The genetic architecture of defence as resistance to and tolerance of bacterial infection in Drosophila melanogaster

Defence against pathogenic infection can take two forms: resistance and tolerance. Resistance is the ability of the host to limit a pathogen burden, whereas tolerance is the ability to limit the negative consequences of infection at a given level of infection intensity. Evolutionarily, a tolerance strategy that is independent of resistance could allow the host to avoid mounting a costly immune response and, theoretically, to avoid a co‐evolutionary arms race between pathogen virulence and host resistance. Biomedically, understanding the mechanisms of tolerance and how they relate to resistance could potentially yield treatment strategies that focus on health improvement instead of pathogen elimination. To understand the impact of tolerance on host defence and identify genetic variants that determine host tolerance, we defined genetic variation in tolerance as the residual deviation from a binomial regression of fitness under infection against infection intensity. We then performed a genomewide association study to map the genetic basis of variation in resistance to and tolerance of infection by the bacterium Providencia rettgeri. We found a positive genetic correlation between resistance and tolerance, and we demonstrated that the level of resistance is highly predictive of tolerance. We identified 30 loci that predict tolerance, many of which are in genes involved in the regulation of immunity and metabolism. We used RNAi to confirm that a subset of mapped genes have a role in defence, including putative wound repair genes grainy head and debris buster. Our results indicate that tolerance is not an independent strategy from resistance, but that defence arises from a collection of physiological processes intertwined with canonical immunity and resistance.     

Pliant pathogens: Estimating viral spread when confronted with new vector,host, and environmental conditions

1. Pathogen spread rates are determined, in part, by the performance of pathogens under altered environmental conditions and their ability to persist while switching among hosts and vectors.
2. To determine the effects of new conditions (host, vector, and nutrient) on pathogen spread rate, we introduced a vector‐borne viral plant pathogen, Barley Yellow Dwarf Virus PAV (BYDV‐PAV) into hosts, vectors, and host nutrient supplies that it had not encountered for thousands of viral generations. We quantified pathogen prevalence over the course of two serial inoculations under the new conditions. Using individual‐level transmission rates from this experiment, we parameterized a dynamical model of disease spread and projected spread across host populations through a growing season.
3. A change in nutrient conditions (increased supply of phosphorus) reduced viral transmission whereas shifting to a new vector or host species had no effect on infection prevalence. However, the reduction in the new nutrient environment was only temporary; infection prevalence recovered after the second inoculation.
4. Synthesis. These results highlight how robust the pathogen, BYDV‐PAV, is to changes in its biotic and abiotic environment. Our study also highlights the need to quantify longitudinal infection information beyond snapshot assessments to project disease risk for pathogens in new environments.

     

Competitive interactions and partial displacement of Anastrepha obliqua by Ceratitis capitata in the occupation of host mangoes (Mangifera indica)

1. We examined the competitive interactions between a native fruit fly species (Anastrepha obliqua Macquart) and the invasive medfly (Ceratitis capitata Wiedemann) when these co-occur on a shared mango fruit host (Mangifera indica L.).
2. Using mango fruits of distinct levels of ripeness, we investigated both competition among larvae and among adult females for oviposition. We quantified competition by the numbers of eggs laid and the intensity of agonistic interactions between adult females.
3. Interactions between immature fruit flies led to reduced size and number of emerged adults of both species. These impacts were felt more acutely in the native species.
4. Interspecific competition between females led to fewer eggs laid on semi-ripe fruit by both species, which may be the result of niche overlap associated with oviposition.
5. Intraspecific interactions between A. obliqua individuals led to intense agonistic behaviour, with a concurrent decrease in number of landings on these host fruits.
6. These results suggest that the native species undergoes a partial niche displacement when facing the invasive species. A portion of the fundamental niche of A. obliqua remained unoccupied by the invading C. capitata, which may allow their coexistence under natural conditions.

     

Exposure of the wild bee Osmia bicornis to the honey bee pathogen Nosema ceranae

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Experimental viral spillover can harm Bombus terrestris workers under field conditions

1. Deformed wing virus (DWV), notorious for its virulence in the western honey bee (Apis mellifera) when vectored by the ectoparasitic mite Varroa destructor, is also widespread among wild bumble bee species, presumably through spillover from honey bees. Experimental studies on the virulence of DWV in Bombus spp. have provided equivocal results and have until now been confined to bumble bees under laboratory conditions.
2. Here, we inoculated commercially reared Bombus terrestris workers with DWV-A through feeding or injection and introduced them into experimental colonies placed in the field, thus exposing them to the environment and associated stressors. We monitored the survival of inoculated worker bumble bees and quantified their viral load at 10 days post inoculation.
3. Bombus terrestris workers injected with DWV-A supported high viral loads and exhibited significantly reduced median survival compared to controls. Bumble bees inoculated by feeding had low or zero detectable viral loads while their mortality did not differ from the control group.
4. Our results demonstrate that, although DWV-A is pathogenic for commercial B. terrestris, the risks for individual fitness from spillover of DWV-A during foraging on shared flowers appear limited.
5. The findings of this experiment also highlight the necessity to address the potential context-dependence of virulence when evaluating the impact of a pathogen in an alternative host.

