulations manipulating the self‐structuring phenotype, dispersal distance, over a range of environmental conditions, as well as letting both dispersal and mutualism evolve independently, with and without a cost of dispersal. I found that environmental productivity is negatively correlated with the stability of mutualism, and that the stability of mutualism relied on the ability of mutualists to evolve shorter dispersal distances than non‐mutualists. The inclusion of a dispersal cost essentially fixed the upper limit of dispersal, and therefore limits the ability of non‐mutualists to evolve higher average dispersal than mutualists, but as costs are relaxed, the differences are recovered. These results show how selection on seemingly unrelated traits can align suites of traits into holistic life history strategies.     

Evolutionary double suicide in symbiotic systems

Mutualism is thought to face a threat of coextinction cascade because the loss of a member species could lead to the extinction of the other member. Despite this common emphasis on the perils of such knock-on effect, hitherto, the evolutionary causes leading to extinction have been less emphasised. Here, we examine how extinction could be triggered in mutualism and whether an evolutionary response to partner loss could prevent collateral extinctions, by theoretically examining the coevolution of the host exploitation by symbionts and host dependence on symbiosis. Our model reveals that mutualism is more vulnerable to co-extinction through adaptive evolution (evolutionary double suicide) than parasitism. Additionally, it shows that the risk of evolutionary double suicide rarely promotes the backward evolution to an autonomous (non-symbiotic) state. Our results provide a new perspective on the evolutionary fragility of mutualism and the rarity of observed evolutionary transitions from mutualism to parasitism.     

榕树-榕小蜂互惠合作系统中的非对称性博弈

榕树及其传粉榕小蜂是自然界中目前所知道的关系最为紧密的互利共生系统之一。随着研究的深入, 越来越多的证据发现榕树-传粉榕小蜂之间互惠合作的过程中存在着复杂的竞争和对抗关系, 例如榕树与传粉榕小蜂之间对公共资源的竞争、传粉欺骗与宿主对传粉者的惩罚、榕树与传粉小蜂之间的“军备竞赛”等。在相互竞争或者对抗关系中, 双方表现出非对称性相互作用。其非对称性关系主要表现出如下3个特征: (1)收益不对称, 即榕树(宿主)与传粉榕小蜂(共生体)之间在资源利用等方面的实力不对称; (2)榕树与传粉榕小蜂之间的信息不对称; (3)进化速率不对称。这些非对称的相互作用可能导致种群的波动、榕树与传粉榕小蜂相互适应和进化策略的变化。因此, 理解榕树与传粉榕小蜂之间的非对称交互作用有助于理解为什么合作和冲突在互利共生关系中经常能同时存在, 也将有助于解释榕树-传粉榕小蜂种间相互关系和物种的多样性。     

Evolutionary responses to climate change in parasitic systems

Species may respond to climate change in many ecological and evolutionary ways. In this simulation study, we focus on the concurrent evolution of three traits in response to climate change, namely dispersal probability, temperature tolerance (or niche width), and temperature preference (optimal habitat). More specifically, we consider evolutionary responses in host species involved in different types of interaction, that is parasitism or commensalism, and for low or high costs of a temperature tolerance–fertility trade‐off (cost of generalization). We find that host species potentially evolve all three traits simultaneously in response to increasing temperature but that the evolutionary response interacts and may be compensatory depending on the conditions. The evolutionary adjustment of temperature preference is slower in the parasitism than in commensalism scenario. Parasitism, in turn, selects for higher temperature tolerance and increased dispersal. High costs for temperature tolerance (i.e. generalization) restrict evolution of tolerance and thus lead to a faster response in temperature preference than that observed under low costs. These results emphasize the possible role of biotic interactions and the importance of ‘multidimensional’ evolutionary responses to climate change.     

