Antagonisms, mutualisms and commensalisms affect outbreak dynamics of the southern pine beetle

Feedback from community interactions involving mutualisms are a rarely explored mechanism for generating complex population dynamics. We examined the effects of two linked mutualisms on the population dynamics of a beetle that exhibits outbreak dynamics. One mutualism involves an obligate association between the bark beetle, Dendroctonus frontalis and two mycangial fungi. The second mutualism involves Tarsonemus mites that are phoretic on D. frontalis (“commensal”), and a blue-staining fungus, Ophiostoma minus. The presence of O. minus reduces beetle larval survival (“antagonistic”) by outcompeting beetle-mutualistic fungi within trees yet supports mite populations by acting as a nutritional mutualist. These linked interactions potentially create an interaction system with the form of an endogenous negative feedback loop. We address four hypotheses: (1) Direct negative feedback: Beetles directly increase the abundance of O. minus, which reduces per capita reproduction of beetles. (2) Indirect negative feedback: Beetles indirectly increase mite abundance, which increases O. minus, which decreases beetle reproduction. (3) The effect of O. minus on beetles depends on mites, but mite abundance is independent of beetle abundance. (4) The effect of O. minus on beetles is independent of beetle and mite abundance. High Tarsonemus and O. minus abundances were strongly correlated with the decline and eventual local extinction of beetle populations. Manipulation experiments revealed strong negative effects of O. minus on beetles, but falsified the hypothesis that horizontal transmission of O. minus generates negative feedback. Surveys of beetle populations revealed that reproductive rates of Tarsonemus, O. minus, and beetles covaried in a manner consistent with strong indirect interactions between organisms. Co-occurrence of mutualisms embedded within a community may have stabilizing effects if both mutualisms limit each other. However, delays and/or non-linearities in the interaction systems may result in large population fluctuations. Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

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.     

Ecological theory of mutualism: Robust patterns of stability and thresholds in two‐species population models

Mutualisms are ubiquitous in nature, provide important ecosystem services, and involve many species of interest for conservation. Theoretical progress on the population dynamics of mutualistic interactions, however, comparatively lagged behind that of trophic and competitive interactions, leading to the impression that ecologists still lack a generalized framework to investigate the population dynamics of mutualisms. Yet, over the last 90 years, abundant theoretical work has accumulated, ranging from abstract to detailed. Here, we review and synthesize historical models of two‐species mutualisms. We find that population dynamics of mutualisms are qualitatively robust across derivations, including levels of detail, types of benefit, and inspiring systems. Specifically, mutualisms tend to exhibit stable coexistence at high density and destabilizing thresholds at low density. These dynamics emerge when benefits of mutualism saturate, whether due to intrinsic or extrinsic density dependence in intraspecific processes, interspecific processes, or both. We distinguish between thresholds resulting from Allee effects, low partner density, and high partner density, and their mathematical and conceptual causes. Our synthesis suggests that there exists a robust population dynamic theory of mutualism that can make general predictions.     

Gene flow and geographically structured coevolution

Many of the dynamic properties of coevolution may occur at the level of interacting populations, with local adaptation acting as a force of diversification, as migration between populations homogenizes these isolated interactions. This interplay between local adaptation and migration may be particularly important in structuring interactions that vary from mutualism to antagonism across the range of an interacting set of species, such as those between some plants and their insect herbivores, mammals and trypanosome parasites, and bacteria and plasmids that confer antibiotic resistance. Here we present a simple geographically structured genetic model of a coevolutionary interaction that varies between mutualism and antagonism among communities linked by migration. Inclusion of geographic structure with gene flow alters the outcomes of local interactions and allows the maintenance of allelic polymorphism across all communities under a range of selection intensities and rates of migration. Furthermore, inclusion of geographic structure with gene flow allows fixed mutualisms to be evolutionarily stable within both communities, even when selection on the interaction is antagonistic within one community. Moreover, the model demonstrates that the inclusion of geographic structure with gene flow may lead to considerable local maladaptation and trait mismatching as predicted by the geographic mosaic theory of coevolution.     

