Silencing the expression of the salivary sheath protein causes transgenerational feeding suppression in the aphid Sitobion avenae

Aphids produce gel saliva during feeding which forms a sheath around the stylet as it penetrates through the apoplast. The sheath is required for the sustained ingestion of phloem sap from sieve elements and is thought to form when the structural sheath protein (SHP) is cross‐linked by intermolecular disulphide bridges. We investigated the possibility of controlling aphid infestation by host‐induced gene silencing (HIGS) targeting shp expression in the grain aphid Sitobion avenae. When aphids were fed on transgenic barley expressing shp double‐stranded RNA (shp‐dsRNA), they produced significantly lower levels of shp mRNA compared to aphids feeding on wild‐type plants, suggesting that the transfer of inhibitory RNA from the plant to the insect was successful. shp expression remained low when aphids were transferred from transgenic plants and fed for 1 or 2 weeks, respectively, on wild‐type plants, confirming that silencing had a prolonged impact. Reduced shp expression correlated with a decline in growth, reproduction and survival rates. Remarkably, morphological and physiological aberrations such as winged adults and delayed maturation were maintained over seven aphid generations feeding on wild‐type plants. Targeting shp expression therefore appears to cause strong transgenerational effects on feeding, development and survival in S. avenae, suggesting that the HIGS technology has a realistic potential for the control of aphid pests in agriculture.     

The effect of starvation and subsequent feeding on the reproductive potential of the grain aphid,Sitobion avenae

The short‐term starvation tolerance of alate and apterous morphs and the effect of periods of starvation on the longevity and fecundity of alate adults were evaluated in the grain aphid, Sitobion avenae (Fabricius) (Hemiptera: Aphididae). Alate adults exhibited a proportionally larger length of survival compared with apterous adults under continuous starvation conditions. Newly molted pre‐reproductive adults were starved for 0–96 h and their survival rate on the 1st day after recovering with food was not significantly different from that of control aphids. Starvation reduced lifetime fecundity, but increased the reproductive rate immediately after nutrition being improved. Fecundity and longevity after 24, 48, 72, and 96 h of starvation were significantly higher than after 120 or 144 h of starvation. However, no significant differences were observed for alate adults after 24, 48, 72, or 96 h of starvation. This study suggests that the ability of alatae to adapt to brief periods of starvation could be one of the important factors affecting the reproductive success of aphids during delays in locating host plants.     

Bio-fertilizers and micronutrients affect the digestibility,detoxification, and intermediary metabolisms of English grain aphid,Sitobion avenae,in greenhouse

The English grain aphid, Sitobion avenae (Fabricius) (Hemiptera: Aphididae), is one of the most serious pests of cereals as the transmitter of viral diseases, mainly in wheat, Triticum aestivum. This agricultural pest is controlled with chemical insecticides, which is environmental pollutants and toxic for human. This study evaluated the potential of alternative environmentally friendly compounds to control this insect pest. The activities of digestive, antioxidants, and intermediary metabolism enzymes of S. avenae reared on wheat plants treated with bio-fertilizers (Biofarm and Probio96) and micronutrients (Librel Zinc and α-Iron) in the greenhouse were evaluated. The results reveal that α-amylase, total protease, trypsin, chymotrypsin, amino- and carboxypeptidases, alanine- and aspartate- aminotransferases, and acid phosphatase enzymes had lower activities in S. avenae reared on Biofarm treated plants compared to control. On the other hand, aphids reared on treated plants with Biofarm had the highest activities of antioxidant enzymes superoxide dismutase, catalase, peroxidase, and ascorbate oxidase, γ- glutamyl transferase, as well as lactate dehydrogenase. Moreover, the oxidized/reduced thiols ratio and malondialdehyde indicated higher activity in the aphids reared on Biofarm-treated plants than control. These results suggest that the bio-fertilizer Biofarm may compromise the physiology of S. avenae as a potential alternative toll in the integrated pest management of this aphid.     

Development and use of a monoclonal antibody to detect semi-digested proteins of the English grain aphid, Sitobion avenae, in the guts of ladybird beetle predators

