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Leybourne, D. J.

Publications and source records attributed to Leybourne, D. J..

10 recordsLinked to original sources

Top-down and bottom-up landscape processes influence the formation of microbial partnerships in herbivorous insects

Many insects form intimate associations with microbial partners, spanning a continuum from obligate mutualisms to transient associations. These microbial partners confer a range of functional benefits, including protection from natural enemies, detoxification of plant secondary metabolites, and improved fitness. The prevalence and abundance of microbial symbionts can vary between insect populations, indicating that the insect-microbe relationship is influenced by external factors. However, little is known on the factors that determine the assembly, structure, and composition of the microbiome of herbivorous insects. We posit that the factors influencing the insect-microbe relationship occur at the landscape-scale, acting through a combination of bottom-up, top-down, and indirect effects between plants, herbivores, and their natural enemies. We test this in two agro-ecosystems by sampling individual insects from three sap-feeding and one leaf-chewing species. Our results explicitly show for the first time that habitat configurational complexity and the proportion of host-plant crop in the landscape, combined with natural enemy abundance, can act as direct and indirect drivers of microbial symbiosis in herbivorous insects. This highlights the wider implications landscape habitat and ecosystem structure has on species interactions across managed agricultural landscapes.

ecology↗

A modelling framework to estimate vector dispersal and disease spread in an important agricultural pathosystem

Cereals are some of the most agriculturally important crops grown worldwide. Cereal aphids are small sap-feeding insects that infest cereals and vector devastating cereal pathogens, principally the yellow dwarf viruses, with severe infection reducing yields by 20 - 80%. Currently, farmers are advised to apply insecticide if a single cereal aphid is found within the crop. However, this is an oversimplification of the biology and ecology of the vector-virus system: Each aphid species can transmit a range of yellow dwarf virus species with variable efficiency, and intra-species diversity within a vector species (genotype) can influence this further. Accounting for this variation in decision-making processes has the potential to help with developing bespoke management options based on the composition of the local vector-virus population, and represents a novel avenue that could be explored to develop more sustainable management strategies. Here we describe a stage-structured model that can estimate vector dispersal and disease spread. We use data for the two main cereal aphid species and the two yellow dwarf virus species of greatest concern in Europe to examine how diversity at each level of the vector-virus system impacts disease spread. More broadly, our modelling framework represents a tool that can be used to explore vector-virus-host interactions in greater detail, and we use cereal systems as a case study. Our modelling scenarios highlight diversity at each scale as an important factor. We show that the two main vector species have contrasting dispersal patterns, and that this interacts with virus transmission efficacy to influence disease spread; genetic variation within a vector population is a key driver behind disease spread and disease risk; and for vector species that transmit multiple virus species, the specific vector-virus species combination is a key risk factor to consider.

ecology↗

Genetic diversity in vector populations influences the transmission efficiency of an important plant virus

The transmission efficiency of aphid-vectored plant viruses can differ between aphid populations. Intra-species diversity (genetic variation, endosymbionts) is a key determinant of aphid phenotype; however, the extent of which intra-species diversity contributes towards variation in virus transmission efficiency is unclear. Here, we use multiple populations of two key aphid species that vector barley yellow dwarf virus (BYDV) strain PAV (BYDV-PAV), the grain aphid (Sitobion avenae) and the bird cherry-oat aphid (Rhopalosiphum padi), and examine how diversity in vector populations influences virus transmission efficiency. We use Illumina sequencing to characterise genetic and endosymbiont variation in multiple S. avenae and R. padi populations and conduct BYDV-PAV transmission experiments to identify links between intra-species diversity in the vector and virus transmission efficiency. We observe limited variation in the transmission efficiency of S. avenae, with transmission efficiency consistently low for this species. However, for R. padi we observe a range of transmission efficiency and show that BYDV transmission efficiency is influenced by genetic diversity within the vector, identifying 542 SNPs that potentially contribute towards variable transmission efficiency in R. padi. Our results represent an important advancement in our understanding of the relationship between genetic diversity, vector-virus interactions, and virus transmission efficiency.

