Explore the vast range of titles available.

Aphids are important agricultural pests and also biological models for studies of insect-plant interactions, symbiosis, virus vectoring, and the developmental causes of extreme phenotypic plasticity. Here we present the 464 Mb draft genome assembly of the pea aphid Acyrthosiphon pisum. This first published whole genome sequence of a basal hemimetabolous insect provides an outgroup to the multiple published genomes of holometabolous insects. Pea aphids are host-plant specialists, they can reproduce both sexually and asexually, and they have coevolved with an obligate bacterial symbiont. Here we highlight findings from whole genome analysis that may be related to these unusual biological features. These findings include discovery of extensive gene duplication in more than 2000 gene families as well as loss of evolutionarily conserved genes. Gene family expansions relative to other published genomes include genes involved in chromatin modification, miRNA synthesis, and sugar transport. Gene losses include genes central to the IMD immune pathway, selenoprotein utilization, purine salvage, and the entire urea cycle. The pea aphid genome reveals that only a limited number of genes have been acquired from bacteria; thus the reduced gene count of Buchnera does not reflect gene transfer to the host genome. The inventory of metabolic genes in the pea aphid genome suggests that there is extensive metabolite exchange between the aphid and Buchnera, including sharing of amino acid biosynthesis between the aphid and Buchnera. The pea aphid genome provides a foundation for post-genomic studies of fundamental biological questions and applied agricultural problems.

Pea ( Pisum sativum L.) is a major legume crop frequently infested by various parasites, including the pea aphid ( Acyrthosiphon pisum Harris), which takes nutrients from its host and transmits phytopathogenic viruses. This aphid species comprises several biotypes, each one capable of feeding and reproducing on a limited range of specific legume species. However, little is known about the transcriptional response of the plants to different aphid biotypes. To investigate pea defense mechanisms against the pea-adapted and pea non-adapted A. pisum biotypes, we analyzed the transcriptional responses by mRNA sequencing of six pea genotypes with contrasting resistance levels and different haplotypes at the ApRVII locus. This locus confers partial resistance to the pea-adapted and non-adapted A. pisum biotypes. Transcriptomic analyses of pea genotypes with and without aphid infestation revealed 9,217 differentially expressed genes in pea genotypes infested with the pea-adapted aphids, while fewer genes, 1,561 genes total, were expressed in response to the pea non-adapted aphids. Both aphid biotypes activated immune responses and the biosynthesis of secondary metabolites, including flavonoids. However, the pea-adapted biotype appeared to suppress multiple pathways associated with photosynthesis, cell wall biosynthesis, fatty acid metabolism, and other growth-related processes. Candidate genes potentially involved in aphid resistance were identified both within and outside of the ApRVII locus. These findings provide insights into pea resistance mechanisms against both pea-adapted and pea non-adapted A. pisum biotypes, as well as the ability of the adapted biotype to modulate pea defenses leading to host susceptibility, and pave the way for follow-up studies, including metabolomic analyses.

Climate change can affect species directly and indirectly by altering interactions between species within communities. These indirect effects can ramify through a community and affect many species, including some that may not have been directly affected by the perturbation. Identifying these chains of indirect effects is difficult, and most studies only follow indirect effects across two or three species. Here, we use a factorial field experiment to demonstrate that precipitation affects spotted aphids through a complex chain of indirect interactions that are mediated by other herbivores and a generalist predator. We experimentally simulated drought, which reduced water content in alfalfa plants. While water stress in alfalfa had no direct effect on spotted aphids, it lowered the population growth rate of pea aphids, another common alfalfa pest. Because ladybeetle predators were attracted to high pea aphid densities, predator densities were lower in drought treatments. Consequently, spotted aphid densities were released from top-down control (apparent competition) in drought treatments and reached densities three times higher than spotted aphids in ambient treatments with high pea aphid densities. Thus, drought affected spotted aphids in the interaction chain: drought → alfalfa → pea aphids → predators → spotted aphids. This result illustrates the lengthy path that indirect effects of climate change may take through a community, as well as the importance of community-level experiments in determining the net effect of climate change.