Parasites of mutualisms

Cooperation invites cheating, and nowhere is this more apparent than when different species cooperate, known as mutualism. In almost all mutualisms studied, specialist parasites have been identified that purloin the benefits that one mutualist provides another. Explaining how parasites are kept from driving mutualisms extinct remains an unsolved problem because existing theories explaining the maintenance of cooperation do not apply to parasites of mutualisms. Nonetheless, these theories can be summarized in such a way as to suggest how mutualisms can persist in the face of parasites. (1) For cooperation to occur, the recipient of a benefit must reciprocate, and the recriprocated benefit must be captured by the initial giver or its offspring. (2) For cooperation to persist, the mutualism must be re-assembled each generation. Because most mutualisms are of the "by-product' type, broadly defined, the first condition is normally always fulfilled. Thus, the maintenance of mutualism usually requires enforcement of the second condition: reliable re-assembly. Hence, I argue that the persistence of mutualism is best understood by using theories of species coexistence, because each mutualist can be considered a resource for the other, and species coexistence theory explains how multiple taxa (e.g. parasites and mutualists) can stably partition a resource over multiple generations. This approach connects the study of mutualism to theories of population regulation and helps to identify key factors that have promoted the evolution, maintenance and breakdown of mutualism. I discuss how these ideas might apply to and be tested in ant-plant, fig-wasp and yucca-moth mutualisms.     

Allee dynamics generated by protection mutualisms can drive oscillations in trophic cascades

Understanding the relative effect of top predators and primary producers on intermediate trophic levels is a key question in ecology. Most previous work, however, has not considered either realistic nonlinearities in feedback between trophic levels or the effect of mutualists on trophic cascades. Here, we develop a realistic model for a protection mutualism that explicitly includes interactions between a protected herbivore and both its food plant and generalist predators. In the absence of protection, herbivores and plant resources approach a stable equilibrium, provided that predation is not so high as to cause herbivore extinction. In contrast, adding protection by mutualists increases the range of dynamical outcomes to include unstable equilibria, stable and unstable limit cycles, and heteroclinic orbits. By reducing the impact of predators, protection by mutualists can allow herbivores to exert strong negative effects on their host plants, which in turn can lead to repeated cycles of overexploitation and recovery. Our results indicate that it may be essential to consider protection mutualisms to understand the dynamics of trophic cascades. Conversely, it may be essential to explicitly include dynamical feedback between plants and herbivores to fully understand the population and community dynamical consequences of protection mutualism.     

A general model for the evolution of mutualisms

The evolution of mutualisms presents a puzzle. Why does selection favour cooperation among species rather than cheaters that accept benefits but provide nothing in return? Here we present a general model that predicts three key factors will be important in mutualism evolution: (i) high benefit to cost ratio, (ii) high within‐species relatedness and (iii) high between‐species fidelity. These factors operate by moderating three types of feedback benefit from mutualism: cooperator association, partner‐fidelity feedback and partner choice. In defining the relationship between these processes, our model also allows an assessment of their relative importance. Importantly, the model suggests that phenotypic feedbacks (partner‐fidelity feedback, partner choice) are a more important explanation for between‐species cooperation than the development of genetic correlations among species (cooperator association). We explain the relationship of our model to existing theories and discuss the empirical evidence for our predictions.     