pathology↗

Common facultative endosymbionts do not influence sensitivity of cereal aphids to pyrethroids

O_LICereal aphids, including the bird cherry-oat aphid, Rhopalosiphum padi, and the grain aphid, Sitobion avenae, can transmit viruses that significantly reduce crop yields. To mitigate against yield losses, insecticides are routinely used to manage aphid populations. C_LIO_LIAphids can form relationships with endosymbionts that confer fitness benefits or consequences to the aphid. Recent artificial inoculation experiments indicate that endosymbionts could increase aphid susceptibility to insecticides, but this has not been explored using aphid populations naturally infected with endosymbionts. C_LIO_LIHere, we sampled aphids from an important cereal production region in Lower Saxony, Germany. We characterised the endosymbiont profile of these aphid populations and conducted pyrethroid dose-response assays to test the hypothesis that facultative endosymbionts increase aphid susceptibility to insecticides. C_LIO_LIWe find that the level of insecticide susceptibility is highly variable in S. avenae and we identify populations that are sensitive and tolerant to pyrethroids, including populations collected from the same field. For R. padi, we find evidence for decreased sensitivity to pyrethroids, representing the first report of reduced sensitivity to pyrethroids in R. padi sampled from Central Europe. C_LIO_LIWe detected high endosymbiont infection frequencies in the aphid populations. 84% of aphids carry one facultative endosymbiont and 9% of aphids carry two facultative endosymbionts. We detected associations with Regiella insecticola, Fukatsia symbiotica, and Hamiltonella defensa. However, we do not identify a link between endosymbiont infection and insecticide susceptibility, indicating that other factors may govern the development of insecticide resistance and the need for alternative management strategies. C_LI

zoology↗

Common resistance mechanisms are deployed by plants against sap-feeding herbivorous insects: insights from a meta-analysis and systematic review

Sap-feeding insects cause significant yield losses to the worlds crops, these insects feed using syringe-like mouthparts and electrophysiology can be used to compare feeding behaviour on susceptible and resistant plants to identify the mechanistic processes behind resistant phenotypes. Data extracted from 129 studies, comprising 41 insect species across eight insect taxa and 12 host-plant families representing over 30 species, demonstrates that mechanisms deployed by resistant plants have common consequences on the feeding behaviour of diverse insect groups. We show that insects feeding on resistant plants take longer to establish a feeding site and have their feeding duration suppressed two-fold compared with insects feeding on susceptible plants. Our results reveal that the underlying traits contributing towards resistant phenotypes are conserved across plant families, deployed against taxonomically diverse insect groups, and that the underlying resistance mechanisms are conserved. These findings provide new insight that will be beneficial when developing future crop varieties.

zoology↗

Development of a pest threshold decision support system for minimising damage to winter wheat from wheat bulb fly, Delia coarctata

