Rapid induction of immune density-dependent prophylaxis in adult social insects

The innate immune system provides defence against parasites and pathogens. This defence comes at a cost, suggesting that immune function should exhibit plasticity in response to variation in environmental threats. Density-dependent prophylaxis (DDP) has been demonstrated mostly in phase-polyphenic insects, where larval group size determines levels of immune function in either adults or later larval instars. Social insects exhibit extreme sociality, but DDP has been suggested to be absent from these ecologically dominant taxa. Here we show that adult bumble-bee workers (Bombus terrestris) exhibit rapid plasticity in their immune function in response to social context. These results suggest that DDP does not depend upon larval conditions, and is likely to be a widespread and labile response to rapidly changing conditions in adult insect populations. This has obvious ramifications for experimental analysis of immune function in insects, and serious implications for our understanding of the epidemiology and impact of pathogens and parasites in spatially structured adult insect populations.     

Generalist insects behave in a jasmonate-dependent manner on their host plants,leaving induced areas quickly and staying longer on distant parts

Plants are sessile, so have evolved sensitive ways to detect attacking herbivores and sophisticated strategies to effectively defend themselves. Insect herbivory induces synthesis of the phytohormone jasmonic acid which activates downstream metabolic pathways for various chemical defences such as toxins and digestion inhibitors. Insects are also sophisticated animals, and many have coevolved physiological adaptations that negate this induced plant defence. Insect behaviour has rarely been studied in the context of induced plant defence, although behavioural adaptation to induced plant chemistry may allow insects to bypass the host''s defence system. By visualizing jasmonate-responsive gene expression within whole plants, we uncovered spatial and temporal limits to the systemic spread of plant chemical defence following herbivory. By carefully tracking insect movement, we found induced changes in plant chemistry were detected by generalist Helicoverpa armigera insects which then modified their behaviour in response, moving away from induced parts and staying longer on uninduced parts of the same plant. This study reveals that there are plant-wide signals rapidly generated following herbivory that allow insects to detect the heterogeneity of plant chemical defences. Some insects use these signals to move around the plant, avoiding localized sites of induction and staying ahead of induced toxic metabolites.     

An inducible morphological defence is a passive by-product of behaviour in a marine snail

Many organisms have evolved inducible defences in response to spatial and temporal variability in predation risk. These defences are assumed to incur large costs to prey; however, few studies have investigated the mechanisms and costs underlying these adaptive responses. I examined the proximate cause of predator-induced shell thickening in a marine snail (Nucella lamellosa) and tested whether induced thickening leads to an increase in structural strength. Results indicate that although predators (crabs) induce thicker shells, the response is a passive by-product of reduced feeding and somatic growth rather than an active physiological response to predation risk. Physical tests indicate that although the shells of predator-induced snails are significantly stronger, the increase in performance is no different than that of snails with limited access to food. Increased shell strength is attributable to an increase in the energetically inexpensive microstructural layer rather than to material property changes in the shell. This mechanism suggests that predator-induced shell defences may be neither energetically nor developmentally costly. Positive correlations between antipredator behaviour and morphological defences may explain commonly observed associations between growth reduction and defence production in other systems and could have implications for the evolutionary potential of these plastic traits.     

Foliar aphid feeding recruits rhizosphere bacteria and primes plant immunity against pathogenic and non-pathogenic bacteria in pepper

Background and Aims

Plants modulate defence signalling networks in response to different biotic stresses. The present study evaluated the effect of a phloem-sucking aphid on plant defence mechanisms in pepper (Capsicum annuum) during subsequent pathogen attacks on leaves and rhizosphere bacteria on roots.

Methods

Plants were pretreated with aphids and/or the chemical trigger benzothiadiazol (BTH) 7 d before being challenged with two pathogenic bacteria, Xanthomonas axonopodis pv. vesicatoria (Xav) as a compatible pathogen and X. axonopodis pv. glycines (Xag) as an incompatible (non-host) pathogen.