The Benefits of Mutualism: A Conceptual Framework

There are three general mechanisms by which phenotypic benefits are transferred between unrelated organisms. First, one organism may purloin benefits from another by preying on or parasitizing the other organism. Second, one organism may enjoy benefits that are incidental to or a by-product of the self-serving traits of another organism. Third, an organism may invest in another organism if that investment produces return benefits which outweigh the cost of the investment. Interactions in which both parties gain a net benefit are mutualistic. The three mechanisms by which benefits are transferred between organisms can be combined in pairs to produce six possible kinds of original or 'basal' mutualisms that can arise from an amutualistic state. A review of the literature suggests that most or all interspecific mutualism have origins in three of the six possible kinds of basal mutualism. Each of these three basal mutualisms have byproduct benefits flowing in at least one direction. The transfer of by-product benefits and investment are common to both intra- and interspecific mutualisms, so that some interspecific mutualisms have intraspecific analogs. A basal mutualism may evolve to the point where each party invests in the other, sometimes obscuring the nature of the original interaction along the way. Two prominent models for the evolution of mutualism do not include by-product benefits: Roughgarden's model for the evolution of the damsel-fish anemone mutualism and the 'Tit-for-Tat' model of reciprocity. Using the conceptual framework presented here, including in particular by-product benefits, I have shown how it is possible to construct more parsimonious alternatives to both models.     

The Stability and Persistence of Mutualisms Embedded in Community Interactions

In this paper we argue that two-species models of mutualism may be oversimplifications of the real world that lead to erroneous predictions. We present a four-species model of a pollination mutualism embedded in other types of community interactions. Conclusions derived from two-species models about the destabilizing effect of mutualisms are misleading when applied to the present scenario; although the mutualisms are locally destabilizing, the effect is more than canceled by an increased chance of feasibility. The crucial difference is the interaction of the mutualists with other species in a larger web. Furthermore, community persistence (without unrealistic population explosion), arguably a superior ecological criterion, is greatly enhanced by the presence of mutualisms. Therefore, we predict that mutualisms should be common in the real world, a prediction matching empirial findings and in contrast to the predictions from local stability analysis of basic two-species models. This method of stabilizing a mutualism appears superior in some ways to the often-used method of introducing density dependence in the strength of the mutualism, because it permits obligate mutualisms to exist even at low densities, again matching empirical findings. Lastly, this study is an example of how complex model assemblages can behave qualitatively differently from analogous simpler ones.     

Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism

Mutualisms, beneficial interactions between species, are expected to be unstable because delivery of benefit likely involves fitness costs and selection should favour partners that deliver less benefit. Yet, mutualisms are common and persistent, even in the largely promiscuous associations between plants and soil microorganisms such as arbuscular mycorrhizal fungi. In two different systems, we demonstrate preferential allocation of photosynthate by host plants to the more beneficial of two AM fungal symbionts. This preferential allocation could allow the persistence of the mutualism if it confers sufficient advantage to the beneficial symbiont that it overcomes the cost of mutualism. We find that the beneficial fungus does increase in biomass when the fungi are spatially separated within the root system. However, in well-mixed fungal communities, non-beneficial fungi proliferate as expected from their reduced cost of mutualism. Our findings suggest that preferential allocation within spatially structured microbial communities can stabilize mutualisms between plants and root symbionts.     

Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit

A basic tenet of ecology is that negative feedback on abundance plays an important part in the coexistence of species within guilds. Mutualistic interactions generate positive feedbacks on abundance and therefore are not thought to contribute to the maintenance of diversity. Here, I report evidence of negative feedback on plant growth through changes in the composition of their mutualistic fungal symbionts, arbuscular mycorrhizal (AM) fungi. Negative feedback results from asymmetries in the delivery of benefit between plant and AM fungal species in which the AM fungus that grows best with the plant Plantago lanceolata is a poor growth promoter for Plantago. Growth of Plantago is, instead, best promoted by the AM fungal species that accumulate with a second plant species, Panicum sphaerocarpon. The resulting community dynamic leads to a decline in mutualistic benefit received by Plantago, and can contribute to the coexistence of these two competing plant species.     

