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Ant-plant interactions represent a diversity of strategies, from exploitative to mutualistic, and how these strategies evolve is poorly understood. Here, we link physiological, ecological, and phylogenetic approaches to study the evolution and coexistence of strategies in the Acacia-Pseudomyrmex system. Host plant species represented 2 different strategies. High-reward hosts produced significantly more extrafloral nectar (EFN), food bodies, and nesting space than low-reward hosts, even when being inhabited by the same species of ant mutualist. High-reward hosts were more effectively defended against herbivores and exploited to a lower extent by nondefending ants than low-reward hosts. At the phenotypic level, secretion of EFN and ant activity were positively correlated and a mutualistic ant species induced nectar secretion, whereas a nondefending exploiter did not. All of these mechanisms contribute to the stable association of high-reward hosts with defending ant species. However, exploiter ants are less dependent on the host-derived rewards and can colonize considerable proportions of the low-reward hosts. Mapping these strategies onto phylogenetic trees demonstrated that the low-reward hosts represent the derived clade within a monophyletic group of obligate ant plants and that the observed exploiter ant species evolved their strategy without having a mutualistic ancestor. We conclude that both types of host strategies coexist because of variable net outcomes of different investment-payoff regimes and that the effects of exploiters on the outcome of mutualisms can, thus, increase the diversity within the taxa involved.

1. Multiple plant species are engaged in defensive mutualisms with members of the third trophic level. However, mutualisms are prone to exploitation by low-quality symbionts that do not provide the adequate service to their host. Can mutualisms proceed only when hosts identify their symbionts in advance or continuously monitor their activity, or are there other mechanisms to avoid the invasion of mutualisms by exploiters? 2. High-reward species amongst Mesoamerican Acacia myrmecophytes are dominantly colonized by defending mutualistic ants, whereas about 50% of the low-reward hosts are inhabited by non-defending exploiters. I followed the development of recently founded ant colonies on a high-reward and a low-reward Acacia host species over 7 months, to investigate whether reward production correlates with a preferred maintenance of defending ants on the respective hosts. 3. Ant diversity decreased sooner on high-reward than on low-reward hosts, and mutualistic ants were more likely to finally dominate the high-reward hosts. I observed an increased frequency of mutualists replacing parasites at high initial rates of reward production. Apparently, higher nectar provisioning by the host plants shifted the competitive balance between mutualistic and parasitic ants. Independently of the causal reason for the different secretion rates, producing more nectar thereby favours the maintenance of defending mutualists on high-reward hosts. 4. Synthesis. The aggressiveness that enables ants to outcompete other ants also underlies their defensive effect against herbivores. I conclude that hosts can preferably associate with high-quality mutualists without measuring their effectiveness. Mutualisms remain stable when partner screening is based on traits that are relevant for the mutualistic interaction, with no need for the host to have information on the quality or identity of the symbiont.

Social organisation of colonies of obligate plant-ants can affect their interaction with myrmecophyte hosts and with other ants competing for the resources they offer. An important parameter of social organisation is whether nest sites of a colony include one or several host individuals. We determined colony boundaries in a plant-ant associated with the rainforest understorey tree Leonardoxa africana subsp. africana, found in coastal forests of Cameroon (Central Africa). This myrmecophyte is strictly associated with two ants, Petalomyrmex phylax and Cataulacus mckeyi. Plants provide food and nesting sites for P. phylax, which protects young leaves against insect herbivores. This mutualism is often parasitised by C. mckeyi, which uses but does not protect the host. The presence of C. mckeyi on a tree excludes the mutualistic ant. Because Petalomyrmex -occupied trees are better protected, their growth and survival are superior to those of Cataulacus -occupied trees, giving P. phylax an advantage in occupation of nest sites. C. mckeyi often colonises trees that have lost their initial associate P. phylax, as a result of injury to the tree caused by disturbance. Polydomy may allow C. mckeyi to occupy small clumps of trees, without the necessity of claustral colony foundation in each tree. Investigating both the proximate (behavioural repertoire, colony odour) and the ultimate factors (genetic structure) that may influence colony closure, we precisely defined colony boundaries. We show that colonies of C. mckeyi are monogynous and facultatively polydomous, i.e. a colony occupies one to several Leonardoxa trees. Workers do not produce males. Thus, the hypothesis that polydomy allows workers in queenless nests to evade queen control for their reproduction is not supported in this instance. This particular colony structure may confer on C. mckeyi an advantage in short-distance dispersal, and this could help explain its persistence within the dynamic Leonardoxa system.

