Microbial manipulation of receptor crosstalk in innate immunity

In the arms race of host-microbe co-evolution, successful microbial pathogens have evolved ingenious ways to evade host immune responses. In this Review, we focus on 'crosstalk manipulation' - the microbial strategies that instigate, subvert or disrupt the molecular signalling crosstalk between receptors of the innate immune system. This proactive interference undermines host defences and contributes to microbial adaptive fitness and persistent infections. Understanding how pathogens exploit host receptor crosstalk mechanisms and infiltrate the host signalling network is essential for developing interventions to redirect the host response and achieve protective immunity.     

A molecular and genomic reference system for conifer defence against insects

Insect pests are part of natural forest ecosystems contributing to forest rejuvenation but can also cause ecological disturbance and economic losses that are expected to increase with climate change. The white pine or spruce weevil (Pissodes strobi) is a pest of conifer forests in North America. Weevil–host interactions with various spruce (Picea) species have been explored as a genomic and molecular reference system for conifer defence against insects. Interactions occur in two major phases of the insect life cycle. In the exophase, adult weevils are free‐moving and display behaviour of host selection for oviposition that is affected by host traits. In the endophase, insects live within the host where mobility and development from eggs to young adults are affected by a complex system of host defences. Genetic resistance exists in several spruce species and involves synergism of constitutive and induced chemical and physical defences that comprise the conifer defence syndrome. Here, we review conifer defences that disrupt the weevil life cycle and mechanisms by which trees resist weevil attack. We highlight molecular and genomic aspects and a possible role for the weevil microbiome. Knowledge of this conifer defence system is supporting forest health strategies and tree breeding for insect resistance.     

Egg phenotype matching by cuckoos in relation to discrimination by hosts and climatic conditions

Although parasites and their hosts often coexist in a set of environmentally differentiated populations connected by gene flow, few empirical studies have considered a role of environmental variation in shaping correlations between traits of hosts and parasites. Here, we studied for the first time the association between the frequency of adaptive parasitic common cuckoo Cuculus canorus phenotypes in terms of egg matching and level of defences exhibited by its reed warbler Acrocephalus scirpaceus hosts across seven geographically distant populations in Europe. We also explored the influence of spring climatic conditions experienced by cuckoos and hosts on cuckoo-host egg matching. We found that between-population differences in host defences against cuckoos (i.e. rejection rate) covaried with between-population differences in degree of matching. Between-population differences in host egg phenotype were associated with between-population differences in parasitism rate and spring climatic conditions, but not with host level of defences. Between-population differences in cuckoo egg phenotype covaried with between-population differences in host defences and spring climatic conditions. However, differences in host defences still explained differences in mimicry once differences in climatic conditions were controlled, suggesting that selection exerted by host defences must be strong relative to selection imposed by climatic factors on egg phenotypes.     

Entering and breaking: virulence effector proteins of oomycete plant pathogens

Oomycete pathogens of plants and animals are related to marine algae and have evolved mechanisms to avoid or suppress host defences independently of other groups of pathogens, such as bacteria and fungi. They cause many destructive diseases affecting crops, forests and aquaculture. The development of genomic resources has led to a dramatic increase in our knowledge of the effectors used by these pathogens to suppress host defences. In particular, a huge, rapidly diverging superfamily of effectors with 100–600 members per genome has been identified. Proteins in this family use the N-terminal motifs RxLR and dEER to cross the host plasma cell membrane autonomously. Once inside the host cell, the proteins suppress host defence signalling. The importance of this effector family is underlined by the fact that plants have evolved intracellular defence receptors to detect the effectors and trigger a rapid counter-attack. The mechanisms by which the effector enter host cells, and by which they suppress host defences, remain to be elucidated.     

Differential reproductive success favours strong host preference in a highly specialized brood parasite

Obligate avian brood parasites show dramatic variation in the degree to which they are host specialists or host generalists. The screaming cowbird Molothrus rufoaxillaris is one of the most specialized brood parasites, using a single host, the bay-winged cowbird (Agelaioides badius) over most of its range. Coevolutionary theory predicts increasing host specificity the longer the parasite interacts with a particular avian community, as hosts evolve defences that the parasite cannot counteract. According to this view, host specificity can be maintained if screaming cowbirds avoid parasitizing potentially suitable hosts that have developed effective defences against parasitic females or eggs. Specialization may also be favoured, even in the absence of host defences, if the parasite's reproductive success in alternative hosts is lower than that in the main host. We experimentally tested these hypotheses using as alternative hosts two suitable but unparasitized species: house wrens (Troglodytes aedon) and chalk-browed mockingbirds (Mimus saturninus). We assessed host defences against parasitic females and eggs, and reproductive success of the parasite in current and alternative hosts. Alternative hosts did not discriminate against screaming cowbird females or eggs. Egg survival and hatching success were similarly high in current and alternative hosts, but the survival of parasitic chicks was significantly lower in alternative hosts. Our results indicate that screaming cowbirds have the potential to colonize novel hosts, but higher reproductive success in the current host may favour host fidelity.     