Potential impacts of multiple partners on mycorrhizal community dynamics

The significance of arbuscular mycorrhizal (AM) fungi in terrestrial ecosystems is widely acknowledged, but the causes and consequences of diversity in these fungi are not well understood. A recent frequency-dependent model suggests that dynamics within mycorrhizal mutualisms could promote the coexistence of at least two competing plant species and two competing fungal species within a community. Models are developed here in which simultaneous association with multiple partners may result in elevated or depressed fitness relative to association with either partner alone. This increases the range of conditions under which negative feedback occurs and coexistence of all four species is possible. Differences between plants in the relative proportions of fungi at which maximum fitness occurs may facilitate coexistence, as may differences between fungi in their abilities to establish interplant connections. These models suggest additional mechanisms by which mutualistic interactions could promote local diversity of plants and AM fungi.     

Limiting cheaters in mutualism: evidence from hybridization between mutualist and cheater yucca moths

Mutualisms are balanced antagonistic interactions where both species gain a net benefit. Because mutualisms generate resources, they can be exploited by individuals that reap the benefits of the interaction without paying any cost. The presence of such 'cheaters' may have important consequences, yet we are only beginning to understand how cheaters evolve from mutualists and how their evolution may be curtailed within mutualistic lineages. The yucca-yucca moth pollination mutualism is an excellent model in this context as there have been two origins of cheating from within the yucca moth lineage. We used nuclear and mitochondrial DNA markers to examine genetic structure in a moth population where a cheater species is parapatric with a resident pollinator. The results revealed extensive hybridization between pollinators and cheaters. Hybrids were genetically intermediate to parental populations, even though all individuals in this population had a pollinator phenotype. The results suggest that mutualisms can be stable in the face of introgression of cheater genes and that the ability of cheaters to invade a given mutualism may be more limited than previously appreciated.     

Mutualisms in a changing world: an evolutionary perspective

Ecology Letters (2010) 13: 1459-1474 ABSTRACT: There is growing concern that rapid environmental degradation threatens mutualistic interactions. Because mutualisms can bind species to a common fate, mutualism breakdown has the potential to expand and accelerate effects of global change on biodiversity loss and ecosystem disruption. The current focus on the ecological dynamics of mutualism under global change has skirted fundamental evolutionary issues. Here, we develop an evolutionary perspective on mutualism breakdown to complement the ecological perspective, by focusing on three processes: (1) shifts from mutualism to antagonism, (2) switches to novel partners and (3) mutualism abandonment. We then identify the evolutionary factors that may make particular classes of mutualisms especially susceptible or resistant to breakdown and discuss how communities harbouring mutualisms may be affected by these evolutionary responses. We propose a template for evolutionary research on mutualism resilience and identify conservation approaches that may help conserve targeted mutualisms in the face of environmental change.     

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.     

Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus‐tending ants

Interspecific facultative mutualisms typically involve guilds of interacting species, and species within a guild can vary in the quality of services they provide. For plants that secrete extrafloral nectar (EFN), visitation by multiple ant species that vary in anti–herbivore abilities may result in reduced benefits, relative to an exclusive association with a high-quality mutualist. This raises the intriguing problem of how facultative ant-plant mutualisms persist, given that EFN is costly to produce, yet may confer diminishing returns as partner diversity increases. I tested the prediction that association with two ant partners ( Crematogaster opuntiae and Liometopum apiculatum ) weakens benefits to the EFN-producing tree cholla cactus ( Opuntia imbricata ). I found that only one ant ( L. apiculatum ) provided protection against herbivores and seed predators. However, this species associated with cacti more frequently than Crematogaster across multiple temporal scales. Within years, Liometopum showed greater constancy on plants they occupied, more frequently colonized vacant plants, and replaced but were never replaced by Crematogaster . Across years of plant development, Liometopum was more abundant on reproductive plants and showed greater overlap with cactus enemies. Simulations of cactus lifetime reproductive output indicated that associating with high- and low-quality mutualists did not significantly reduce plant benefits relative to an exclusive L. apiculatum – O. imbricata association. The results suggest that non-random interaction frequencies, possibly driven by competition, may contribute to the maintenance of facultative mutualisms involving multiple, qualitatively different partners.     