Obligate ant-defended plants provide food and shelter in exchange for protection against herbivores. Mesoamerican acacia trees have an obligate ant mutualism, but parasitic non-defending ants can also nest on the tree. We assessed whether rewards corresponded to ant defense within a plant species. As we expected, we found that parasite-inhabited trees had fewer swollen spines than ant-defended trees. Spine diameter was smaller in parasite-inhabited plants, but there were no differences in spine length, suggesting that spines serve as mechanical protection against herbivory. Parasite-inhabited plants may have reduced rewards because of plant differences when establishing, a plastic response to limited resources, or differential energy allocation when sensing the lack of defense.

Virtually all plants and animals, including humans, are home to symbiotic microorganisms. Symbiotic interactions can be neutral, harmful or have beneficial effects on the host organism. However, growing evidence suggests that microbial symbionts can evolve rapidly, resulting in drastic transitions along the parasite–mutualist continuum. In this Review, we integrate theoretical and empirical findings to discuss the mechanisms underpinning these evolutionary shifts, as well as the ecological drivers and why some host–microorganism interactions may be stuck at the end of the continuum. In addition to having biomedical consequences, understanding the dynamic life of microorganisms reveals how symbioses can shape an organism’s biology and the entire community, particularly in a changing world.Symbiotic interactions can be neutral, harmful or have beneficial effects for host organisms. In this Review, Drew, Stevens and King discuss the evolutionary transitions of host–microorganism symbioses along the parasite–mutualist continuum, the mechanisms underlying evolutionary changes, the selective pressures involved and common empirical approaches for studying them.

Symbiotic microbes have become increasingly recognized to mediate interactions between natural enemies and their hosts. The ecologies of these symbioses, however, are poorly understood in many systems, and a predictive framework is needed to guide future studies. To achieve this, we focus on heritable, defensive microbes of insects. Our review of laboratory‐based studies identifies diverse bacterial species that have independently evolved to protect a range of insects against parasitoids, parasites, predators and pathogens. Although defensive mechanisms are typically unknown, some involve toxins or the upregulation of host immunity. Despite substantial benefits of infection in the presence of natural enemies, the protective symbionts of insects are often found at intermediate levels in natural populations. Using a host‐centred population genetics approach made possible by the host restriction and cytoplasmic inheritance of these microbes, we propose that balancing selection plays a major role in symbiont maintenance, with protective benefits in the presence of enemies and infection costs in their absence. Other mediating factors are likely to be important, including temperature, superinfections and transmission dynamics. While few studies have provided evidence for defence in the field, several studies have shown symbiont infection frequencies to be dynamic, varying across temporal and spatial gradients and food–plant associations. Newly presented data from our pea aphid research reveal that temporal shifts in defensive symbiont prevalence can be quite rapid, with Hamiltonella defensa showing 10–20% shifts around a seasonal average of c. 50%. Such findings contrast with more unidirectional changes seen in laboratory population cages, suggesting temporal changes in the costs and benefits of symbionts in the field. To frame future research on defensive symbiont ecology, we briefly consider a range of studies needed to test laboratory‐ and field‐derived predictions on defensive symbiosis. Included are investigations of defensive mechanisms, symbiont‐driven co‐evolution and community‐level effects. We also consider the need for more thorough and highly resolved molecular diagnostics of natural infections, laboratory studies on functional differences between symbiont strains and species and studies on the relative costs and benefits of defenders in nature. The emerging theme of symbiont‐mediated defence across eukaryotes suggests that knowledge of the functional mechanisms behind protection and natural symbiont dynamics could be key to understanding many of the world's antagonistic species interactions. Thus, the development of insects as a model for such studies holds promise for these organisms and beyond.