Key Results

Disease severity was noticeably lower in aphid- and BTH + aphid-treated plants than in controls. Although treatment with BTH or aphids alone did not affect the hypersensitive response (HR) against Xag strain 8ra, the combination treatment had a synergistic effect on the HR. The aphid population was reduced by BTH pretreatment and by combination treatment with BTH and bacterial pathogens in a synergistic manner. Analysis of the expression of the defence-related genes Capsicum annum pathogenesis-related gene 9 (CaPR9), chitinase 2 (CaCHI2), SAR8·2 and Lipoxygenase1 (CaLOX1) revealed that aphid infestation resulted in the priming of the systemic defence responses against compatible and incompatible pathogens. Conversely, pre-challenge with the compatible pathogen Xav on pepper leaves significantly reduced aphid numbers. Aphid infestation increased the population of the beneficial Bacillus subtilis GB03 but reduced that of the pathogenic Ralstonia solanacearum SL1931. The expression of defence-related genes in the root and leaf after aphid feeding indicated that the above-ground aphid infestation elicited salicylic acid and jasmonic acid signalling throughout the whole plant.

Conclusions

The findings of this study show that aphid feeding elicits plant resistance responses and attracts beneficial bacterial populations to help the plant cope with subsequent pathogen attacks.     

Parents lend a helping hand to their offspring in plant defence

Plants under attack by pathogens and pests can mount a range of inducible defences, encompassing both chemical and structural changes. Although few reports exist, it appears that plants responding to pathogen or herbivore attack, or chemical defence elicitors, may produce progeny that are better able to defend themselves against attack, compared with progeny from unthreatened or untreated plants. To date, all research on transgenerational effects of biotic stress has been conducted on dicotyledenous plants. We examined the possibility that resistance induced by application of chemical defence elicitors to the monocot plant barley, could be passed on to the progeny. Plants were treated with acibenzolar-S-methyl (ASM) or saccharin, and grain harvested at maturity. Germination was unaffected in seed collected from plants treated with saccharin, while germination was reduced significantly in seed collected from ASM-treated plants. The subsequent growth of the seedlings was not significantly different in any of the treatments. However, plants from parents treated with both ASM or saccharin exhibited significantly enhanced resistance to infection by Rhynchosporium commune, despite not being treated with elicitor themselves. These data hint at the possibility of producing disease-resistant plants by exposing parent plants to chemical elicitors.     

Response of the entomopathogenic fungus Pandora neoaphidis to aphid-induced plant volatiles

We used a model plant-aphid system to investigate whether the aphid-specific entomopathogenic fungus Pandora neoaphidis responds to aphid-induced defence by the broad-bean plant, Vicia faba. Laboratory experiments indicated that neither in vivo sporulation, conidia size nor the in vitro growth of P. neoaphidis was affected by Acyrthosiphon pisum-induced V. faba volatiles. The proportion of conidia germinating on A. pisum feeding on previously damaged plants was significantly greater than on aphids feeding on undamaged plants, suggesting a direct functional effect of the plant volatiles on the fungus. However, there were no significant differences in the infectivity of P. neoaphidis towards A. pisum feeding on either undamaged V. faba plants or plants previously infested with A. pisum. Therefore, these results provide no evidence to suggest that P. neoaphidis contributes to plant indirect defence strategies.     

Extending the Bacillus cereus group genomics to putative food-borne pathogens of different toxicity