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.     

Host-specificity and coevolution among pollinating and nonpollinating New World fig wasps

Figs (Ficus spp., Moraceae) and their pollinating wasps (Hymenoptera, Agaonidae, Chalcidoidea) constitute a classic example of an obligate plant-pollinator mutualism, and have become an ideal system for addressing questions on coevolution, speciation, and the maintenance of mutualisms. In addition to pollinating wasps, figs host several types of nonpollinating, parasitic wasps from a diverse array of Chalcid subfamilies with varied natural histories and ecological strategies (e.g. competitors, gallers, and parasitoids). Although a few recent studies have addressed the question of codivergence between specific genera of pollinating and nonpollinating fig wasps, no study has addressed the history of divergence of a fig wasp community comprised of multiple genera of wasps associated with a large number of sympatric fig hosts. Here, we conduct phylogenetic analyses of mitochondrial DNA sequences (COI) using 411 individuals from 69 pollinating and nonpollinating fig wasp species to assess relationships within and between five genera of fig wasps (Pegoscapus, Idarnes, Heterandrium, Aepocerus, Physothorax) associated with 17 species of New World Urostigma figs from section Americana. We show that host-switching and multiple wasp species per host are ubiquitous across Neotropical nonpollinating wasp genera. In spite of these findings, cophylogenetic analyses (TREEMAP 1.0, TREEMAP 2.02beta, and parafit) reveal evidence of codivergence among fig wasps from different ecological guilds. Our findings further challenge the classical notion of strict-sense coevolution between figs and their associated wasps, and mirror conclusions from detailed molecular studies of other mutualisms that have revealed common patterns of diffuse coevolution and asymmetric specialization among the participants.     

Ants farm subterranean aphids mostly in single clone groups - an example of prudent husbandry for carbohydrates and proteins?

ABSTRACT: BACKGROUND: Mutualistic interactions are wide-spread but the mechanisms underlying their evolutionary stability and ecological dynamics remain poorly understood. Cultivation mutualisms in which hosts consume symbionts occur in phylogenetically diverse groups, but often have symbiont monocultures for each host. This is consistent with the prediction that symbionts should avoid coexistence with other strains so that host services continue to benefit relatives, but it is less clear whether hosts should always favor monocultures and what mechanisms they might have to manipulate symbiont diversity. Few mutualisms have been studied in sufficient genetic detail to address these issues, so we decided to characterize symbiont diversity in the complex mutualism between multiple root aphid species and Lasius flavus ants. After showing elsewhere that three of these aphid species have low dispersal and mostly if not exclusively asexual reproduction, we here investigate aphid diversity within and between ant nest mounds. RESULTS: The three focal species (Geoica utricularia, Forda marginata and Tetraneura ulmi) had considerable clonal diversity at the population level. Yet more than half of the ant mounds contained just a single aphid species, a significantly higher percentage than expected from a random distribution. Over 60% of these single-species mounds had a single aphid clone, and clones tended to persist across subsequent years. Whenever multiple species/clones cooccurred in the same mound, they were spatially separated with more than 95% of the aphid chambers containing individuals of a single clone. CONCLUSIONS: L. flavus "husbandry" is characterized by low aphid "livestock" diversity per colony, especially at the nest-chamber level, but it lacks the exclusive monocultures known from other cultivation mutualisms. The ants appear to eat most of the early instar aphids, so that adult aphids are unlikely to face limited phloem resources and scramble competition with other aphids. We suggest that such culling of carbohydrate-providing symbionts for protein ingestion may maintain maximal host yield per aphid while also benefitting the domesticated aphids as long as their clone-mates reproduce successfully. The cost-benefit logic of this type of polyculture husbandry has striking analogies with human farming practices based on slaughtering young animals for meat to maximize milk-production by a carefully regulated adult livestock population.     

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.