A kin selection model for the evolution of virulence.

The costs and benefits of parasite virulence are analysed in an evolutionarily stable strategy (ESS) model. Increased host mortality caused by disease (virulence) reduces a parasite's fitness by damaging its food supply. The fitness costs of high virulence may be offset by the benefits of increased transmission or ability to withstand the host's defences. It has been suggested that multiple infections lead to higher virulence because of competition among parasite strains within a host. A quantitative prediction is given for the ESS virulence rate as a function of the coefficient of relatedness among co-infecting strains. The prediction depends on the quantitative relation between the costs of virulence and the benefits of transmission or avoidance of host defences. The particular mechanisms by which parasites can increase their transmission or avoid host defences also have a key role in the evolution of virulence when there are multiple infections.     

Anthropogenic increase in carbon dioxide modifies plant–insect interactions

Industrialisation has elevated atmospheric levels of CO₂ from original 280 ppm to current levels at 400 ppm, which is estimated to double by 2050. Although high atmospheric CO₂ levels affect insect interactions with host plants, the impact of global change on plant defences in response to insect attack is not completely understood. Recent studies have made advances in elucidating the mechanisms of the effects of high CO₂ levels in plant–insect interactions. New studies have proposed that gene regulation and phytohormones regulate resource allocation from photosynthesis to plant defences against insects. Biochemical and molecular studies demonstrated that both defensive hormones jasmonic acid (JA) and ethylene (ET) participate in modulating chemical defences against herbivores in plants grown under elevated CO₂ atmosphere rather than changes in C:N ratio. High atmospheric CO₂ levels increase vulnerability to insect damage by down‐regulating both inducive and constitutive chemical defences regulated by JA and ET. However, elevated CO₂ levels increase the JA antagonistic hormone salicylic acid that increases other chemical defences. How plants grown under elevated CO₂ environment allocate primary metabolites from photosynthesis to secondary metabolism would help to understand innate defences and prevent future herbivory in field crops. We present evidence demonstrating that changes in chemical defences in plants grown under elevated CO₂ environment are hormonal regulated and reject the C:N hypothesis. In addition, we discuss current knowledge of the mechanisms that regulate plants defences against insects in elevated CO₂ atmospheres.     

Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences

Plants and herbivores are thought to be engaged in a coevolutionary arms race: rising frequencies of plants with anti-herbivore defences exert pressure on herbivores to resist or circumvent these defences and vice versa. Owing to its frequency-dependent character, the arms race hypothesis predicts that herbivores exhibit genetic variation for traits that determine how they deal with the defences of a given host plant phenotype. Here, we show the existence of distinct variation within a single herbivore species, the spider mite Tetranychus urticae, in traits that lead to resistance or susceptibility to jasmonate (JA)-dependent defences of a host plant but also in traits responsible for induction or repression of JA defences. We characterized three distinct lines of T. urticae that differentially induced JA-related defence genes and metabolites while feeding on tomato plants (Solanum lycopersicum). These lines were also differently affected by induced JA defences. The first line, which induced JA-dependent tomato defences, was susceptible to those defences; the second line also induced JA defences but was resistant to them; and the third, although susceptible to JA defences, repressed induction. We hypothesize that such intraspecific variation is common among herbivores living in environments with a diversity of plants that impose diverse selection pressure.     

Bacterial strategies to overcome insect defences

Recent genetic and molecular analyses have revealed how several strategies enable bacteria to persist and overcome insect immune defences. Genetic and genomic tools that can be used with Drosophila melanogaster have enabled the characterization of the pathways that are used by insects to detect bacterial invaders and combat infection. Conservation of bacterial virulence factors and insect immune repertoires indicates that there are common strategies of host invasion and pathogen eradication. Long-term interactions of bacteria with insects might ensure efficient dissemination of pathogens to other hosts, including humans.     

Costs to host defence and the persistence of parasitic cuckoos.

Raising genetically unrelated young is maladaptive, yet brood parasitism is widespread in birds. In several systems, hosts can evolve near-perfect defences against the parasite (discrimination and rejection of unlike eggs), making it difficult to understand how the parasite continues to exist. This study demonstrates costs to host defences (e.g. rejection of one's own eggs) such that once the parasite goes extinct on a particular host species, defence mechanisms are selectively disadvantageous. The consequent loss of host defences, and potential for re-exploitation of the host by the parasite, can explain the continued persistence of avian brood parasites. The results provide one general explanation for coexistence of parasites and their hosts.     