The Bacillus cereus group represents sporulating soil bacteria containing pathogenic strains which may cause diarrheic or emetic food poisoning outbreaks. Multiple locus sequence typing revealed a presence in natural samples of these bacteria of about 30 clonal complexes. Application of genomic methods to this group was however biased due to the major interest for representatives closely related to Bacillus anthracis. Albeit the most important food-borne pathogens were not yet defined, existing data indicate that they are scattered all over the phylogenetic tree. The preliminary analysis of the sequences of three genomes discussed in this paper narrows down the gaps in our knowledge of the B. cereus group. The strain NVH391-98 is a rare but particularly severe food-borne pathogen. Sequencing revealed that the strain should be a representative of a novel bacterial species, for which the name Bacillus cytotoxis or Bacillus cytotoxicus is proposed. This strain has a reduced genome size compared to other B. cereus group strains. Genome analysis revealed absence of sigma B factor and the presence of genes encoding diarrheic Nhe toxin, not detected earlier. The strain B. cereus F837/76 represents a clonal complex close to that of B. anthracis. Including F837/76, three such B. cereus strains had been sequenced. Alignment of genomes suggests that B. anthracis is their common ancestor. Since such strains often emerge from clinical cases, they merit a special attention. The third strain, KBAB4, is a typical facultative psychrophile generally found in soil. Phylogenic studies show that in nature it is the most active group in terms of gene exchange. Genomic sequence revealed high presence of extra-chromosomal genetic material (about 530kb) that may account for this phenomenon. Genes coding Nhe-like toxin were found on a big plasmid in this strain. This may indicate a potential mechanism of toxicity spread from the psychrophile strain community. The results of this genomic work and ecological compartments of different strains incite to consider a necessity of creating prophylactic vaccines against bacteria closely related to NVH391-98 and F837/76. Presumably developing of such vaccines can be based on the properties of non-pathogenic strains such as KBAB4 or ATCC14579 reported here or earlier. By comparing the protein coding genes of strains being sequenced in this project to others we estimate the shared proteome, or core genome, in the B. cereus group to be 3000+/-200 genes and the total proteome, or pan-genome, to be 20-25,000 genes.     

Worldwide Distribution of Potato-Cyst Nematodes and Their Importance in Crop Production

The potato-cyst nematodes Heterodera rostochiensis and H. pallida are important pathogens of potatoes, a basic food crop. When soil populations of either species are high, potato yields are often less than the seed planted. Apparently, these nematodes originated in the Andean mountains of South America, the home of the potato. One or both species have spread from this region to approximately 47 countries. The two species may occur together or separately in potato-growing areas. Although these nematodes can be spread in numerous ways, contaminated soil associated with seed potatoes, farm machinery, and reusable containers is among the most important. An integrated control program used in the U.S.A. is described.     

Simultaneous detection of pathogenic <Emphasis Type="Italic">B. cereus,S. aureus</Emphasis> and <Emphasis Type="Italic">L. monocytogenes</Emphasis> by multiplex PCR

Three important foodborne pathogens, Bacillus cereus, Listeria monocytogenes and Staphylococcus aureus are of major concern for food safety in terms of frequency and seriousness of the disease. The occurrence these three important pathogens and their coexistence in food matrices are predominant. Moreover, symptoms associated with B. cereus and S. aureus food poisoning not only closely resembles each other but can also be overlapping with other foodborne infections. In this context, detection of these three pathogens simultaneously in food samples by a single multiplex PCR (mPCR) would have advantages in terms of rapidity and cost saving, when compared with single organism specific PCRs. mPCR has been standardized by targeting three major diarrheal enterotoxin genes hbl A, cyt K and nhe A of B. cereus, virulence associated nuc and Ent B genes of S. aureus and virulence associated hly and iap genes of L. monocytogenes along with internal amplification control (IAC). The results showed that mPCR accurately identified all the three organisms individually or in combination without non-specificity. The mPCR was able to detect as low as 10 to 100 organisms per ml of growth following overnight enrichment of spiked food samples (vegetable biriyani and milk) and their presence in naturally contaminated samples also. The high throughput and cost effective multiplex PCR method developed in this study could provide a powerful tool for simultaneous, rapid and reliable detection of B. cereus, S. aureus and L. monocytogenes in food samples.     

