Cover Caption

Host alternation has significant consequences for the diversification and success of the superfamily of aphids. We explored the underlying molecular mechanism through a large‐scale gene expression analysis on the mealy aphid Hyalopterus persikonus, a worldwide pest to stone fruits, collected from its winter and summer host plants. More than four times as many unigenes of the mealy aphid were significantly upregulated on summer host. Putative salivary gland expressed genes and genes encoding secretory proteins were given special attentions (see pages 431–442). Photo provided by Le Kang.     

Aphid specialization on different summer hosts is associated with strong genetic differentiation and unequal symbiont communities despite a common mating habitat

Specialization on different host plants can promote evolutionary diversification of herbivorous insects. Work on pea aphids (Acyrthosiphon pisum) has contributed significantly to the understanding of this process, demonstrating that populations associated with different host plants exhibit performance trade‐offs across hosts, show adaptive host choice and genetic differentiation and possess different communities of bacterial endosymbionts. Populations specialized on different secondary host plants during the parthenogenetic summer generations are also described for the black bean aphid (Aphis fabae complex) and are usually treated as different (morphologically cryptic) subspecies. In contrast to pea aphids, however, host choice and mate choice are decoupled in black bean aphids, because populations from different summer hosts return to the same primary host plant to mate and lay overwintering eggs. This could counteract evolutionary divergence, and it is currently unknown to what extent black bean aphids using different summer hosts are indeed differentiated. We addressed this question by microsatellite genotyping and endosymbiont screening of black bean aphids collected in summer from the goosefoot Chenopodium album (subspecies A. f. fabae) and from thistles of the genus Cirsium (subspecies A. f. cirsiiacanthoides) across numerous sites in Switzerland and France. Our results show clearly that aphids from Cirsium and Chenopodium exhibit strong and geographically consistent genetic differentiation and that they differ in their frequencies of infection with particular endosymbionts. The dependence on a joint winter host has thus not prevented the evolutionary divergence into summer host‐adapted populations that appear to have evolved mechanisms of reproductive isolation within a common mating habitat.     

Mitochondrial COI and morphological specificity of the mealy aphids (Hyalopterus ssp.) collected from different?hosts in Europe (Hemiptera,Aphididae)

Forty three European population samples of mealy aphids from various winter and summer host plants were attributed to respective species of Hyalopterus by means of their partial sequences of mitochondrial COI gene. Used Hyalopterus samples emerged as monophyletic relative to outgroup and formed three major clades representing three host specific mealy aphid species in the Neighbor joining, Maximum parsimony, Maximum likelihood and Bayesian inference trees. Hyalopterus pruni and Hyalopterus persikonus emerged as a sister species, whilst Hyalopterus amygdali was located basally. Samples representing different clades in the molecular trees were used for canonical discrimination analysis based on twenty two morphological characters. Length of the median dorsal head hair enabled a 97.3 % separation of Hyalopterus amygdali from the remaining two species. No single character enabled satisfactory discrimination between apterous viviparous females of Hyalopterus pruni and Hyalopterus persikonus. A modified key for the morphological identification of Hyalopterus species is suggested and their taxonomic status discussed.     

Are primary woody hosts ‘island refuges’ for host‐alternating aphids and important for colonization of local cereals?

Only few studies are available dealing with the relation between winter host density and spatial distribution and spring colonization of winter cereals by the host‐alternating cereal aphid species Rhopalosiphum padi and Metopolophium dirhodum. Large‐scale studies in climatically different agroecosystems in Germany from 2004 to 2006 revealed for R. padi and M. dirhodum larger spring/summer populations in landscapes with higher densities of winter hosts. A small‐scale study was performed in winter wheat fields adjacent to a large hedge with several typical winter hosts plants, bird cherry (Prunus padus) and wild rose species (Rosa spp.) to indentify distance effects (0–8, 8–24 and 24–60 m). Weekly measurements of aphid density between May to July showed significantly higher densities of R. padi compared with those of other aphids. Statistical analysis (Tukey–Kramer test and regression analyses) revealed significant gradients from the hedge to the field centre for R. padi and M. dirhodum. In comparative studies, winged R. padi from winter and adjacent summer hosts were genotyped using four microsatellite markers. The results showed that individuals from a certain winter host were not genetically similar with individuals from neighbouring summer hosts; it, therefore, seems that winter host clones did not significantly contribute to population built‐up in cereal fields over short distances. It could be concluded that on a regional scale, the density of sources for early migrants of R. padi is important for colonization intensity of surrounding summer hosts, but that the high local movement intensity and the relative small proportion of aphids that could be analysed in such tracking studies are blurring close spatial relations within short time periods.     