Some bacterial symbionts alter their hosts reproduction through various mechanisms that enhance their transmission in the host population. In addition to its obligatory symbiont Buchnera aphidicola, the pea aphid Acyrthosiphon pisum harbors several facultative symbionts influencing several aspects of host ecology. Aphids reproduce by cyclical parthenogenesis whereby clonal and sexual reproduction alternate within the annual life cycle. Many species, including the pea aphid, also show variation in their reproductive mode at the population level, with some lineages reproducing by cyclical parthenogenesis and others by permanent parthenogenesis. While the role of facultative symbionts has been well studied during the parthenogenetic phase of their aphid hosts, very little is known on their possible influence during the sexual phase. Here we investigated whether facultative symbionts modulate the capacity to produce sexual forms in various genetic backgrounds of the pea aphid with controlled symbiont composition and also in different aphid genotypes from natural populations with previously characterized infection status and reproductive mode. We found that most facultative symbionts exhibited detrimental effects on their hosts fitness under sex-inducing conditions in comparison with the reference lines. We also showed that the loss of sexual phase in permanently parthenogenetic lineages of A. pisum was not explained by facultative symbionts. Finally, we demonstrated that Spiroplasma infection annihilated the production of males in the host progeny by inducing a male-killing phenotype, an unexpected result for organisms such as aphids that reproduce primarily through clonal reproduction.

Background Natural products are important sources for the discovery of new biopesticides to control the worldwide destructive pests Acyrthosiphon pisum Harris . Here, insecticidal substances were discovered and characterized from the secondary metabolites of the bio-control microorganism Bacillus velezensis strain ZLP-101, as informed by whole-genome sequencing and analysis. Results The genome was annotated, revealing the presence of four potentially novel gene clusters and eight known secondary metabolite synthetic gene clusters. Crude extracts, prepared through ammonium sulfate precipitation, were used to evaluate the effects of strain ZLP-101 on Acyrthosiphon pisum Harris aphid pests via exposure experiments. The half lethal concentration (LC50) of the crude extract from strain ZLP-101 against aphids was 411.535 mg/L. Preliminary exploration of the insecticidal mechanism revealed that the crude extract affected aphids to a greater extent through gastric poisoning than through contact. Further, the extracts affected enzymatic activities, causing holes to form in internal organs along with deformation, such that normal physiological activities could not be maintained, eventually leading to death. Isolation and purification of extracellular secondary metabolites were conducted in combination with mass spectrometry analysis to further identify the insecticidal components of the crude extracts. A total of 15 insecticidal active compounds were identified including iturins, fengycins, surfactins, and spergualins. Further insecticidal experimentation revealed that surfactin, iturin, and fengycin all exhibited certain aphidicidal activities, and the three exerted synergistic lethal effects. Conclusions This study improved the available genomic resources for B. velezensis and serves as a foundation for comprehensive studies of the insecticidal mechanism by Bacillus velezensis ZLP-101 in addition to the active components within biological control strains.

The Asian yellow-legged hornet Vespa velutina nigrithorax, a major predator of honeybees, is spreading in Europe in part due to a lack of efficient control methods. In this study, as a first step to identify biological control agents, we characterized viral RNA sequences present in asymptomatic or symptomatic hornets. Among 19 detected viruses, the honey bee virus Deformed wing virus-B was predominant in all the samples, particularly in muscles from the symptomatic hornet, suggesting a putative cause of the deformed wing symptom. Interestingly, two new viruses closely related to Acyrthosiphon pisum virus and Himetobi P virus and viruses typically associated with honey bees, Acute bee paralysis virus and Black queen cell virus, were detected in the brain and muscles, and may correspond to the circulation and possible replication forms of these viruses in the hornet. Aphid lethal paralysis virus, Bee Macula-like virus, and Moku virus, which are known to infect honey bees, were also identified in the gut virus metagenome of hornets. Therefore, our study underlined the urgent need to study the host range of these newly discovered viruses in hornets to determine whether they represent a new threat for honey bees or a hope for the biocontrol of V. velutina.

Individuals vary in their ability to defend against pathogens. Determining how natural selection maintains this variation is often difficult, in part because there are multiple ways that organisms defend themselves against pathogens. One important distinction is between mechanisms of resistance that fight off infection, and mechanisms of tolerance that limit the impact of infection on host fitness without influencing pathogen growth. Theory predicts variation among genotypes in resistance, but not necessarily in tolerance. Here, we study variation among pea aphid (Acyrthosiphon pisum) genotypes in defense against the fungal pathogen Pandora neoaphidis. It has been well established that pea aphids can harbor symbiotic bacteria that protect them from fungal pathogens. However, it is unclear whether aphid genotypes vary in defense against Pandora in the absence of protective symbionts. We therefore measured resistance and tolerance to fungal infection in aphid lines collected without symbionts, and found variation among lines in survival and in the percent of individuals that formed a sporulating cadaver. We also found evidence of variation in tolerance to the effects of pathogen infection on host fecundity, but no variation in tolerance of pathogen-induced mortality. We discuss these findings in light of theoretical predictions about host-pathogen coevolution.

