Trade-offs in insect disease resistance

The ability to mount an efficient immune response should be an important life-history trait as parasitism can impact upon an individual's fecundity and survival prospects, and hence its fitness. However, immune function is likely to be costly as resources must be divided between many important traits. Whilst many studies have examined host resistance to particular parasite types, fewer have considered general immune responses. Studies that have considered general immune responses tend to do so in vertebrate models. However, the complexity of the vertebrate immune system makes the examination of evolutionary aspects of immune function difficult. Using larvae of the genus Spodoptera (Lepidoptera: Noctuidae) as a model system, this study examines' genetic and phenotypic aspects of innate immunity. The aims were to assess the levels of additive genetic variation maintained in immune traits, to consider possible costs that could maintain this variation, and to assess the role of phenotypic plasticity in ameliorating those costs. A key finding of this study was that high levels of additive genetic variation were maintained in all of the measured Immune traits. Analysis of the genetic correlations between traits revealed potential trade-offs within the immune system and between immune components and body condition. In addition, it was shown that larvae living at high densities invest more in immune function than those living in solitary conditions, suggesting that larvae can minimise the costs of immune function by employing them only when the risk of pathogenesis is high

Trade-offs between personal immunity and reproduction in the burying beetle, N. vespilloides

We know that parental investment and immune investment are costly processes, but it is unclear which trait will be prioritised when both may be required. Here we address this question using the burying beetle Nicrophorus vespilloides, carrion breeders that exhibit biparental care of young. Our results show that immunosuppression occurs during provision of parental care. We measured Phenoloxidase (PO) on Day 1-8 of the breeding bout and results show a clear decrease in PO immediately from presentation of the breeding resource onwards. Having established baseline immune investment during breeding we then manipulated immune investment at different times by applying a wounding challenge. Beetles were wounded prior to and during the parental care period and reproductive investment quantified. Different effects on reproductive output occur depending on the timing of wounding. Challenging the immune system with wounding prior to breeding does not affect reproductive output and subsequent Lifetime Reproductive Success (LRS). LRS is also unaffected by applying an immune elicitor prior to breeding, though different arms of the immune system are up/downregulated, perhaps indicating a trade-off between cellular and humoral immunity. In contrast, wounding during breeding reduces reproductive output and to the greatest extent if the challenge is applied early in the breeding bout. Despite being immunosuppressed, breeding beetles can still respond to wounding by increasing PO, albeit not to pre-breeding levels. This upregulation of PO during breeding may affect parental investment, resulting in a reduction in reproductive output. The potential role of juvenile hormone in controlling this trade-off is discussed

Consumption of rodenticide baits by invertebrates as a potential route into the diet of insectivores

Non-target species are commonly exposed to anticoagulant rodenticides worldwide, which may pose a key threat to declining species. However, the main pathway of exposure is usually unknown, potentially hindering conservation efforts. This study aimed to examine whether baits mixed with the biomarker rhodamine B can be used to track invertebrate consumption of rodenticides in a field environment, using this to observe whether invertebrate prey are a potential vector for anticoagulant rodenticides in the diet of insectivores such as the European hedgehog (Erinaceus europaeus). Rhodamine B baits were found to create an observable response. Uptake was negligible in captured insects; however, 20.7% of slugs and 18.4% of snails captured showed uptake of bait. Maximum temperature, distance from bait, proximity to buildings, and the addition of copper tape to bait boxes all influenced the rate of bait uptake in molluscs. Based on these data, it seems likely that molluscs could be a source of rodenticide poisoning in insectivores. This research demonstrates which prey may pose exposure risks to insectivores and likely environmental factors, knowledge of which can guide effective mitigation measures. We suggest that further investigation into using mollusc repellents around bait boxes should be considered

Social immunity of the family: parental contributions to a public good modulated by brood size.

Social immunity refers to any immune defence that benefits others, besides the individual that mounts the response. Since contributions to social immunity are known to be personally costly, they are contributions to a public good. However, individuals vary in their contributions to this public good and it is unclear why. Here we investigate whether they are responding to contributions made by others with experiments on burying beetle (Nicrophorus vespilloides) families. In this species, females, males and larvae each contribute to social immunity through the application of antimicrobial exudates upon the carrion breeding resource. We show experimentally that mothers reduce their contributions to social immunity when raising large broods, and test two contrasting hypotheses to explain why. Either mothers are treating social immunity as a public good, investing less in social immunity when their offspring collectively contribute more, or mothers are trading off investment in social immunity with investment in parental care. Overall, our experiments yield no evidence to support the existence of a trade-off between social immunity and other parental care traits: we found no evidence of a trade-off in terms of time allocated to each activity, nor did the relationship between social immunity and brood size change with female condition. Instead, and consistent with predictions from models of public goods games, we found that higher quality mothers contributed more to social immunity. Therefore our results suggest that mothers are playing a public goods game with their offspring to determine their personal contribution to the defence of the carrion breeding resource.AD was supported by NERC grant NE/H019731/1 to RMK. ODeG was supported by the Cambridge Trust and the Mexican Council for Science and Technology (CONACyT). RMK was supported in part by ERC Consolidators grant 310785 BALDWINIAN_BEETLES. SCC was supported by a NERC fellowship (NE/H014225/2), CER was supported by a Department for Employment and Learning PhD studentship. We thank A. Backhouse for help in maintaining the burying beetle population. We thank two anonymous reviewers for helpful comments on the manuscript.This is the final version of the article. It was first available from Springer via http://dx.doi.org/10.1007/s10682-015-9806-