The trait and host plant ecology of aphids and their distribution and abundance in the United Kingdom

Aim We characterized the annual populations of 170 aphid species by their log abundance, site occupancy and site continuity (i.e. the persistence of species in time) and used this information to make predictions about groups of species that displayed characteristic patterns. By doing so, we aimed to identify commonalities in functional traits (host‐alternation; mode of reproduction; life‐cycle plasticity; median body size) and host plant geographic range sizes that may indicate why some species are common and others not. Location The population dynamics of winged aphids at 27 locations in the United Kingdom were studied. Methods The annual numbers of aphids were studied using a dataset comprising over 11 million individuals across 509 site‐years. Traits and host plants were analysed using linear mixed effects models and nonlinear regression models. Results Linear mixed effects models showed that the fixed effects of host alternation and winter host plant area of occupancy were important in predicting log abundance, site occupancy and site continuity. Life‐cycle plasticity was also a significant effect, although not for log abundance. Relationships between site continuity, site occupancy and log abundance were strongly nonlinear. Site continuity always lagged site occupancy, indicating that species were less likely to retain previously occupied sites when abundances were low. Main conclusions Aphid traits are a better paradigm than taxonomic relatedness in explaining macroecological patterns. Host alternation induces an annual flux of migrants that engenders higher annual log abundances, consistent with the theory that species with high local densities tend to confer a much wider distribution than those with low densities. The abundance of aphids is monotonically related to the geographic range size of their winter host, suggestive of a strong bottom‐up effect (i.e. resource controlled). The areas of occupancy (AOO) of winter host plants constrain aphids to low abundances because a greater proportion of hosts are trees and shrubs which tend to have smaller AOO than herbs and grasses, the common summer host types.     

Temporal and spatial variability of rosy apple aphid Dysaphis plantaginea populations: is there a role of the alternate host plant Plantago major?

• 1 The rosy apple aphid Dysaphis plantaginea (Passerini) (Homoptera: Aphididae) is a pest of economic importance to the apple industry worldwide, particularly in organic apple orchards where no acceptable controls are available. In the Similkameen Valley of British Columbia, Canada, the rosy apple aphid population size varies widely between orchards and between years. To explain this variation, potential environmental correlates of aphid density were evaluated. The architecture of the alternate host was also evaluated for its effect on rosy apple aphid summer survival and reproduction.
• 2 The percentage of trees infested by rosy apple aphids among orchards was in the range 8–94% for trees having at least one cluster with more than ten aphids in 2007 and in the range 0–39% in 2008.
• 3 A general linear model correlating aphid densities to the environmental variables of abundance of the alternate host (plantain Plantago spp.), foliar nitrogen, tree age and planting density, and reduced by stepwise regression, indicated that foliar nitrogen and tree age explained 33% of the variation. Abundance of the summer, alternate food plant, plantain, was not related to later aphid densities on apple trees.
• 4 Plantain architecture, however, influenced aphid numbers and 25‐fold more aphids were found on low‐lying plantain leaves than on more upright leaves. Experimental manipulation of leaf angle and leaf size showed that significantly more aphids occurred on low angle, large leaves. Finally, mowing that encouraged low lying plants prior to spring aphid migration was associated with a four‐fold greater number of both winged and wingless aphids on the plantain.

     

A potent, morph-specific parturition stimulant in the overwintering host plant of the black bean aphid, Aphis fabae