The survival strategies of hookworms

Carefully conducted field studies of human necatoriasis have failed to demonstrate the presence of strong immunity, indicating that hookworms have evolved survival strategies to counteract specific immune responses that undoubtedly occur in the host. David Pritchard focuses on these recent field data and on our current knowledge of the biochemical nature of molecules produced by hookworms which have the potential to neutralize host defences and ensure parasite survival.     

Mutualism versus pathogenesis: the give-and-take in plant–bacteria interactions

Pathogenic bacteria and mutualistic rhizobia are able to invade and establish chronic infections within their host plants. The success of these plant–bacteria interactions requires evasion of the plant innate immunity by either avoiding recognition or by suppressing host defences. The primary plant innate immunity is triggered upon recognition of common microbe-associated molecular patterns. Different studies reveal striking similarities between the molecular bases underlying the perception of rhizobial nodulation factors and microbe-associated molecular patterns from plant pathogens. However, in contrast to general elicitors, nodulation factors can control plant defences when recognized by their cognate legumes. Nevertheless, in response to rhizobial infection, legumes show transient or local defence-like responses suggesting that Rhizobium is perceived as an intruder although the plant immunity is controlled. Whether these responses are involved in limiting the number of infections or whether they are required for the progression of the interaction is not yet clear. Further similarities in both plant–pathogen and Rhizobium –legume associations are factors such as surface polysaccharides, quorum sensing signals and secreted proteins, which play important roles in modulating plant defence responses and determining the outcome of the interactions.     

Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities

Background Plants are hotbeds for parasites such as arthropod herbivores, which acquire nutrients and energy from their hosts in order to grow and reproduce. Hence plants are selected to evolve resistance, which in turn selects for herbivores that can cope with this resistance. To preserve their fitness when attacked by herbivores, plants can employ complex strategies that include reallocation of resources and the production of defensive metabolites and structures. Plant defences can be either prefabricated or be produced only upon attack. Those that are ready-made are referred to as constitutive defences. Some constitutive defences are operational at any time while others require activation. Defences produced only when herbivores are present are referred to as induced defences. These can be established via de novo biosynthesis of defensive substances or via modifications of prefabricated substances and consequently these are active only when needed. Inducibility of defence may serve to save energy and to prevent self-intoxication but also implies that there is a delay in these defences becoming operational. Induced defences can be characterized by alterations in plant morphology and molecular chemistry and are associated with a decrease in herbivore performance. These alterations are set in motion by signals generated by herbivores. Finally, a subset of induced metabolites are released into the air as volatiles and function as a beacon for foraging natural enemies searching for prey, and this is referred to as induced indirect defence.Scope The objective of this review is to evaluate (1) which strategies plants have evolved to cope with herbivores and (2) which traits herbivores have evolved that enable them to counter these defences. The primary focus is on the induction and suppression of plant defences and the review outlines how the palette of traits that determine induction/suppression of, and resistance/susceptibility of herbivores to, plant defences can give rise to exploitative competition and facilitation within ecological communities “inhabiting” a plant.Conclusions Herbivores have evolved diverse strategies, which are not mutually exclusive, to decrease the negative effects of plant defences in order to maximize the conversion of plant material into offspring. Numerous adaptations have been found in herbivores, enabling them to dismantle or bypass defensive barriers, to avoid tissues with relatively high levels of defensive chemicals or to metabolize these chemicals once ingested. In addition, some herbivores interfere with the onset or completion of induced plant defences, resulting in the plant’s resistance being partly or fully suppressed. The ability to suppress induced plant defences appears to occur across plant parasites from different kingdoms, including herbivorous arthropods, and there is remarkable diversity in suppression mechanisms. Suppression may strongly affect the structure of the food web, because the ability to suppress the activation of defences of a communal host may facilitate competitors, whereas the ability of a herbivore to cope with activated plant defences will not. Further characterization of the mechanisms and traits that give rise to suppression of plant defences will enable us to determine their role in shaping direct and indirect interactions in food webs and the extent to which these determine the coexistence and persistence of species.     