     

Elucidating cryptic dynamics of Theileria communities in African buffalo using a high‐throughput sequencing informatics approach

1. Increasing access to next‐generation sequencing (NGS) technologies is revolutionizing the life sciences. In disease ecology, NGS‐based methods have the potential to provide higher‐resolution data on communities of parasites found in individual hosts as well as host populations.
2. Here, we demonstrate how a novel analytical method, utilizing high‐throughput sequencing of PCR amplicons, can be used to explore variation in blood‐borne parasite (Theileria—Apicomplexa: Piroplasmida) communities of African buffalo at higher resolutions than has been obtained with conventional molecular tools.
3. Results reveal temporal patterns of synchronized and opposite fluctuations of prevalence and relative abundance of Theileria spp. within the host population, suggesting heterogeneous transmission across taxa. Furthermore, we show that the community composition of Theileria spp. and their subtypes varies considerably between buffalo, with differences in composition reflected in mean and variance of overall parasitemia, thereby showing potential to elucidate previously unexplained contrasts in infection outcomes for host individuals.
4. Importantly, our methods are generalizable as they can be utilized to describe blood‐borne parasite communities in any host species. Furthermore, our methodological framework can be adapted to any parasite system given the appropriate genetic marker.
5. The findings of this study demonstrate how a novel NGS‐based analytical approach can provide fine‐scale, quantitative data, unlocking opportunities for discovery in disease ecology.

     

Temperature and host diet jointly influence the outcome of infection in a Daphnia-fungal parasite system

1. Climate change has the potential to shape the future of infectious diseases, both directly and indirectly. In aquatic systems, for example, elevated temperatures can modulate the infectivity of waterborne parasites and affect the immune response of zooplanktonic hosts. Moreover, lake warming causes shifts in the communities of primary producers towards cyanobacterial dominance, thus lowering the quality of zooplankton diet. This may further affect host fitness, resulting in suboptimal resources available for parasite growth.
2. Previous experimental studies have demonstrated the respective effects of temperature and host diet on infection outcomes, using the zooplankter Daphnia and its microparasites as model systems. Although cyanobacteria blooms and heat waves are concurrent events in nature, few attempts have been made to combine both stressors in experimental settings.
3. Here, we raised the zooplankter Daphnia (two genotypes) under a full factorial design with varying levels of temperature (the standard 19°C and elevated 23°C), food quality (Scenedesmus obliquus as high-quality green algae, Microcystis aeruginosa and Planktothrix agardhii as low-quality cyanobacteria) and exposed them to the parasitic yeast Metschnikowia bicuspidata. We recorded life history parameters of the host as well as parasite traits related to transmission.
4. The combination of low-quality cyanobacterial diets and elevated temperature resulted in additive detrimental effects on host fecundity. Low-quality diets reduced parasite output, while temperature effects were context dependent. Overall, we argue that the combined effects of elevated water temperature and poor-quality diets may decrease epidemics of a common fungal parasite under a climate change scenario.

     

Fungal pathogen and ethanol affect host selection and colonization success in ambrosia beetles

1. Ambrosia beetles exhibit broad host ranges but a narrow preference based on the condition of the host. Tissues infected by pathogens or containing ethanol can facilitate attacks by ambrosia beetles, although it still remains unclear how these factors interact.
2. The present study aimed to examine how (i) chestnut logs infected with the fungal pathogen Cryphonectria parasitica and treated with ethanol (i.e. baited with ethanol lure, soaked in ethanol or untreated) and (ii) hornbeam logs soaked in different ethanol concentrations (3–12.5%) affect host selection and colonization success of ambrosia beetles.
3. Ethanol‐soaked logs were more attractive to Anisandrus dispar than ethanol‐baited logs or untreated logs, although this difference was more evident in uninfected than infected logs. Increasing ethanol concentration in host tissues was differentially attractive to Xyleborinus saxesenii and Xylosandrus germanus. A nonlinear relationship was also documented between ethanol concentration and emergence of X. germanus adults.
4. Overall, the results obtained suggest that the presence of C. parasitica in chestnut logs can affect host selection in ambrosia beetles. In addition, the ethanol concentration in tree tissues affects host selection and colonization success, although the effect varies depending on the beetle species. This contrasting response could be a niche‐partitioning mechanism based on ethanol within host tissues.