Abstract. The black bean aphid, Aphis fabae Scopoli, has a host‐alternating life cycle. Winged female autumn migrants (gynoparae) develop on numerous summer host plants but as adults will only colonize the winter host (spindle, Euonymus europaeus L.). When stylet activities of gynoparae were electrically recorded during access to a spindle leaf, the insects spent the majority (75%) of the 6‐h experimental period penetrating the plant surface and a large proportion of it (44%) ingesting from either phloem or xylem vessels. Most (95%) gynoparae initiated reproduction on spindle, producing 4.15 ± 0.59 offspring per adult by the end of the experiment (mean ± SEM). By contrast, gynoparae placed on a seedling of their natal, summer host (broad bean, Vicia faba L.) penetrated the plant for only 39% of the available time, rarely ingested plant sap and never reproduced. The number of nymphs deposited on spindle leaves was not correlated with the occurrence or duration of ingestion from vascular tissues, suggesting that parturition stimulants are detected before feeding, probably during penetration of nonvascular cells. Presentation of an aqueous spindle extract to the aphids in artificial feeding chambers showed that water‐soluble spindle factors evoke stimulation of parturition by gynoparae in 72‐h bioassays. The stimulant was extremely potent, remaining active until the total extracted material was diluted to less than 10 p.p.m. Stylet activities and reproductive responses were also evaluated for summer winged females (alate virginoparae), which have a broad host range, and will colonize both bean and spindle under laboratory conditions. On both of these plant species, virginoparae often ingested plant sap and deposited nymphs during the 6‐h electrical recording experiment (producing 4.60 ± 0.48 offspring on bean; 2.70 ± 0.35 on spindle: mean ± SEM), but no significant correlations were found between reproduction and the occurrence or duration of particular stylet activities. Aqueous host‐plant extracts had no effect on the numbers of offspring deposited by virginoparae in artificial feeding chambers, showing that this form of the aphid is not responsive to the spindle‐derived parturition stimulant. The results highlight the need for more information on the factors determining host acceptance and parturition by polyphagous aphid phenotypes.     

Proteins Identified from Saliva and Salivary Glands of the Chinese Gall Aphid Schlechtendalia chinensis

Aphid saliva plays an essential role in the interaction between aphids and their host plants. Several aphid salivary proteins have been identified but none from galling aphids. Here the salivary proteins from the Chinese gall aphid are analyzed, Schlechtendalia chinensis, via an LC‐MS/MS analysis. A total of 31 proteins are identified directly from saliva collected via an artificial diet, and 141 proteins are identified from extracts derived from dissected salivary glands. Among these identified proteins, 17 are found in both collected saliva and dissected salivary glands. In comparison with salivary proteins from ten other free‐living Hemipterans, the most striking feature of the salivary protein from S. chinensis is the existence of high proportion of proteins with binding activity, including DNA‐, protein‐, ATP‐, and iron‐binding proteins. These proteins maybe involved in gall formation. These results provide a framework for future research to elucidate the molecular basis for gall induction by galling aphids.     

Food web structure of aphids and their parasitoids in Belgian fruit agroecosystems

Community structures of aphids and their parasitoids were studied in fruit crop habitats of eastern Belgium in 2014 and 2015. Quantitative food webs of these insects were constructed separately for each year, and divided into subwebs on three host‐plant categories, fruit crop plants, non‐crop woody and shrub plants and non‐crop herbaceous plants. The webs were analyzed using the standard food web statistics designed for binary data. During the whole study period, 78 plant species were recorded as host plants of 71 aphid species, from which 48 parasitoid species emerged. The community structure, aphid / parasitoid species‐richness ratio and trophic link number varied between the two years, whereas the realized connectance between parasitoids and aphids was relatively constant. A new plant–aphid–parasitoid association for Europe was recorded. Dominant parasitoid species in the study sites were Ephedrus persicae, Binodoxys angelicae and Praon volucre: the first species was frequently observed on non‐crop trees and shrubs, but the other two on non‐crop herbaceous plants. The potential influence, through indirect interactions, of parasitoids on aphid communities was assessed with quantitative parasitoid‐overlap diagrams. Symmetrical links were uncommon, and abundant aphid species seemed to have large indirect effects on less abundant species. These results show that trophic indirect interactions through parasitoids may govern aphid populations in fruit crop habitats with various non‐crop plants, implying the importance for landscape management and biological control of aphid pests in fruit agroecosystems.     

Field‐level effects of preventative management tactics on soybean aphids (Aphis glycines Matsumura) and their predators

A 2‐year field experiment was conducted in northern Illinois to evaluate the effects of host plant resistance and an insecticidal seed treatment (thiamethoxam) on soybean aphids, Aphis glycines Matsumura and their predators. Densities of soybean aphids varied between the 2 years of the experiment. During both years, resistant plants experienced fewer cumulative aphid days than susceptible plants. Populations of soybean aphids on resistant plants rarely exceeded the economic injury level of 250 soybean aphids per plant. The use of thiamethoxam reduced cumulative aphid days in 2007, but not in 2008. Although soybean aphids reached densities that were sufficient to cause yield‐loss for untreated and susceptible plants, no yield‐benefit was associated with using the two management tactics in either year. This latter finding suggests that densities of soybean aphids need to be greater and sustained for a longer period of time than what we observed if the two management tactics are expected to provide a yield‐benefit. Monitoring natural enemies revealed that densities of key aphidophagous predators were relatively unaffected by host plant resistance or thiamethoxam; the effect of these management tactics on densities of predators, as well as the effectiveness of the method used to sample predators, is discussed.     