Novel fungal disease in complex leaf‐cutting ant societies

Abstract 1. The leaf‐cutting ants practise an advanced system of mycophagy where they grow a fungus as a food source. As a consequence of parasite threats to their crops, they have evolved a system of morphological, behavioural, and chemical defences, particularly against fungal pathogens (mycopathogens). 2. Specific fungal diseases of the leaf‐cutting ants themselves have not been described, possibly because broad spectrum anti‐fungal defences against mycopathogens have reduced their susceptibility to entomopathogens. 3. Using morphological and molecular tools, the present study documents three rare infection events of Acromyrmex and Atta leaf‐cutting ants by Ophiocordyceps fungi, agenus of entomopathogens that is normally highly specific in its host choice. 4. As leaf‐cutting ants have been intensively studied, the absence of prior records of Ophiocordyceps suggests that these infections may be a novel event and that switching from one host to another is possible. To test the likelihood of this hypothesis, host switching was experimentally induced, and successfully achieved, among five distinct genera of ants, one of which was in a different sub‐family than the leaf‐cutter ants. 5. Given the substantial differences among the five host ants, the ability of Ophiocordyceps to shift between such distant hosts is remarkable; the results are discussed in the context of ant ecological immunology and fungal invasion strategies.     

Behavioural ecology of defence in a risky environment: caterpillars versus ants in a Neotropical savanna

1. Predatory ants may reduce infestation by herbivorous insects, and slow‐moving Lepidopteran larvae are often vulnerable on foliage. We investigate whether caterpillars with morphological or behavioural defences have decreased risk of falling prey to ants, and if defence traits mediate host plant use in ant‐rich cerrado savanna. 2. Caterpillars were surveyed in four cerrado localities in southeast Brazil (70–460 km apart). The efficacy of caterpillar defensive traits against predation by two common ant species (Camponotus crassus, C. renggeri) was assessed through experimental trials using caterpillars of different species and captive ant colonies. 3. Although ant presence can reduce caterpillar infestation, the ants' predatory effects depend on caterpillar defence traits. Shelter construction and morphological defences can prevent ant attacks (primary defence), but once exposed or discovered by ants, caterpillars rely on their size and/or behaviour to survive (secondary defence). 4. Defence efficiency depends on ant identity: C. renggeri was more aggressive and lethal to caterpillars than C. crassus. Caterpillars without morphological defences or inside open shelters were found on plants with decreased ant numbers. No unsheltered caterpillar was found on plants with extrafloral nectaries (EFNs). Caterpillars using EFN‐bearing plants lived in closed shelters or presented morphological defences (hairs, spines), and were less frequently attacked by ants during trials. 5. The efficiency of defences against ants is thus crucial for caterpillar survival and determines host plant use by lepidopterans in cerrado. Our study highlights the effect of EFN‐mediated ant‐plant interactions on host plant use by insect herbivores, emphasizing the importance of a tritrophic viewpoint in risky environments.     

Symbiont infection affects aphid defensive behaviours

Aphids harbour both an obligate bacterial symbiont, Buchnera aphidicola, and a wide range of facultative ones. Facultative symbionts can modify morphological, developmental and physiological host traits that favour their spread within aphid populations. We experimentally investigated the idea that symbionts may also modify aphid behavioural traits to enhance their transmission. Aphids exhibit many behavioural defences against enemies. Despite their benefits, these behaviours have some associated costs leading to reduction in aphid reproduction. Some aphid individuals harbour a facultative symbiont Hamiltonella defensa that provides protection against parasitoids. By analysing aphid behaviours in the presence of parasitoids, we showed that aphids infected with H. defensa exhibited reduced aggressiveness and escape reactions compared with uninfected aphids. The aphid and the symbiont have both benefited from these behavioural changes: both partners reduced the fitness decrements associated with the behavioural defences. Such symbiont-induced changes of behavioural defences may have consequences for coevolutionary processes between host organisms and their enemies.     

Adaptive value of host discrimination in parasitoids: when host defences are very costly

Host acceptance decision in parasitic wasps strongly depends on the parasitism status of the encountered host. In solitary species, a host only allows the development of a single parasitic larva and then, any oviposition in an already parasitised host leads to larval competition and loss of offspring. Females of many parasitoid species are able to discriminate between parasitised hosts and healthy ones. However, the host discrimination process may require more time than oviposition, exposing the wasp to high risks when the host has efficient defences. Consequently, depending on the degree of success of the host defence, the cost of host inspection for discrimination can outweigh the benefit of superparasitism avoidance. In the present paper, a theoretical approach was developed for determining how host defences may affect optimal host acceptance behaviour in parasitoids. The present model compares the lifetime reproductive success over the strategy used, discrimination and no-discrimination: a discriminating wasp sets a relatively greater value in its current oviposition, while a non-discriminating female sets a greater value in its own survival and future reproduction. The model predicts that depending on physiological state variables and environmental state variables, the optimal policy is not discriminating. Our results suggest that the low discriminating ability observed in some parasitic wasps could probably be an evolutionary response to host defences pressure.