Immune defence under extreme ambient temperature

Owing to global climate change, the extreme weather conditions are predicted to become more frequent, which is suggested to have an even greater impact on ecological interactions than the gradual increase in average temperatures. Here, we examined whether exposure to high ambient temperature affects immune function of the great pond snail (Lymnaea stagnalis). We quantified the levels of several immune traits from snails maintained in a non-stressful temperature (15°C) and in an extreme temperature (30°C) that occurs in small ponds during hot summers. We found that snails exposed to high temperature had weaker immune defence, which potentially predisposes them to infections. However, while phenoloxidase and antibacterial activity of snail haemolymph were reduced at high temperature, haemocyte concentration was not affected. This suggests that the effect of high temperature on snail susceptibility to infections may vary across different pathogens because different components of invertebrate immune defence have different roles in resistance.     

Endemic cattle diseases: comparative epidemiology and governance

Cattle are infected by a community of endemic pathogens with different epidemiological properties that invoke different managerial and governmental responses. We present characteristics of pathogens that influence their ability to persist in the UK, and describe a qualitative framework of factors that influence the political response to a livestock disease. We develop simple transmission models for three pathogens (bovine viral diarrhoea virus, bovine herpesvirus and Mycobacterium avium spp. paratuberculosis) using observed cattle movements, and compare the outcomes to an extensive dataset. The results demonstrate that the epidemiology of the three pathogens is determined by different aspects of within- and between-farm processes, which has economic, legal and political implications for control. We consider how these pathogens, and Mycobacterium bovis (the agent of bovine tuberculosis), may be classified by the process by which they persist and by their political profile. We further consider the dynamic interaction of these classifications with pathogen prevalence and with the action taken by the government.     

Subtle cues of predation risk: starlings respond to a predator's direction of eye-gaze

For prey animals to negotiate successfully the fundamental trade-off between predation and starvation, a realistic assessment of predation risk is vital. Prey responses to conspicuous indicators of risk (such as looming predators or fleeing conspecifics) are well documented, but there should also be strong selection for the detection of more subtle cues. A predator's head orientation and eye-gaze direction are good candidates for subtle but useful indicators of risk, since many predators orient their head and eyes towards their prey as they attack. We describe the first explicit demonstration of a bird responding to a live predator's eye-gaze direction. We present wild-caught European starlings (Sturnus vulgaris) with human 'predators' whose frontal appearance and gaze direction are manipulated independently, and show that starlings are sensitive to the predator's orientation, the presence of eyes and the direction of eye-gaze. Starlings respond in a functionally significant manner: when the predator's gaze was averted, starlings resumed feeding earlier, at a higher rate and consumed more food overall. By correctly assessing lower risk and returning to feeding activity earlier (as in this study), the animal gains a competitive advantage over conspecifics that do not respond to the subtle predator cue in this way.     

Chemical deterrent enables a socially parasitic ant to invade multiple hosts

Social parasites are involved in a coevolutionary arms race, which drives increasing specialization resulting in a very narrow host range. The Formicoxenus ants are a small group of social parasites with a xenobiotic lifestyle. Formicoxenus quebecensis and Formicoxenus provancheri are highly specialized ants using chemical mimicry to blend into their respective Myrmica ant host colonies. However, Formicoxenus nitidulus is unique in being able to survive in over 11 different ant host species. We observed that when live or dead F. nitidulus adults are seized by their host they are immediately dropped undamaged, despite possessing a cuticular hydrocarbon profile that differs markedly from its host. Hexane extracts of the F. nitidulus cuticle made previously acceptable prey items unattractive to their Formica host, indicating a chemical deterrent effect. This is the first time that a social parasite has been shown to exploit the generalized deterrence strategy to avoid host aggression over long periods of time. This supports the idea that coevolved and generalist diseases or parasites require fundamentally different defence mechanisms. We suggest that F. nitidulus uses its cuticular chemistry, possible alkadienes, as a novel deterrent mechanism to allow it to switch hosts easily and so become a widespread and abundant social parasite.     