Reversal of mutualism in a leafflower–leafflower moth association: the possible driving role of a third‐party partner

A major goal in the study of mutualism is to understand how co‐operation is maintained when mutualism may potentially turn into parasitism. Although certain mechanisms facilitate the persistence of mutualism, parasitic species have repeatedly evolved from mutualistic ancestors. However, documented examples of mutualism reversals are still rare. Leafflowers (Phyllantheae; Phyllanthaceae) include approximately 500 species that engage in obligate mutualism with leafflower moths (Epicephala; Gracillariidae), which actively pollinate flowers, and whose larvae feed on the resulting seeds. We found that the Taiwanese population of the Phyllanthus reticulatus species complex was associated with six sympatric Epicephala species, of which three were derived parasites that induced gall formation on flowers/buds and produced no seeds. Notably, two parasitic species have retained mutualistic pollination behaviour, suggesting that the parasitism was likely not selected for to reduce the cost of mutualism. We propose that the galling habit evolved as an adaptation to escape parasitism by a specialized braconid wasp. The tough gall produced by one species was almost free of braconid parasitism, and the swollen gall induced by the other species probably prevents attack as a result of the larger airspace inside the gall. Our findings suggest that the presence of a third‐party partner can greatly influence the evolutionary fate of mutualisms, regardless of whether the pairwise interaction continues to favour co‐operation.     

Parasitism,the diversity of life,and paleoparasitology

The parasite-host-environment system is dynamic, with several points of equilibrium. This makes it difficult to trace the thresholds between benefit and damage, and therefore, the definitions of commensalism, mutualism, and symbiosis become worthless. Therefore, the same concept of parasitism may encompass commensalism, mutualism, and symbiosis. Parasitism is essential for life. Life emerged as a consequence of parasitism at the molecular level, and intracellular parasitism created evolutive events that allowed species to diversify. An ecological and evolutive approach to the study of parasitism is presented here. Studies of the origin and evolution of parasitism have new perspectives with the development of molecular paleoparasitology, by which ancient parasite and host genomes can be recovered from disappeared populations. Molecular paleoparasitology points to host-parasite co-evolutive mechanisms of evolution traceable through genome retrospective studies.     

Long‐term coevolution between avian brood parasites and their hosts

Coevolutionary theory predicts that the most common long‐term outcome of the relationships between brood parasites and their hosts should be coevolutionary cycles based on a dynamic change selecting the currently least‐defended host species, given that when well‐defended hosts are abandoned, hosts will be selected to decrease their defences as these are usually assumed to be costly. This is assumed to be the case also in brood parasite‐host systems. Here I examine the frequency of the three potential long‐term outcomes of brood parasite–host coevolution (coevolutionary cycles, lack of rejection, and successful resistance) in 182 host species. The results of simple exploratory comparisons show that coevolutionary cycles are very scarce while the lack of rejection and successful resistance, which are considered evolutionary enigmas, are much more frequent. I discuss these results considering (i) the importance of different host defences at all stages of the breeding cycle, (ii) the role of phenotypic plasticity in long‐term coevolution, and (iii) the evolutionary history of host selection. I suggest that in purely antagonistic coevolutionary interactions, such as those involving brood parasites and their hosts, that although cycles will exist during an intermediate phase of the interactions, the arms race will end with the extinction of the host or with the host acquiring successful resistance. As evolutionary time passes, this resistance will force brood parasites to use previously less suitable host species. Furthermore, I present a model that represents the long‐term trajectories and outcomes of coevolutionary interactions between brood parasites and their hosts with respect to the evolution of egg‐rejection defence. This model suggests that as an increasing number of species acquire successful resistance, other unparasitized host species become more profitable and their parasitism rate and the costs imposed by brood parasitism at the population level will increase, selecting for the evolution of host defences. This means that although acceptance is adaptive when the parasitism rate and the costs of parasitism are very low, this cannot be considered to represent an evolutionary equilibrium, as conventional theory has done to date, because it is not stable.     