Graphical AbstractIn this article we describe two predictive models that can be used for the integrated management of wheat bulb fly. Our first model is a pest level prediction model and our second model predicts the number of shoots a winter wheat crop will achieve by the terminal spikelet developmental stage. We revise and update current wheat bulb fly damage thresholds and combine this with our two models to devise a tolerance-based decision support system that can be used to minimise the risk of crop damage by wheat bulb fly. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=152 SRC="FIGDIR/small/435242v1_ufig1.gif" ALT="Figure 1"> View larger version (37K): org.highwire.dtl.DTLVardef@ee5b9aorg.highwire.dtl.DTLVardef@c0197corg.highwire.dtl.DTLVardef@1c9519eorg.highwire.dtl.DTLVardef@d6a52_HPS_FORMAT_FIGEXP M_FIG C_FIG SummaryWheat bulb fly, Delia coarctata, is an important pest of winter wheat in the UK, causing significant damage of up to 4 t ha-1. Accepted population thresholds for D. coarctata are 250 eggs m-2 for crops sown up to the end of October and 100 eggs m-2 for crops sown from November. Fields with populations of D. coarctata that exceed the thresholds are at higher risk of experiencing economically damaging pest infestations. In the UK, recent withdrawal of insecticides means that only a seed treatment is available for chemical control of D. coarctata, however this is only effective for late-sown crops (November onwards) and accurate estimations of annual population levels are required to ensure a seed treatment is applied if needed. As a result of the lack of post-drilling control strategies, the management of D. coarctata is becoming increasingly reliant on non-chemical methods of control. Control strategies that are effective in managing similar stem-boring pests of wheat include sowing earlier and using higher seed rates to produce crops with more shoots and greater tolerance to shoot damage. In this study we develop two predictive models that can be used for integrated D. coarctata management. The first is an updated pest level prediction model that predicts D. coarctata populations from meteorological parameters with a predictive accuracy of 70%, which represents a significant improvement on the previous D. coarctata population prediction model. Our second model predicts the maximum number of shoots for a winter wheat crop that would be expected at the terminal spikelet development stage. This shoot number model uses information about the thermal time from plant emergence to terminal spikelet, leaf phyllochron length, plant population, and sowing date to predict the degree of tolerance a crop will have against D. coarctata. The shoot number model was calibrated against data collected from five field experiments and tested against data from four experiments. Model testing demonstrated that the shoot number model has a predictive accuracy of 70%. A decision support system using these two models for the sustainable management of D. coarcata risk is described.

plant biology↗

Stressful times in a climate crisis: how will aphids respond to more frequent drought?

AimAphids are abundant in natural and managed vegetation, supporting a diverse community of organisms and causing damage to agricultural crops. Using a meta-analysis approach, we aimed to advance understanding of how increased drought incidence will affect this ecologically and economically important insect group, and to characterise the underlying mechanisms. LocationGlobal. Time period1958-2020. Major taxa studiedAphids. MethodsWe used qualitative and quantitative synthesis techniques to determine whether drought stress has a negative, positive, or null effect on aphid fitness. We examined these effects in relation to 1) aphid biology, 2) the aphid-plant. species combination. We compiled two datasets: 1) a "global" dataset (n = 55 from 55 published studies) comprising one pooled effect size per study, and 2) an "expanded" dataset (n = 93) containing multiple datapoints per study, separated into different measures of aphid fitness but pooled across aphid-plant combinations. Where reported, we extracted data on the effect of drought on plant vigour, and plant tissue concentrations of nutrients and defensive compounds, to capture the potential causes of aphid responses. ResultsAcross all studies ("global" dataset), drought stress had a negative effect on aphid fitness: Hedges g = -0.57; 95% confidence interval (CI95) = {+/-}0.31. The "expanded" dataset indicated that, on average, drought stress reduced aphid fecundity (g = - 0.98; CI95 = {+/-}0.50) and increased development time (g = 1.13; CI95 = {+/-}1.02). Furthermore, drought stress had a negative impact on plant vigour (g = -7.06; CI95 = {+/-}2.86) and increased plant concentrations of defensive chemicals (g = 3.14; CI95 = {+/-}3.14). Main conclusionsAphid fitness is typically reduced under drought, associated with reduced plant vigour and increased chemical defence in drought-stressed plants. We propose a conceptual model to predict drought effects on aphid fitness in relation to plant vigour and defence.

ecology↗

A fitness cost resulting from Hamiltonella defensa infection is associated with altered probing and feeding behaviour in Rhopalosiphum padi