Translocation of bacteria from the gut to the eggs triggers maternal transgenerational immune priming in Tribolium castaneum

Invertebrates can be primed to enhance their protection against pathogens they have encountered before. This enhanced immunity can be passed maternally or paternally to the offspring and is known as transgenerational immune priming. We challenged larvae of the red flour beetle Tribolium castaneum by feeding them on diets supplemented with Escherichia coli, Micrococcus luteus or Pseudomonas entomophila, thus mimicking natural exposure to pathogens. The oral uptake of bacteria induced immunity-related genes in the offspring, but did not affect the methylation status of the egg DNA. However, we observed the translocation of bacteria or bacterial fragments from the gut to the developing eggs via the female reproductive system. Such translocating microbial elicitors are postulated to trigger bacterial strain-specific immune responses in the offspring and provide an alternative mechanistic explanation for maternal transgenerational immune priming in coleopteran insects.     

Evidence that implicit assumptions of ‘no evolution’ of disease vectors in changing environments can be violated on a rapid timescale

Projected impacts of climate change on vector-borne disease dynamics must consider many variables relevant to hosts, vectors and pathogens, including how altered environmental characteristics might affect the spatial distributions of vector species. However, many predictive models for vector distributions consider their habitat requirements to be fixed over relevant time-scales, when they may actually be capable of rapid evolutionary change and even adaptation. We examine the genetic signature of a spatial expansion by an invasive vector into locations with novel temperature conditions compared to its native range as a proxy for how existing vector populations may respond to temporally changing habitat. Specifically, we compare invasions into different climate ranges and characterize the importance of selection from the invaded habitat. We demonstrate that vector species can exhibit evolutionary responses (altered allelic frequencies) to a temperature gradient in as little as 7–10 years even in the presence of high gene flow, and further, that this response varies depending on the strength of selection. We interpret these findings in the context of climate change predictions for vector populations and emphasize the importance of incorporating vector evolution into models of future vector-borne disease dynamics.     

Inducible defence and its modulation by environmental stress in the red alga Chondrus yendoi (Yamada and Mikami in Mikami, 1965) from Honshu Island, Japan

Among the numerous anti-herbivore defences developed by macroalgae, chemical and morphological traits are best documented and understood. Plant defence theory suggests that these resistances, which can either be constitutive or inducible, are associated with metabolic costs. They should therefore be impaired under conditions of energy limitation, but evidence for this prediction is scarce. In two subsequent experiments, we tested whether a reduction of light availability is changing feeding rates of the two mesoherbivores Idotea ochotensis and Lacuna smithii on the red alga Chondrus yendoi. Algal individuals were kept in outdoor mesocosm facilities for 10 days, during which we manipulated the amount of incoming sunlight at 6 levels (0%-99% reduction, i.e. 2000-20 μmol s^− 1 m^− 2). Orthogonal to this, we established the presence or absence of one of the herbivores to test whether C. yendoi can generate a defence. Algal palatability was investigated afterwards in no-choice feeding assays using naïve grazer individuals. The consumption of algal tissue in L. smithii increased with decreasing light, while this was not the case for I. ochotensis. However, we found a defence induced as a reaction to herbivory only by the highly mobile isopod but not when the slowly moving snail grazed on C. yendoi. Isopod total consumption rates in our experiments were 40 times higher than those of the gastropods. We therefore suggest that C. yendoi exhibits grazer-specific reactions to herbivory, depending on the mobility and voracity of the consumers. Interestingly, only for one of the grazers, i.e. the snail, short-term light reduction influenced the palatability of algal tissue. We discuss different but not mutually exclusive models that could explain this pattern. In conclusion, we view this three-species system as an illustrative example for specificity in grazer-algal interactions and their modification by environmental stress.     

Defence strategies against a parasitoid wasp in Drosophila: fight or flight?