Exploitative competition and coexistence in a parasitoid assemblage

Most insect populations are exploited by a complex of different parasitoid species, providing ample opportunities for competitive interactions among the latter. Despite this, resource-mediated competition (i.e., exploitative competition) among insect parasitoids remains poorly documented in natural systems. Here we propose a novel way to infer the presence of competitive interactions from covariance patterns in parasitism levels, and illustrate the use of this approach on a relatively well-defined and simple host–parasitoid system. The parasitism levels caused by three parasitoid species on a shared host showed a highly consistent negative covariance among samples. With the levels of parasitism by one species increasing, the levels of parasitism attributable to the two others decreased. Importantly, negative covariance between parasitism levels by different species appeared at high abundance, but not at low abundance of the phenologically earlier parasitoid species. This as well as several other lines of evidence indicates the importance of competitive interactions in this system. Feeding biology and phenology of the parasitoids suggest that competition in this parasitoid assemblage is primarily resource-mediated rather than occurring through direct interference. The species attacking earlier stages of the host are competitively superior to those attacking their host later in the season. Better dispersal ability and use of alternative host species by the inferior species could contribute to the coexistence of these competing parasitoids.     

Prey temporarily escape from predation in the presence of a second prey species

1. Indirect interactions between populations of different prey species mediated by a shared predator population are known to affect prey dynamics. 2. Depending on the temporal and spatial scale, these indirect interactions may result in positive (apparent mutualism), neutral or negative effects (apparent competition) of the prey on each other's densities. Although there is ample evidence for the latter, evidence for apparent mutualism is scarce. 3. The effectiveness of using one species of predator for biological control of more than one pest species depends on the occurrence of such positive or negative effects. 4. We used an experimental system consisting of the two prey species Western flower thrips (Franklineilla occidentalis Pergande) and greenhouse whitefly (Trialeurodes vaporariorum Westwood) and a shared predator, the phytoseiid mite Amblyseius swirskii Athias‐Henriot. We released all three species on the same plant and studied their dynamics and distribution along rows of plants. 5. We expected that the more mobile prey species (thrips) would escape temporarily in the presence of the other prey species (whitefly) by dispersing from plants with the predator. The predator was expected to disperse slower in the presence of two prey species because of the higher availability of food. 6. Evidence was found for slower dispersal of predators and short‐term escape of thrips from predation when whiteflies were present, thus confirming the occurrence of short‐term apparent mutualism. 7. The apparent mutualism resulted in a cascade to the first trophic level: a higher proportion of fruits was damaged by thrips in the presence of whiteflies. 8. We conclude that apparent mutualism can be an important phenomenon in population dynamics, and can significantly affect biological control of pest species that share a natural enemy.     

Evolution of mutualistic symbiosis: A differential equation model

In geological history, rapid speciation, called adaptive radiation, has occurred repeatedly. The origins of such newly developing taxa often evolved from the symbiosis of different species. Mutualistic symbioses are generally considered to evolve from parasitic relationships. As well as the previous model of host population with discrete generations, a differential equation model of host population with overlapping generations shows that vertical transmission, defined as the direct transfer of infection from a parent host to its progeny, is an important factor which can stimulate reduction of parasite virulence. Evolution of the vertical transmission rate from both points of view, the parasite and the host, is analyzed. There is a critical level of the rate, below which an evolutionary conflict arises (the parasite would want an increase in the rate while the host would not), and above which both species would correspond to increase the rate. Therefore, once the parasite dominates the evolutionary race so as to overcome this critical level, one-way evolution begins toward a highly mutualistic relationship with a high vertical transmission rate, possibly creating a new organism through symbiosis with perfect vertical transmission. Changes in other parameters may decrease the critical level, initiating one-way evolution. However, changes in traits, probably developed through a long interrelationship in parasitism, do not necessarily induce the evolution of mutualism. Establishment of the ability to make use of metabolic and digestive wastes from the partner certainly facilitates the evolution of mutualism, while improvements in reproductive efficiency of parasites and reduction of negative effects from exploitation in hosts on the contrary disturb mutualism.     