     

Seasonal polyphenism of spotted‐wing Drosophila is affected by variation in local abiotic conditions within its invaded range,likely influencing survival and regional population dynamics

1. Overwintering Drosophila often display adaptive phenotypic differences beneficial for survival at low temperatures. However, it is unclear which morphological traits are the best estimators of abiotic conditions, how those traits are correlated with functional outcomes in cold tolerance, and whether there are regional differences in trait expression.
2. We used a combination of controlled laboratory assays, and collaborative field collections of invasive Drosophila suzukii in different areas of the United States, to study the factors affecting phenotype variability of this temperate fruit pest now found globally.
3. Laboratory studies demonstrated that winter morph (WM) trait expression is continuous within the developmental temperature niche of this species (10–25°C) and that wing length and abdominal melanization are the best predictors of the larval abiotic environment.
4. However, the duration and timing of cold exposure also produced significant variation in development time, morphology, and survival at cold temperatures. During a stress test assay conducted at ?5°C, although cold tolerance was greater among WM flies, long‐term exposure to cold temperatures as adults significantly improved summer morph (SM) survival, indicating that these traits are not controlled by a single mechanism.
5. Among wild D. suzukii populations, we found that regional variation in abiotic conditions differentially affects the expression of morphological traits, although further research is needed to determine whether these differences are genetic or environmental in origin and whether thermal susceptibility thresholds differ among populations within its invaded range.

     

Predators reduce Batrachochytrium dendrobatidis infection loads in their prey

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The effects of non-crop habitat on spotted wing drosophila (Drosophila suzukii) abundance in fruit systems: A meta-analysis

1. Drosophila suzukii (SWD) poses a threat to soft and stone fruit globally. SWD inhabits non-crop areas adjacent to farms from where it moves into crops to cause damage. Effective IPM control strategies, considering both the crop and non-crop area, are needed to control this economically important pest.
2. We conducted a meta-analysis to quantify the impacts of different non-crop habitats around fruit farms on SWD populations, comparing abundance of SWD trapped in crop and non-crop habitats.
3. Overall, SWD abundance was greater in non-crop habitats than in cropped areas and this difference was greatest in farms adjacent to woodland, or field margins containing known SWD host plants.
4. The difference in SWD abundance between crop and non-crop habitats was not affected by crop type but was greatest in the winter months and in conventional compared to organic farms, indicating conventional approaches can reduce relative SWD abundance.
5. Drosophila suzukii overwinter in non-crop habitats which provide refuge outside the cropping season. However, certain habitats support greater relative abundance of SWD than others and this is also affected by farm management. We discuss what these findings mean for effective control of SWD.

     

Interactive effects between diet and genotypes of host and pathogen define the severity of infection

Host resistance and parasite virulence are influenced by multiple interacting factors in complex natural communities. Yet, these interactive effects are seldom studied concurrently, resulting in poor understanding of host‐pathogen‐environment dynamics. Here, we investigated how the level of opportunist pathogen virulence, strength of host immunity and the host condition manipulated via diet affect the survival of wood tiger moth Parasemia plantaginis (Arctidae). Larvae from “low cuticular melanin” and “high cuticular melanin” (considered as low and high pathogen resistance, respectively) selection lines were infected with moderately and highly virulent bacteria strains of Serratia marcescens, while simultaneously manipulating host diet (with or without antibacterial compounds). We measured host survival and food preference before and after infection to test whether the larvae “self‐medicate” by choosing an anti‐infection diet (Plantago major, i.e., plantain leaf) over lettuce (Lactuca sativa). “High melanin” larvae were more resistant than “low melanin” larvae to the less virulent strain that had slower growth and colonization rate compared with the more virulent strain. Cuticular melanin did not enhance survival when the larvae were infected with the highly virulent strain. Anti‐infection diet enhanced survival of the “high melanin” but not the “low melanin” hosts. Survival was dependent on family origin even within the melanin selection lines. Despite the intrinsic preference for lettuce, no evidence of self‐medication was found. These results demonstrate that the relative benefit of host cuticular melanin depends on both diet and pathogen virulence: plantain diet only boosted the immunity of already resistant “high melanin” hosts, and cuticular melanin increased host survival only when infected with moderately virulent pathogen. Moreover, there was considerable variation in host survival between families within both melanin lines suggesting genetic basis for resistance. These results indicate that although melanin is an important predictor of insect immunity, its effect on disease outcomes greatly depends on other interacting factors.     