The performance of herbivorous insects is greatly affected by plant nutritional quality and resistance, which are likely to be altered by rising concentrations of atmospheric CO2. We previously reported that elevated CO2 enhanced biological nitrogen (N) fixation of Medicago truncatula, which could result in an increased supply of amino acids to the pea aphid (Acyrthosiphon pisum). The current study examined the N nutritional quality and aphid resistance of sickle, an ethylene-insensitive mutant of M. truncatula with supernodulation, and its wild-type control A17 under elevated CO2 in open-top field chambers. Regardless of CO2 concentration, growth and amino acid content were greater and aphid resistance was lower in sickle than in A17. Elevated CO2 up-regulated N assimilation and transamination-related enzymes activities and increased phloem amino acids in both genotypes. Furthermore, elevated CO2 down-regulated expression of 1-amino-cyclopropane-carboxylic acid (ACC), sickle gene (SKL) and ethylene response transcription factors (ERF) genes in the ethylene signaling pathway of A17 when infested by aphids and decreased resistance against aphids in terms of lower activities of superoxide dismutase (SOD), peroxidase (POD), and polyphenol oxidase (PPO). Our results suggest that elevated CO2 suppresses the ethylene signaling pathway in M. truncatula, which results in an increase in plant nutritional quality for aphids and a decrease in plant resistance against aphids.

1. Determining the factors governing investment in immunity is critical to understanding host-pathogen ecological and evolutionary dynamics. Studies often consider disease resistance in the context of life-history theory, with the expectation that investment in immunity will be optimized in anticipation of disease risk. Immunity, however, is constrained by context-dependent fitness costs. How the costs of immunity vary across life-history strategies has yet to be considered. 2. Pea aphids are typically unwinged but produce winged offspring in response to high population densities and deteriorating conditions. This is an example of polyphenism, a strategy used by many organisms to adjust to environmental cues. The goal of this study was to examine the relationship between the fitness costs of immunity, pathogen resistance and the strength of an immune response across aphid morphs that differ in life-history strategy but are genetically identical. 3. We measured fecundity of winged and unwinged aphids challenged with a heat-inactivated fungal pathogen, and found that immune costs are limited to winged aphids. We hypothesized that these costs reflect stronger investment in immunity in anticipation of higher disease risk, and that winged aphids would be more resistant due to a stronger immune response. However, producing wings is energetically expensive. This guided an alternative hypothesis that investing resources into wings could lead to a reduced capacity to resist infection. 4. We measured survival and pathogen load after live fungal infection, and we characterized the aphid immune response to fungi by measuring immune cell concentration and gene expression. We found that winged aphids are less resistant and mount a weaker immune response than unwinged aphids, demonstrating that winged aphids pay higher costs for a less effective immune response. 5. Our results show that polyphenism is an understudied factor influencing the expression of immune costs. More generally, our work shows that in addition to disease resistance, the costs of immunity vary between individuals with different life-history strategies. We discuss the implications of these findings for understanding how organisms invest optimally in immunity in the light of context-dependent constraints.

1. Although phytophagous insects can vary genetically in host use and exhibit long-range movements, the combined implications of these phenomena for pest management have received limited attention. 2. To address this, we surveyed the genetic diversity of pea aphid Acyrthosiphon pisum using twelve microsatellite loci and assessed host association patterns and annual movement from a putative source region (Columbia River Basin) to the Palouse region of northern Idaho and western Washington, where the aphid is a pest of pea Pisum sativum. 3. A total of 320 identified unique genotypes clustered into four genetic groups, with two host plant associations: alfalfa Medicago sativa (three genetic groups), and pea Pisum sativum and vetch Vicia villosa (one genetic group). All four genetic groups occurred in the Columbia River Basin and in migrant aphids collected in pan traps during spring colonization in the Palouse during 2 years of this study. Patterns of group arrival on the Palouse were spatially structured early in the season, consistent with differing migration patterns. Despite genetic diversity of migrants, a single genetic group became predominant in pea crops each year. 4. Clonal laboratory colonies of pea aphids established from field-collected specimens and representing two predominant genetic groups exhibited reciprocal performance trade-offs, with alfalfa being a poor host for a pea-associated aphid genotype and vice versa. 5. Synthesis and applications. Annual spring migrants of pea aphids in the pea production region of the Palouse are genetically diverse, with different host plant affinities consistent with origination from source populations in the Columbia River Basin. As the season progresses, a single genetic group adapted to pea becomes predominant in the crop. Management of pea aphid in the Palouse will be improved by monitoring the temporal and spatial variation of specific genetic groups of the aphid arriving as immigrants during each crop season, providing this information to producers and adjusting estimates of risk of crop damage accordingly. The principle could apply to other pest species with host-adapted populations that colonize crops on an annual basis.