Ant association facilitates the evolution of diet breadth in a lycaenid butterfly

The role of mutualistic interactions in adaptive diversification has not been thoroughly examined. Lycaenid butterflies provide excellent systems for exploring mutualistic interactions, as more than half of this family is known to use ants as a resource in interactions that range from parasitism to mutualism. We investigate the hypothesis that protection from predators offered to caterpillars by ants might facilitate host-range evolution. Specifically, experiments with the butterfly Lycaeides melissa investigated the role of ant association in the use of a novel host, alfalfa, Medicago sativa, which is a sub-optimal host for larval development. Survival on alfalfa is increased by the presence of ants, thus supporting the hypothesis that interaction with ants might be important for host-range evolution. Using a demographic model to explore ecological conditions associated with host-range expansion in L. melissa, we conclude that the presence of ants might be an essential component for populations persisting on the novel, sub-optimal host.     

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.     

The phylogeny of a mutualism: evolution and coadaptation between Trollius and its seed-parasitic pollinators

Interactions between seed-parasitic pollinators and their hosts provide useful model systems for the analysis of evolution of mutualism and potential coevolution between plants and insects. Here I present the systematics, pollination ecology and evolution of one of these interactions. I have documented and analysed the phylogenetic and geographic associations between Trollius (Ranunculaceae: 18 spp.) and Chiastocheta (Diptera: Anthomyiidae; 17 spp.), a host-specific genus of seed-parasitic flies that pollinate their host plants to varying extent. Their interactions are usually facultative mutualisms, but in the specialized T. europaeus three fly species are obligate mutualists and a fourth species is an antagonist. The distribution patterns of fly species among Trollius species suggest that the flies evolved in associations with five highly derived Trollius species, and secondarily colonized four more primitive taxa in the parts of their ranges that overlapped with primary hosts. In general, host specificity is maintained primarily through allopatry, with colonization occurring in regions of overlap between parapatric taxa. Fly speciation has occurred in allopatry, both within and among host taxa. Cospeciation is not evident, but convergent evolution in Trollius flowers of several traits, viz. orange sepals, elongated staminodia and increased carpel number per flower, may be the result of mutualism with Chiastocheta.     

An interaction between a specialized seed predator moth and its dioecious host plant shifting from parasitism to mutualism

Seed predator/pollinator and host plant interactions, which may be considered as antagonistic, have the potential to provide good model systems for the study of the early stages of evolution towards mutualism. I describe a relationship between a seed predator, the geometrid moth Perizoma affinitatum , and the dioecious plant Silene dioica . The moth is an obligate seed predator on its host plant. The searching and ovipositing behaviour of the female moths, number of eggs deposited per flower, the pollinating ability of the moths and the seed consumption by the larvae are described as different parameters and studied in two Finnish coastal populations. A high pollinating ability and limited seed consumption by the predator was found and discussed in relation to fitness models of P. affinitatum and S. dioica . In a mutualistic relationship there must be a balance between the costs and benefits so that the seed production by the moths is larger than the seed consumption by the larvae, given a net seed output larger than zero. The data of the parameters included in a seed production/consumption model give a positive seed output when the proportion of S. dioica flowers pollinated by other non-predating insects is less than 60%. Accordingly, even if P. affinitatum would become the exclusive pollinator it would not endanger the survival of the host plant and both partners would benefit from this interaction. Limited seed consumption, high pollinating ability and host specificity as seen in the P. affinitatum and S. dioica interaction are considered to have been important pre-existing qualities in the evolution of the obligate mutualisms between yucca and yucca moths and fig and fig wasps. In isolated serpentine populations where the gene flow is restricted and co-pollinators are rare the interaction between P. affinitatum and S. dioica has the potential to shift from parasitism to mutualism.     