Assessing Condition-dependence of Male Flash Signals in <Emphasis Type="Italic">Photinus</Emphasis> Fireflies

Females often show a preference for exaggerated male sexual traits or courtship behaviors. Such preferences can benefit females if trait expression is correlated with male genetic quality or phenotypic condition. Previous studies of several Photinus fireflies have revealed considerable intraspecific variation in the bioluminescent courtship signals emitted by males, and have also demonstrated that females prefer more conspicuous male signals. Thus, females might gain information about male phenotypic quality if courtship signals reflect male condition. We examined possible condition-dependence of Photinus male courtship signals using two complementary approaches. First we experimentally manipulated male mating status, which is expected to affect male condition by depleting resources required for nuptial gift formation, and looked at how individual male flash signals changed with mating status and over time. We used an additional approach to assess condition-dependence by examining whether a relationship exists between flash signal parameters and measures of male condition and body shape. We found that the pulse rate of P. greeni courtship signals was not altered by male mating status or age, and that the pulse duration of P. ignitus signals was also not affected by male mating status. In P. pyralis fireflies, males showed a non-significant trend toward reduced signal pulse duration with age. When we examined the relationship between male flash signals and condition measures, we found no effect of male condition or body shape on courtship signals in P. greeni or P. ignitus; in P. pyralis, males with wider body shapes produced longer duration flash signals. On the other hand, we found no evidence in P. pyralis that condition predicted flash duration. Taken together, these results indicate that Photinus males’ flash signals do not reflect adult male condition, and suggest that females are unlikely to use courtship signals as an indicator of male phenotypic quality.     

Weak relationships of parasite infection with sexual and life‐history traits in wild‐caught Texas field crickets (Gryllus texensis)

1. Sex differences in immune investment and infection rate are predicted due to the divergent life histories of males and females, where females invest more toward immunity due to the fitness consequences of a reduced lifespan and males allocate less toward immunity due to increased resource investment in traits critical to sexual selection. Consequently, males are expected to fight infection less adeptly, resulting in higher parasite loads relative to females across all taxa.
2. Wild animals rarely face a single parasite within their given environment, yet nearly all studies on sex‐biased infection rates have focused on a single host–parasite relationship. Here, we investigate how simultaneous natural infections of ecto‐ and endosymbionts (i.e. both parasitic and phoretic taxa) correlate with sex biases in host immune response and reproductive investment in a field‐caught cricket, Gryllus texensis.
3. Our comprehensive analysis found no significant sex differences in two measures of immune response (melanization and nodulation), and found no strong evidence of a sex bias in the prevalence or intensity of parasitism by the three most common parasites infecting wild G. texensis field crickets (Eutrombidiidae, gregarines, and nematodes).
4. Two traits related to female fitness, egg number and egg size, showed no relation to parasitic infection; however, males having wider heads and poorer body condition were significantly more infected by eutrombidiid mites, gregarines, and nematodes.
5. Despite frequent predictions of male‐biased parasitism in the literature, our results concur with many other studies indicating that the divergent life histories of males and females alone are not sufficient to explain natural infection rates in wild insects.

     

Isolation and Identification of Bacteria Associated with Adult Laboratory Mexican Fruit Flies, Anastrepha ludens (Diptera: Tephritidae)

From the guts of new and old colonies (female and male) of Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae), we identified a total of 18 different bacterial species belonging to the family Enterobacteriaceae, Pseudomonadaceae, Vibrionaceae, Micrococcaceae, Deinococcacea, Bacillaceae, and the genus Listeria. Enterobacter, Providencia, Serratia, and Staphylococcus spp. were the most frequently isolated genera, with Citrobacter, Streptococcus, Aerococcus, and Listeria found less frequently. We found Bacillus cereus, Enterobacter sakazakii, Providencia stuartii, and Pseudomonas aeruginosa only in the new colony, Aeromonas hydrophila and Klebsiella pneumoniae spp. pneumoniae only in the old colony. We also studied resistance/sensitivity to 12 antibiotics for six bacterial isolates such as Enterobacter cloacae, E. sakazakii, K. pneumoniae spp., Providencia rettgeri, P. aeruginosa, and Bacillus cereus. Isolates on the whole were resistant to penicillin and ampicillin (five of six isolates) and sensitive to rifampin and streptomycin (six of six isolates). Antibiotic resistance profiles might be useful characteristics for distinguishing among species and strains of these bacteria, probably having ecological significance with respect to intra- and inter-specific competition within host cadavers, and could have implications for the utility of these organisms for biological control, including the alternative control strategy, paratransgenesis. Received: 28 August 2000 / Accepted: 2 October 2000     