Hosts may defend themselves against parasitism through a wide variety of defence mechanisms, but due to finite resources, investment in one defence mechanism may trade-off with investment in another mechanism. We studied resistance strategies against the parasitoid wasp Leptopilina boulardi in two Drosophila species. We found that D. melanogaster had significantly lower physiological resistance against L. boulardi than D. simulans, and hypothesized that D. melanogaster might instead invest more heavily in other forms of defence, such as behavioural defence. We found that when given a choice between clean oviposition sites and sites infested with wasps, both D. melanogaster and D. simulans detected and avoided infested sites, which presumably limits later exposure of their offspring to infection. Unlike D. simulans, however, D. melanogaster laid significantly fewer eggs than controls in the forced presence of wasps. Our findings suggest that D. melanogaster relies more heavily on behavioural avoidance as defence against wasp parasitism than D. simulans, and that this may compensate for a lack of physiological defence.     

Contrasting responses of bumble bees to feeding conspecifics on their familiar and unfamiliar flowers

Animals exploiting their familiar food items often avoid spatio-temporal aggregation with others by avoiding scents, less rewarding areas or visual contacts, thereby minimizing competition or interference when resources are replenished slowly in patches. When animals are searching or assessing available food sources, however, they may benefit from reducing sampling costs by following others at food sites. Therefore, animals may adjust their responses to others depending on their familiarity with foraging situations. Here, we conducted field experiments to test whether nectar-collecting bumble bees make this adjustment. We allowed free-foraging bees to choose between two inflorescences, one occupied by a conspecific bee and another unoccupied. When bees were presented with flowers of a familiar type, they avoided occupied inflorescences. In contrast, bees visited an occupied inflorescence when the flower type was unfamiliar. To our knowledge, this is the first report suggesting that animals adjust their responses to feeding conspecifics depending on their familiarity with food sources. Such behavioural flexibilities should allow foragers to both explore and exploit their environments efficiently.     

Superparasitism in Cotesia glomerata does not benefit the host plant by reduction of herbivory caused by Pieris brassicae

Superparasitism occurs in Cotesia glomerata L. (Hymenoptera: Braconidae), a gregarious endoparasitoid of Pieris spp. (Lepidoptera: Pieridae). The responses of Pieris brassicae L. larvae to superparasitism were examined in order to elucidate the ecological significance of this behaviour. Models of tritrophic interactions often imply that attraction of herbivore natural enemies by the plant constitutes a defence. Parasitoid attack on herbivores is assumed to result in a reduction in herbivory and or an increase in plant fitness. Coupled with the active involvement of the plant in producing signals, this can be seen as an indirect mediation of wound induced defence. The results show that superparasitism of P. brassicae by the parasitoid C. glomerata reduced survivorship but increased food consumption and weight growth in P. brassicae larvae. The duration of host larval development was found prolonged as the number of oviposition increased and superparasitized larvae (three to five time parasitized) grew slower than unparasitized larvae or larvae parasitized one or two times.     

Comparison of diet and feeding activity of two polychaetes, Nephtys caeca (Fabricius) and Nereis virens (Sars), in an estuarine intertidal environment in Québec, Canada

It is crucial to study how food resources are allocated in order to understand how invertebrate species of soft-bottomed benthic communities can live in the same environment, especially when belonging to the same trophic level. On the southern shore of the Lower St. Lawrence Estuary, the polychaetes Nereis virens (Nereidae) and Nephtys caeca (Nephtyidae) represent the main infaunal predators and are known to regulate (by predation) other populations within their community. For these animal populations, there is a high degree of spatial overlap in the horizontal dimension as well as vertically in the sediment column. The purpose of this study was to describe and compare the feeding activity of N. virens and N. caeca in relation to several environmental factors. The feeding activity of N. caeca was further studied under natural and experimental conditions and a feeding experiment was carried out to evaluate how the food resource is subdivided in conditions of high spatial overlap. Finally, the prospecting activity of N. virens was described under natural conditions. N. virens and N. caeca exhibited a high degree of dietary overlap, particularly at the adult stage. This food resource overlap can easily influence the regulation of these species, even though they display different feeding responses to environmental stimuli. Tides and storm events can also influence the feeding behaviour. We conclude that different behavioural feeding responses likely favour the occurrence of these two species in the same trophic environment.