A monoclonal antibody (McAb), EGA-4A9, was developed to detect the semi-digested proteins of the English grain aphid, Sitobion avenae (Fabricius) (Hemiptera: Aphididae), in predatory ladybird beetles (species of the genera Adonia , Coccinella , Hippodamia , and Propylea ) using the gut homogenate of Adonia variegata (Goeze) (Coleoptera: Coccinellidae) adults which had fed on S. avenae as immunogen. The McAb was selected by screening hybridoma lines for antibodies that bound with the semi-digested aphid proteins in ladybirds. A double antibody sandwich enzyme-linked immuno-sorbent assay (ELISA) using Clonotyping^TM System/HRP showed that it belonged to the IgG2a isotype. It did not cross-react with any of the 21 arthropod species tested besides the ladybird beetles fed on S. avenae with an indirect ELISA. It could still detect the semi-digested proteins in the gut of a ladybird adult, kept at 25 °C, that had ingested one aphid 6 days before. The extended antigen detection period and the high specificity of the antibody indicated that EGA-4A9 could be used to study interactions between English grain aphids and their ladybird predators in the field. Between 28 and 72% of coccinellids collected from the field were positive for English grain aphid protein by ELISA. The percentage of McAb-positive predatory ladybird beetles was positively correlated with the density of S. avenae in wheat fields.     

The effect of past natural enemy activity on host‐plant preference of two aphid species

The selection of a host of high nutritional quality is of great importance to the development of offspring of larvipositing aphids, as is the avoidance of natural enemies. Little is known, however, about their ability to select host plants based on these factors. This article tests the preference of aphids Sitobion avenae (Fabricius) and Rhopalosiphum padi (L.) (both Hemiptera: Aphididae) for different winter wheat cultivars, Triticum aestivum (L.) (Poaceae), and their ability to detect and avoid predators in sacrifice of their most preferred host. In both species a preference was observed for nutritionally superior hosts. The preference of both species then exhibited a change towards a nutritionally inferior host after infestations of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), that had been consuming conspecific aphids. This investigation opens the door to the interesting prospect of the ability of aphids to make complex decisions regarding a compromise between high‐quality nutrition and avoidance of predation.     

Olfactory responses of Rhopalosiphum padi to three maize,potato, and wheat cultivars and the selection of prospective crop border plants

Understanding host plant volatile – aphid interactions can facilitate the selection of crop border plants as a strategy to reduce plant virus incidence in crops. Crop border plant species with attractive odours could be used to attract aphids into the border crop and away from the main crop. As different cultivars of the same crop can vary in their olfactory attractiveness to aphids, selecting an attractive cultivar as a border crop is important to increase aphid landing rates. This study evaluated olfactory responses of the bird cherry‐oat aphid, Rhopalosiphum padi (L.) (Hemiptera: Aphididae), to three cultivars each of maize [Zea mays L. (Poaceae)], potato [Solanum tuberosum L. (Solanaceae)], and wheat [Triticum aestivum L. (Poaceae)] with the aim of selecting an attractive crop border plant to reduce the incidence of the non‐persistent Potato virus Y [PVY (Potyviridae)] in seed potatoes. Volatiles emitted by the crop cultivars were collected and identified using coupled gas chromatography/mass spectrometry. Quantitative and qualitative differences were found among cultivars. Behavioural responses of alate R. padi to odours of the cultivars and synthetic compounds identified from the plants were determined with a four‐arm olfactometer. Rhopalosiphum padi was attracted to odours emitted from maize cultivar 6Q‐121, but did not respond to odours from the remaining eight crop cultivars. Volatile compounds from maize and wheat cultivars that elicited a behavioural response from R. padi and contributed to differences in plant volatile profiles included (Z)‐3‐hexenyl acetate (attractant) and α‐farnesene, (E)‐2‐hexenal, indole, and (3E,7E)‐4,8,12‐trimethyltrideca‐1,3,7,11‐tetraene (TMTT) (repellents). We conclude that maize cv. 6Q‐121 is potentially suitable as a crop border plant based on the behavioural response of R. padi to the olfactory cues emitted by this cultivar. The findings provide insight into selecting crop cultivars capable of attracting R. padi to crop border plants.     

Feeding behaviour and performance of different populations of the black currant‐lettuce aphid,Nasonovia ribisnigri,on resistant and susceptible lettuce

When crops are bred for resistance to herbivores, these herbivores are under strong selection pressure to overcome this resistance, which may result in the emergence of virulent biotypes. This is a growing problem for crop species attacked by aphids. The Nr‐gene in lettuce confers near‐complete resistance against the black currant‐lettuce aphid, Nasonovia ribisnigri (Mosely) (Hemiptera: Aphididae). Since 2007, populations of N. ribisnigri have been reported in several locations in Europe to infest resistant lettuce varieties that possess the Nr‐gene. The objective of this study was to analyse the behaviour and level of virulence of several N. ribisnigri populations observed to have colonized Nr‐locus‐containing lettuce lines. We analysed the stylet penetration and feeding behaviour, and the performance of these N. ribisnigri populations on resistant and susceptible lettuce lines. Large variation in the degree of virulence to the Nr‐locus‐containing lettuce lines was found among populations of the Nr:1 biotype. The German population was highly virulent on the Nr‐containing resistant lettuce lines, and showed similar feeding behaviour and performance on both the susceptible and resistant lettuces. The French population from Paris was the second most virulent, though reproduction on the resistant lines was reduced. The French population from Perpignan and a population from Belgium, however, showed reduced performance and feeding rate on the resistant compared to the susceptible lettuces. The lettuce background in which the Nr‐gene is expressed influences the level of resistance to the various Nr:1 aphid populations, because the performance and feeding behaviour differed between the aphids on the cultivars (romaine lettuce) compared to the near‐isogenic lines (butterhead/iceberg lettuce). This study also shows that being able to feed on a plant not automatically implies that a population can successfully develop on that plant, because aphids showed phloem ingestion during the 8‐h recording period on resistant lettuce, but were not able to survive and reproduce on the same lettuce line.     