The infection of Moina macrocopa by a colonial peritrich, Epistylis daphniae, and its effects on the host

• 1 The effects of infection by Epistylis daphniae on its host, Moina macrocopa, were studied in the laboratory at 28°C by comparing the growth, reproduction and survival between infected and uninfected hosts.
• 2 Infestation by epizoites had little or no effect on the survival of the dadoceran hosts when adequate food was present.
• 3 The infected cladocerans had lower growth rates as juveniles, lower net reproduction rates as adults, and smaller body size at death than uninfected hosts.
• 4 The index of infection at different stages in the life cycle was related to the durations of intermoult period. Ranked in order of both index of infection and intermoult duration, the development stages were: old adult > young adult > juvenile.

     

Inter‐specific competition and competition‐free space in the tephritid parasitoids Utetes anastrephae and Doryctobracon areolatus (Hymenoptera: Braconidae: Opiinae)

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Effect of forest stand type on host plant quality and direct and indirect effects on pine sawfly performance

1. Observed lower levels of herbivory in mixed compared with monoculture stands have been hypothesized to depend on top-down forces, through higher predation pressure by natural enemies or through bottom-up mechanisms through plant quality effects on herbivore performance.
2. In this study, we compared the performance measured as host plant induced mortality, cocoon weight, and predation mortality of the European pine sawfly Neodiprion sertifer (Geoffroy) (Hymenoptera, Diprionidae) in mixed and monoculture forest stands.
3. We did not observe a difference in host plant induced mortality, cocoon weight, or predation mortality between mixed and monoculture forest stands. We did find an effect of local conditions around each experimental tree on pine sawfly performance. For example, the nitrogen content of pine needles is negatively affected by the proportion of pine around the experimental tree, which in turn increases the survival of sawfly larvae.
4. The results suggest that local conditions around individual trees are more important for the performance of the European pine sawfly than stand type, i.e. mixed or monoculture plant stands.
5. We conclude that the ongoing trend for diversification within commercial forestry calls for more research where the effects of both bottom-up and top-down effects are studied at several spatial scales.

     

Complex interactions between bacteria and haemosporidia in coinfected hosts: An experiment

1. Hosts are typically coinfected by multiple parasite species whose interactions might be synergetic or antagonistic, producing unpredictable physiological and pathological impacts on the host. This study shows the interaction between Plasmodium spp. and Leucocytozoon spp. in birds experimentally infected or not infected with Mycoplasma gallisepticum.
2. In 1994, the bacterium Mycoplasma gallisepticum jumped from poultry to wild birds in which it caused a major epidemic in North America. Birds infected with M. gallisepticum show conjunctivitis as well as increased levels of corticosterone.
3. Malaria and other haemosporidia are widespread in birds, and chronic infections become apparent with the detectable presence of the parasite in peripheral blood in response to elevated levels of natural or experimental corticosterone levels.
4. Knowing the immunosuppressive effect of corticosterone on the avian immune system, we tested the hypothesis that chronic infections of Plasmodium spp. and Leucocytozoon spp. in house finches would respond to experimental inoculation with M. gallisepticum as corticosterone levels are known to increase following inoculation.
5. Plasmodium spp. infection intensity increased within days of M. gallisepticum inoculation as shown both by the appearance of infected erythrocytes and by the increase in the number and the intensity of positive PCR tests.
6. Leucocytozoon spp. infection intensity increased when Plasmodium spp. infection intensity increased, but not in response to M. gallisepticum inoculation. Leucocytozoon spp. and Plasmodium spp. seemed to compete in the host as shown by a negative correlation between the changes in their PCR score when both pathogens were present in the same individual.
7. Host responses to coinfection with multiple pathogens measured by the hematocrit and white blood cell count depended on the haemosporidian community composition. Host investment in the leukocyte response was higher in the single‐haemosporidia‐infected groups when birds were infected with M. gallisepticum.
8. A trade‐off was observed between the immune control of the chronic infection (Plasmodium spp./Leucocytozoon spp.) and the immune response to the novel bacterial infection (M. gallisepticum).