Olfactory responses of Aphidius gifuensis to odors of host plants and aphid‐plant complexes

Abstract The olfactory responses of Aphidius gifuensis to odors from two host plants (Nicotiana tabacum and Brassica napus ssp.) and their complexes with different infestation levels of two host aphids (Myzus persicae and Lipaphis erysimi) were respectively examined in an olfactometer. The results showed that female A. gifuensis did not respond to odors of undamaged or mechanically damaged host plants, but significantly responded to odors of aphid/plant complexes. Moreover, A. gifuensis responded significantly to odors of both M. persicae and L. erysimi/plant complexes when host plants were infested by high levels of aphids, suggesting that quantity of aphid‐induced volatiles could be important for attracting A. gifuensis. When tested between aphid/plant complexes, A. gifuensis did not show its preference for either complex. The efficiency of A. gifuensis against aphids in open fields potentially could be improved by using its olfactory response to aphid/plant complexes.     

Cucurbit aphid‐borne yellows virus (CABYV) modifies the alighting,settling and probing behaviour of its vector Aphis gossypii favouring its own spread

Plant pathogens are able to influence the behaviour and fitness of their vectors in such a way that changes in plant–pathogen–vector interactions can affect their transmission. Such influence can be direct or indirect, depending on whether it is mediated by the presence of the pathogen in the vector's body or by host changes as a consequence of pathogen infection. We report the effect that the persistently aphid‐transmitted Cucurbit aphid‐borne yellows virus (CABYV, Polerovirus) can induce on the alighting, settling and probing behaviour activities of its vector, the cotton aphid Aphis gossypii. Only minor direct changes on aphid feeding behaviour were observed when viruliferous aphids fed on non‐infected plants. However, the feeding behaviour of non‐viruliferous aphids was very different on CABYV‐infected than on non‐infected plants. Non‐viruliferous aphids spent longer time feeding from the phloem in CABYV‐infected plants compared to non‐infected plants, suggesting that CABYV indirectly manipulates aphid feeding behaviour through its shared host plant in order to favour viral acquisition. Viruliferous aphids showed a clear preference for non‐infected over CABYV‐infected plants at short and long time, while such behaviour was not observed for non‐viruliferous aphids. Overall, our results indicate that CABYV induces changes in its host plant that modifies aphid feeding behaviour in a way that virus acquisition from infected plants is enhanced. Once the aphids become viruliferous they prefer to settle on healthy plants, leading to optimise the transmission and spread of this phloem‐limited virus.     

Aphid behavioral responses to virus‐infected plants are similar despite divergent fitness effects

We compared the settling preferences and reproductive potential of an oligophagous herbivore, the pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), in response to pea plants, Pisum sativum L. cv. ‘Aragorn’ (Fabaceae), infected with two persistently transmitted viruses, Pea enation mosaic virus (PEMV) and Bean leaf roll virus (BLRV), that differ in their distribution within an infected plant. Aphids preferentially oriented toward and settled on plants infected with PEMV or BLRV in comparison with sham‐inoculated plants (plants exposed to herbivory by uninfected aphids), but aphids did not discriminate between plants infected with the two viruses. Analysis of plant volatiles indicated that plants inoculated with either virus had significantly higher green leaf volatile‐to‐monoterpene ratios. Time until reproductive maturity was marginally influenced by plant infection status, with a trend toward earlier nymph production on infected plants. There were consistent age‐specific effects of plant infection status on aphid fecundity: reproduction was significantly enhanced for aphids on BLRV‐infected plants across most time intervals, though mean aphid fecundity did not differ between sham and PEMV‐infected plants. There was no clear pattern of age‐specific survivorship; however, mean aphid lifespan was reduced on plants infected with PEMV. Our results are consistent with predictions of the host manipulation hypothesis, extended to include plant viruses: non‐viruliferous A. pisum preferentially orient to virus‐infected host plants, potentially facilitating pathogen transmission. These studies extend the scope of the host manipulation hypothesis by demonstrating that divergent fitness effects on vectors arise relative to the mode of virus transmission.     