Scavenging beetles control the temporal response of soil communities to carrion decomposition

1. Carrion is a frequent but overlooked source of nutrients to the soil. The decomposition of carrion is accelerated by invertebrate scavengers but the impact of the scavengers on below-ground biota and its functions is scarcely known. 2. We conducted a laboratory experiment to investigate the effects of the burying beetle Nicrophorus vespilloides on the soil community of a temperate broadleaved forest. We assembled microcosms from soil collected from an oak woodland and treated them with mouse (Mus musculus) carcasses and mating pairs of burying beetles (♀+♂) in a factorial design with control soils. We sampled independent replicates over time to investigate how the beetles affect soil microarthropods and microbial biomass (bacteria and fungi) in relation to soil pH and organic matter content. 3. The beetle treatment initially reduced total microbial biomass and abundance of major groups of microarthropods relative to the control soil. At the same time, organic matter increased in the beetle treatment and then dropped to the pre-beetle level (i.e. soil baseline) at the end of the beetle breeding cycle (2 weeks). The rapid temporal changes in organic matter were mimicked by the relative abundances of the dominant microarthropod groups, with Oribatida relatively more abundant than Collembola and predaceous mites in the beetle treatment. The overall final effect of the beetle (relative to the laboratory control) on microarthropods was negative but the beetle kept these variables within the levels observed for freshly collected soil (baseline), while the final effect on pH was positive, and most likely driven by the surplus of nutrients from the carcass and biochemical changes triggered by the decomposition process. 4. In nature, scavenging invertebrates are widespread. Our study demonstrates that beetles breeding in carcasses regulate the dynamics of key components of the soil food web, including microbial biomass, changes in the relative abundances of dominant microarthropods, and soil organic matter and pH. Given the abundance of these beetles in nature, the study implies that the distribution of these beetles is a key driver of variation in soil nutrient cycling in woodlands

Diet modulates the relationship between immune gene expression and functional immune responses

Nutrition is vital to health and the availability of resources has long been acknowledged as a key factor in the ability to fight off parasites, as investing in the immune system is costly. Resources have typically been considered as something of a "black box", with the quantity of available food being used as a proxy for resource limitation. However, food is a complex mixture of macro- and micronutrients, the precise balance of which determines an animal's fitness. Here we use a state-space modelling approach, the Geometric Framework for Nutrition (GFN), to assess for the first time, how the balance and amount of nutrients affects an animal's ability to mount an immune response to a pathogenic infection. Spodoptera littoralis caterpillars were assigned to one of 20 diets that varied in the ratio of macronutrients (protein and carbohydrate) and their calorie content to cover a large region of nutrient space. Caterpillars were then handled or injected with either live or dead Xenorhabdus nematophila bacterial cells. The expression of nine genes (5 immune, 4 non-immune) was measured 20 h post immune challenge. For two of the immune genes (PPO and Lysozyme) we also measured the relevant functional immune response in the haemolymph. Gene expression and functional immune responses were then mapped against nutritional intake. The expression of all immune genes was up-regulated by injection with dead bacteria, but only those in the IMD pathway (Moricin and Relish) were substantially up-regulated by both dead and live bacterial challenge. Functional immune responses increased with the protein content of the diet but the expression of immune genes was much less predictable. Our results indicate that diet does play an important role in the ability of an animal to mount an adequate immune response, with the availability of protein being the most important predictor of the functional (physiological) immune response. Importantly, however, immune gene expression responds quite differently to functional immunity and we would caution against using gene expression as a proxy for immune investment, as it is unlikely to be reliable indicator of the immune response, except under specific dietary conditions. [Abstract copyright: Copyright © 2019. Published by Elsevier Ltd.