Understanding the factors that modify infection probability and virulence is crucial for identifying the drivers of infection outbreaks and modeling disease epidemic progression, and increases our ability to control diseases and reduce the harm they cause. One factor that can strongly influence infection probability and virulence is the presence of other pathogens. However, while coexposures and coinfections are incredibly common, we still have only a limited understanding of how pathogen interactions alter infection outcomes or whether their impacts are scale dependent. We used a system of one host and two pathogens to show that sequential coinfection can have a tremendous impact on the host and the infecting pathogens and that the outcome of (co-)infection can be negative or positive depending on the focal organization level.

Symbiont community assembly is driven by host–symbiont and symbiont–symbiont interactions. The effects that symbionts exert on their hosts are often context‐dependent, and existing theoretical frameworks of symbiont community assembly do not consider the implications of variable outcomes to assembly processes. We hypothesized that symbiont–symbiont interactions become increasingly important along a parasitism/mutualism continuum because; (i) negative outcomes favour host resistance which in turn reduces symbiont colonization and subsequently reduce symbiont–symbiont interactions, whereas (ii) positive host outcomes favour tolerance and consequently higher symbiont colonization rates, leading to stronger interactions among symbionts. We found support for this hypothesis in the cleaning symbiosis between crayfish and ectosymbiotic branchiobdellidan worms. The symbiosis between crayfish and their worms can shift from parasitism/commensalism to mutualism as crayfish age. Here, field surveys identified changes in worm density, diversity and composition that were concomitant to changing symbiosis outcomes. We conducted several laboratory experiments and behavioural assays to relate patterns from the field to their likely causal processes. Young crayfish typically hosted only two relatively small worm species. Older crayfish hosted two additional larger species. In laboratory experiments, young crayfish exhibited a directed grooming response to all worm species, but were unable to remove small species. Conversely, adult crayfish did not exhibit grooming responses to any worm species. Relaxed grooming allowed the colonization of large worm species and initiated symbiont–symbiont intraguild predation that reduced the abundance and altered the behaviour of small worm species. Thus, the dominant processes of symbiont community assembly shifted from host resistance to symbiont–symbiont interactions through host ontogeny and a concomitant transition towards mutualism. This work shows that host resistance can have a prevailing influence over symbiont community assembly when symbiosis is disadvantageous to the host. However, when symbiosis is advantageous and resistance is relaxed, symbiont colonization rate and consequently abundance and diversity increases and interactions among symbionts become increasingly important to symbiont community assembly.

Vertical and horizontal transmission are terms that describe the transfer of symbionts from parents to offspring and among unrelated hosts, respectively. Many symbionts, including parasites, pathogens, mutualists, and microbiota, use a combination of both strategies, known as mixed-mode transmission (MMT). Here I review what is known about the evolution, ecology, and epidemiology of symbionts with MMT and compare MMT with our expectations for single-mode strategies. Symbionts with MMT are common and, in comparison with single-mode symbionts, show many surprising features. MMT combines the best of two worlds with regard to the ecological conditions required for persistence and plays a role in the evolution of virulence and genome architecture. Even rare transmission by the minority type of these two transmission modes can make a big difference for the system. This review explores the conceptual issues surrounding the dynamics of mixedmode symbionts by reviewing literature from the entire range of host and symbiont taxa.

Most species have one or more natural enemies, e.g., predators, parasites, pathogens, and herbivores, among others. These species in turn typically attack multiple victim species. This leads to the possibility of indirect interactions among those victims, both positive and negative. The term apparent competition commonly denotes negative indirect interactions between victim species that arise because they share a natural enemy. This indirect interaction, which in principle can be reflected in many facets of the distribution and abundance of individual species and more broadly govern the structure of ecological communities in time and space, pervades many natural ecosystems. It also is a central theme in many applied ecological problems, including the control of agricultural pests, harvesting, the conservation of endangered species, and the dynamics of emerging diseases. At one end of the scale of life, apparent competition characterizes intriguing aspects of dynamics within individual organisms-for example, the immune system is akin in many ways to a predator that can induce negative indirect interactions among different pathogens. At intermediate scales of biological organization, the existence and strength of apparent competition depend upon many contingent details of individual behavior and life history, as well as the community and spatial context within which indirect interactions play out. At the broadest scale of macroecology and macroevolution, apparent competition may play a major, if poorly understood, role in the evolution of species' geographical ranges and adaptive radiations.