Winter wheat (Triticum aestivum) response to Barley yellow dwarf virus at various nitrogen application rates in the presence and absence of its aphid vector,Rhopalosiphum padi

Barley yellow dwarf (BYD) is one of the most common diseases of cereal crops, caused by the phloem‐limited, cereal aphid‐borne Barley yellow dwarf virus (BYDV) (Luteoviridae). Delayed planting and controlling aphid vector numbers with insecticides have been the primary approaches to manage BYD. There is limited research on nitrogen (N) application effects on plant growth, N status, and water use in the BYDV pathosystem in the absence of aphid control. Such information will be essential in developing a post‐infection management plan for BYDV‐infected cereals. Through a greenhouse study, we assessed whether manipulation of N supply to BYDV‐infected winter wheat, Triticum aestivum L. (Poaceae), in the presence or absence of the aphid vector Rhopalosiphum padi L. (Hemiptera: Aphididae), could improve N and/or water uptake, and subsequently promote plant growth. Similar responses of shoot biomass and of water and N use efficiencies to various N application rates were observed in both BYDV‐infected and non‐infected plants, suggesting that winter wheat plants with only BYDV infection may be capable of outgrowing infection by the virus. Plants, which simultaneously hosted aphids and BYDV, suffered more severe symptoms and possessed higher virus loads than those infected with BYDV only. Moreover, in plants hosting both BYDV and aphids, aphid pressure was positively associated with N concentration within plant tissue, suggesting that N application and N concentration within foliar tissue may alter BYDV replication indirectly through their influence on aphid reproduction. Even though shoot biomass, tissue N concentration, and water use efficiency increased in response to increased N application, decision‐making on N fertilization to plants hosting both BYDV and aphids should take into consideration the potential of aphid outbreak and/or the possibility of reduced plant resilience to environmental stresses due to decreased root growth.     

Recursive adaptation in action: allochronic isolation and divergence of host-associated populations of the apple maggot fly,Rhagoletis pomonella,following its recent introduction to the western USA

An outstanding issue in the study of insect host races concerns the idea of ‘recursive adaptive divergence’, whereby adaptation can occur repeatedly across space and/or time, and the most recent adaptive episode is defined by one or more previously similar cases. The host plant shift of the apple maggot fly, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae, Carpomyini), from ancestral downy hawthorn [Crataegus mollis (Torr. & A. Gray) Scheele] to introduced, domesticated apple (Malus domestica Borkh.) in the eastern USA has long served as a model system for investigating ecologically driven host race formation in phytophagous insect specialists. Here, we report results from an annual geography survey of eclosion time demonstrating a similar ecological pattern among nascent host-associated populations of the fly recently introduced ca. 40 years ago from its native range in the east into the Pacific Northwest (PNW) region of the USA. Specifically, using data collected from 25 locations across 5 years, we show that apple-infesting fly populations in the PNW have rapidly and repeatedly shifted (and maintained differences in) their adult eclosion life-history timing to infest two novel hawthorn hosts with different fruiting phenologies – a native species (Crataegus douglasii Lindl.) and an introduced species (Crataegus monogyna Jacq.) – generating partial allochronic reproductive isolation in the process. The shifts in the PNW parallel the classic case of host race formation in the eastern USA, but have occurred bi-directionally to two hawthorn species with phenologies slightly earlier (black hawthorn) and significantly later (ornamental hawthorn) than apple. Our results imply that R. pomonella can both possess and retain extensive-standing variation (i.e., ‘adaptive memory’) in diapause traits, even following introductions, to rapidly and temporally track novel phenological host opportunities when they arise. Thus, ‘specialized’ host races may not constitute evolutionary dead ends. Rather, adaptive phenotypic and genetic memory may carry over from one host shift to the next, recursively facilitating host race formation in phytophagous insects.