The complex interactions between nutrition, immunity and infection in insects

Insects are the most diverse animal group on the planet. Their success is reflected by the diversity of habitats in which they live. However, these habitats have undergone great changes in recent decades; understanding how these changes affect insect health and fitness is an important challenge for insect conservation. In this Review, we focus on the research that links the nutritional environment with infection and immune status in insects. We first discuss the research from the field of nutritional immunology, and we then investigate how factors such as intracellular and extracellular symbionts, sociality and transgenerational effects may interact with the connection between nutrition and immunity. We show that the interactions between nutrition and resistance can be highly specific to insect species and/or infection type – this is almost certainly due to the diversity of insect social interactions and life cycles, and the varied environments in which insects live. Hence, these connections cannot be easily generalised across insects. We finally suggest that other environmental aspects – such as the use of agrochemicals and climatic factors – might also influence the interaction between nutrition and resistance, and highlight how research on these is essential

The transition from diet to blood: Exploring homeostasis in the insect haemolymph nutrient pool

Nutrition is vital to health, but while the link between diet and body nutritional composition is well explored in humans and other vertebrates, this information is not well understood in insects, despite the vital roles they play in ecosystems, and their increasing use as experimental models. Here we used Nutritional Geometry to explore the rapid physiological response to ingested nutrients in the haemolymph nutritional profile of Spodoptera littoralis caterpillars. We ask whether blood nutrients are maintained homeostatically in the face of variable nutritional intake, or if regulation is more flexible for some nutrients than others (allostasis), which allows animals to adapt to stress by responding in a way that prioritises efficiency of responses in the face of trade‐offs. Caterpillars were placed on 1 of 20 diets, systematically varying in their nutrient ratios (protein: carbohydrate) and density (calorie content), and their consumption was measured. After 48 h, caterpillars were bled, and the macronutrient (protein, carbohydrates and lipids) and nutrient metabolite (amino acids and simple sugars) content of the haemolymph was measured. Proteins comprised 93% of the haemolymph macronutrient pool on average and their concentration increased with protein eaten. The amino acid (AA) pool was dominated by five AAs, and the total pool increased with total nutrient intake. However, the ratio of essential to non‐essential AAs increased as the proportion of protein consumed increased. Carbohydrates were tightly controlled, increasing only on the most extreme carbohydrate intakes. Simple sugars were dominated by glucose and trehalose, and overall, the simple sugar pool showed high levels of homeostasis. Rather than strict homeostasis of blood nutritional properties, an allostatic model seemed to be a better fit for blood nutrient regulation in this generalist herbivore. This flexibility in response to the nutritional composition of the diet may, in part, explain how this species has evolved to extreme dietary generalism and may play a role in its worldwide pest status. Given the range of fitness‐related processes affected by the haemolymph, future studies should examine the physiological impacts of blood nutrient variation on reproduction, growth and response to infection and the trade‐offs between them

Macronutrients modulate survival to infection and immunity in Drosophila

1. Immunity and nutrition are two essential modulators of individual fitness. However, while the implications of immune function and nutrition on an individual’s lifespan and reproduction are well established, the interplay between feeding behaviour, infection, and immune function, remains poorly understood. Asking how ecological and physiological factors affect immune responses and resistance to infections is a central theme of eco-immunology. 2. In this study, we used the fruit fly, Drosophila melanogaster, to investigate how infection through septic injury modulates nutritional intake, and how macronutrient balance affects survival to infection by the pathogenic Grampositive bacterium Micrococcus luteus. 3. Our results show that infected flies maintain carbohydrate intake, but reduce protein intake, thereby shifting from a protein-to-carbohydrate (P:C) ratio of ~1:4 to ~1:10 relative to non-infected and sham-infected flies. Strikingly, the proportion of flies dying after M. luteus infection was significantly lower when flies were fed a low-P high-C diet, revealing that flies shift their macronutrient intake as means of nutritional self-medication against bacterial infection. 4. These results are likely due to the effects of the macronutrient balance on the regulation of the constitutive expression of innate immune genes, as a low-P high-C diet was linked to an up-regulation in the expression of key antimicrobial peptides. 5. Together, our results reveal the intricate relationship between macronutrient intake and resistance to infection, and integrate the molecular cross-talk between metabolic and immune pathways into the framework of nutritional immunology

No evidence of a cleaning mutualism between burying beetles and their phoretic mites.

Burying beetles (Nicrophorus vespilloides) breed on small vertebrate carcasses, which they shave and smear with antimicrobial exudates. Producing antimicrobials imposes a fitness cost on burying beetles, which rises with the potency of the antimicrobial defence. Burying beetles also carry phoretic mites (Poecilochirus carabi complex), which breed alongside them on the carcass. Here we test the novel hypothesis that P. carabi mites assist burying beetles in clearing the carcass of bacteria as a side-effect of grazing on the carrion. We manipulated the bacterial environment on carcasses and measured the effect on the beetle in the presence and absence of mites. With next-generation sequencing, we investigated how mites influence the bacterial communities on the carcass. We show that mites: 1) cause beetles to reduce the antibacterial activity of their exudates but 2) there are no consistent fitness benefits of breeding alongside mites. We also find that mites increase bacterial diversity and richness on the carcass, but do not reduce bacterial abundance. The current evidence does not support a cleaning mutualism between burying beetles and P. carabi mites, but more work is needed to understand the functional significance and fitness consequences for the beetle of mite-associated changes to the bacterial community on the carcass