Ecological correlates of feather mite prevalence in passerines

The relationship between host ecology and feather mite prevalence was analysed in birds. Feather mites are small arthropods (fam. Pterolichoidea and Analgoidea) commonly found on birds, although the nature of their interactions with the host (commensalism, mutualism or parasitism), still remains unclear. Host body mass and migratory behaviour were unrelated to feather mite prevalence. Contrary to expectation, there was no differences in mite prevalence between colonial and solitary-breeding species. However, winter sociality was associated with increased prevalence, suggesting that winter and breeding sociality affected the distribution patterns of feather mites in different ways. Plumage dichromatism was negatively correlated with feather mite prevalence, a result that is opposite to that predicted by the Hamilton and Zuk hypothesis for the evolution of host secondary sexual characteristics in relation to parasitism.     

Interactions between seed predators/pollinators and their host plants: a first step towards mutualism?

The mutualisms between fig trees and their pollinator fig wasps and between yucca plants and yucca moths are spectacular examples of coevolution. The characteristics of these independently evolved mutualisms have resulted from long‐term processes, the first stages of which are unknown. A fundamental question in the study of mutualism is how these interactions evolve. Seed predator/pollinator and host plant interactions, which may initially be considered as mainly antagonistic, have the potential to provide good model systems for the study of the first stages of evolution towards mutualism. We present here theoretical models assessing the consequences of interactions between specialized seed predator insects and their host plants. These models describe the parameters that affect the fitness of an individual female seed predator and her influence on the fitness of the host plant. In an optimal strategy for the seed predator, the number of eggs laid in each flower depends on the interaction between the adult and larva survival. Along with a growing predation pressure on adults and larvae several eggs must be laid in each flower by the female seed predator to enhance her fitness. However, in a situation where the host plant selectively aborts flowers with a high number of eggs the fitness of the seed predator will seriously decrease. If the cost of selective abortion is less than the cost of seed predation the host plant will maintain fitness. In a mutualistic relationship a balance between the cost and the benefit of the parameters in the fitness models of the seed predator and the host plant has to occur so that the net seed output is larger than zero (0). Any unselfish behaviour or quality of the seed predator that would benefit the host plant in such a way that the net seed output increases might be a first stage in an interaction becoming mutualistic. The models presented here will not only provide a platform for empirical studies on interactions that may swing from parasitism to mutualism, but also for seed predator/pollinator and host plant interactions in general.     

Limited gene dispersal and spatial genetic structure as stabilizing factors in an ant‐plant mutualism

Comparative studies of the population genetics of closely associated species are necessary to properly understand the evolution of these relationships because gene flow between populations affects the partners' evolutionary potential at the local scale. As a consequence (at least for antagonistic interactions), asymmetries in the strength of the genetic structures of the partner populations can result in one partner having a co‐evolutionary advantage. Here, we assess the population genetic structure of partners engaged in a species‐specific and obligatory mutualism: the Neotropical ant‐plant, Hirtella physophora, and its ant associate, Allomerus decemarticulatus. Although the ant cannot complete its life cycle elsewhere than on H. physophora and the plant cannot live for long without the protection provided by A. decemarticulatus, these species also have antagonistic interactions: the ants have been shown to benefit from castrating their host plant and the plant is able to retaliate against too virulent ant colonies. We found similar short dispersal distances for both partners, resulting in the local transmission of the association and, thus, inbred populations in which too virulent castrating ants face the risk of local extinction due to the absence of H. physophora offspring. On the other hand, we show that the plant populations probably experienced greater gene flow than did the ant populations, thus enhancing the evolutionary potential of the plants. We conclude that such levels of spatial structure in the partners' populations can increase the stability of the mutualistic relationship. Indeed, the local transmission of the association enables partial alignments of the partners' interests, and population connectivity allows the plant retaliation mechanisms to be locally adapted to the castration behaviour of their symbionts.