Advanced phenology of intraguild predators shifts herbivore host plant preference and performance

1. The abundance of insect herbivores is mediated by interactions with higher and lower trophic levels. This research asks (i) how phenological change across trophic levels affects host plant quality and selection for aphids, and (ii) what higher trophic level mechanisms drive aphid abundance. 2. Ligusticum porteri is a perennial host for the sap-feeding aphid Aphis asclepiadis and intraguild mirid predators (chiefly Lygus hesperus) in Colorado. We used long-term observational data to discover that aphids and mirids respond differently to phenological cues. These unique responses can impact aphid abundance through changes to host plant selection and quality. 3. We used behavioural choice assays to assess how advanced mirid phenology influences aphid host plant selection. More alates landed and reproduced on mirid-free control plants relative to host plants with prior mirid feeding. However, this preference did not correlate with aphid performance when we compared aphid relative growth rates between treatments. This suggests that advanced mirid phenology would impact aphid populations more through host plant choice, rather than reductions in host quality. The addition of mirids to experimental aphid colonies also demonstrated reduced aphid colony growth via predation. 4. We measured plant cues involved in host selection and found differences in volatile composition between plants with prior mirid feeding compared to control plants, providing the potential for aphids to detect enemy-free space using volatile cues.     

Ant–aphid mutualism: the influence of ants on the aphid summer cycle

There are few longtime studies on the effects on aphids of being tended by ants. The aim of this study is to investigate how the presence of ants influences settling decisions by colonizing aphids and the post‐settlement growth and survival of aphid colonies. We conducted a field experiment using the facultative myrmecophile Aphis fabae and the ant Lasius niger. The experiment relied on natural aphid colonization of potted plants of scentless mayweed Tripleurospermum perforatum placed outdoors. Ants occurred naturally at the field site and had access to half of the pots and were prevented from accessing the remainder. The presence of winged, dispersing aphids, the growth and survival of establishing aphid colonies, and the presence of parasitoids were measured in relation to presence or absence of ants, over a period of five weeks. The presence of ants did not significantly influence the pattern of initial host plant colonization or the initial colony growth, but ant‐tended aphids were subject to higher parasitism by hymenopteran parasitoids. The net result over the experimental period was that the presence of ants decreased aphid colony productivity, measured as the number of winged summer migrants produced from the colonized host plants. This implies that aphids do not always benefit from the presence of ants, but under some conditions rather pay a cost in the form of reduced dispersal.     

The NIa‐Pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector,Myzus persicae (green peach aphid)

Many plant viruses depend on aphids and other phloem‐feeding insects for transmission within and among host plants. Thus, viruses may promote their own transmission by manipulating plant physiology to attract aphids and increase aphid reproduction. Consistent with this hypothesis, Myzus persicae (green peach aphids) prefer to settle on Nicotiana benthamiana infected with Turnip mosaic virus (TuMV) and fecundity on virus‐infected N. benthamiana and Arabidopsis thaliana (Arabidopsis) is higher than on uninfected controls. TuMV infection suppresses callose deposition, an important plant defense, and increases the amount of free amino acids, the major source of nitrogen for aphids. To investigate the underlying molecular mechanisms of this phenomenon, 10 TuMV genes were over‐expressed in plants to determine their effects on aphid reproduction. Production of a single TuMV protein, nuclear inclusion a‐protease domain (NIa‐Pro), increased M. persicae reproduction on both N. benthamiana and Arabidopsis. Similar to the effects that are observed during TuMV infection, NIa‐Pro expression alone increased aphid arrestment, suppressed callose deposition and increased the abundance of free amino acids. Together, these results suggest a function for the TuMV NIa‐Pro protein in manipulating the physiology of host plants. By attracting aphid vectors and promoting their reproduction, TuMV may influence plant–aphid interactions to promote its own transmission.     

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.     

Occurrence of cotton aphids (Aphis gossypii) and lady beetles (Hamonia axyridis) on Hibiscus syriacus Linne: Are the aphids a pest of cucurbits?

Populations of cotton aphid on Hibiscus syriacus increased rapidly from 17 to 24 May 2007, and then decreased as its predator, the lady beetle Hamonia axyridis, increased in number. There was a 10 day time lag between peak populations of aphids and lady beetles. The infestation of aphids on H. syriacus produced some damage, but H. syriacus recovered soon after the lady beetles arrived. Cotton aphid clones from H. syriacus were transferred to other summer host plants: to five different vegetables on two dates, and to cucumber on three dates. Apart from one case where reproduction occurred on eggplant, most H. syriacus aphid clones did not survive on the vegetables. The cotton aphid on H. syriancus was prey and a food source for H. axyridis and acted to conserve natural enemies.