Aphids frequently associate with facultative endosymbiotic bacteria which influence aphid physiology in myriad ways. Endosymbiont infection can increase aphid resistance against parasitoids and pathogens, modulate plant responses to aphid feeding, and promote aphid virulence. These endosymbiotic relationships can also decrease aphid fitness in the absence of natural enemies or when feeding on less suitable plant types. Here, we use the Electrical Penetration Graph (EPG) technique to monitor feeding behaviour of four genetically-similar clonal lines of a cereal-feeding aphid, Rhopalosiphum padi, differentially infected (+/-) with the facultative protective endosymbiont, Hamiltonella defensa, to understand how physiological processes at the aphid-plant interface are affected by endosymbiont infection. Endosymbiont-infected aphids exhibited altered probing and feeding patterns compared with uninfected aphids, characterised by a two-fold increase in the number of plant cell punctures, a 50% reduction in the duration of each cellular puncture, and a greater probability of achieving sustained ingestion of plant phloem. Feeding behaviour was altered further by host plant identity: endosymbiont-infected aphids spent less time probing into plant tissue, required twice as many probes into plant tissue to reach plant phloem, and showed a 44% reduction in phloem ingestion when feeding on the partially-resistant wild relative of barley, Hordeum spontaneum 5, compared with a commercial barley cultivar. These observations might explain reduced growth of H. defensa-infected aphids on the former host plant. This study is the first to demonstrate a physiological mechanism at the aphid-plant interface contributing to endosymbiont effects on aphid fitness on different quality plants through altered aphid feeding behaviour.\n\nSummaryReduced performance of aphids infected with a common facultative endosymbiont on poor quality plants may be explained by changes in aphid probing behaviour and decreased phloem sap ingestion.

physiology↗

Partial-resistance against aphids in wild barley reduces the oviposition success of the generalist parasitoid, Aphidius colemani

Aphids are significant agricultural pests of cereal crops with a worldwide distribution. The control of aphids in agricultural systems is currently heavily reliant on insecticidal compounds, but it is becoming increasingly apparent that chemical-based control of agricultural pests has far-reaching unintended consequences on agro-ecosystems. As a result, more sustainable means of aphid control are becoming increasingly desirable. Potential options include increasing plant resistance against aphids, promoting biocontrol, and the combined use of both strategies. When used together it is important to understand how, and to what extent, increased plant resistance against aphids affects the success of biocontrol agents. In this current study, we examine how partial-resistance against cereal aphids in a wild relative of barley, Hordeum spontaneum 5 (Hsp5), affects the success of the common parasitoid of cereal aphids, Aphidius colemani. We show that the parasitism success of A. colemani attacking nymphs of the bird cherry-oat aphid, Rhopalosiphum padi, contained on Hsp5 is reduced compared with the parasitism success of wasps attacking R. padi nymphs feeding on a susceptible modern cultivar of barley, H. vulgare cv. Concerto. Explanta parasitism assays showed that the in parasitoid success is a direct effect of the plant environment (such as differential architectural traits), rather than an indirect effect dur to a decrease in aphid suitability resulting from increased resistance against aphids in Hsp5. Our study highlights the importance of understanding the direct and indirect effects of plant resistance against aphids on biocontrol strategies.

plant biology↗

Partial-resistance against aphids in wild barley involves phloem and mesophyll-based defences

Aphids, including the bird cherry-oat aphid (Rhopalosiphum padi), are significant agricultural pests. Aphid populations are typically controlled using insecticides, but there is increasing demand for more sustainable pest management practices. The wild relative of barley, Hordeum spontaneum 5 (Hsp5) has been described as partially-resistant to R. padi. Partial-resistance is proposed to involve higher thionin and lipoxygenase gene expression. However, the underlying mechanistic processes are unknown. In this study we compared Hsp5 with a susceptible cultivar of barley (Concerto) to test the extent to which partial-resistance affects aphid fitness. We used the electrical penetration graph technique to monitor R. padi feeding patterns to elucidate the tissue location of partial-resistance factors alongside molecular and biochemical analyses to identify potential mechanisms. We show that partial-resistance in Hsp5 extends to three aphid species and is mediated by phloem/mesophyll-based factors, leading to a three-fold increase in the time aphids take to establish sustained phloem ingestion. Partial-resistance likely involves elevated expression of defence and phytohormone genes alongside altered phloem amino acid composition. Further work is required to establish the function of these traits, however this study highlights plant tissues which are important in conferring broad-spectrum partial-resistance against aphids in barley.\n\nHighlightPartial-resistance against aphids in wild barley is based in the mesophyll and vascular tissue and is potentially associated with higher basal defence gene expression and altered phloem amino acid composition.

plant biology↗