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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.

Background The Russian wheat aphid, Diuraphis noxia Kurdjumov, is one of the most important pests of small grains throughout the temperate regions of the world. This phytotoxic aphid causes severe systemic damage symptoms in wheat, barley, and other small grains as a direct result of the salivary proteins it injects into the plant while feeding. Results We sequenced and de novo assembled the genome of D. noxia Biotype 2, the strain most virulent to resistance genes in wheat. The assembled genomic scaffolds span 393 MB, equivalent to 93% of its 421 MB genome, and contains 19,097 genes. D. noxia has the most AT-rich insect genome sequenced to date (70.9%), with a bimodal CpG( O/E ) distribution and a complete set of methylation related genes. The D. noxia genome displays a widespread, extensive reduction in the number of genes per ortholog group, including defensive, detoxification, chemosensory, and sugar transporter groups in comparison to the Acyrthosiphon pisum genome, including a 65% reduction in chemoreceptor genes. Thirty of 34 known D. noxia salivary genes were found in this assembly. These genes exhibited less homology with those salivary genes commonly expressed in insect saliva, such as glucose dehydrogenase and trehalase, yet greater conservation among genes that are expressed in D. noxia saliva but not detected in the saliva of other insects. Genes involved in insecticide activity and endosymbiont-derived genes were also found, as well as genes involved in virus transmission, although D. noxia is not a viral vector. Conclusions This genome is the second sequenced aphid genome, and the first of a phytotoxic insect. D. noxia ’s reduced gene content of may reflect the influence of phytotoxic feeding in shaping the D. noxia genome, and in turn in broadening its host range. The presence of methylation-related genes, including cytosine methylation, is consistent with other parthenogenetic and polyphenic insects. The D. noxia genome will provide an important contrast to the A. pisum genome and advance functional and comparative genomics of insects and other organisms.

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.

Hesperidin is a highly bioactive natural flavonoid whose role in ecological interactions is poorly known. In particular, the effects of hesperidin on herbivores are rarely reported. Flavonoids have been considered as prospective biopesticides; therefore, the aim of the present study was to examine the influence of hesperidin on the host plant selection behavior of three aphid (Hemiptera: Aphididae) species: Acyrthosiphon pisum Harrris, Rhopalosiphum padi (L.), and Myzus persicae (Sulz.). The aphid host plants were treated with 0.1% and 0.5% ethanolic solutions of hesperidin. Aphid probing behavior in the no-choice experiment was monitored using electropenetrography and aphid settling on plants in the choice experiment was recorded. The results demonstrated that hesperidin can be applied as a pre-ingestive, ingestive, and post-ingestive deterrent against A. pisum, as an ingestive deterrent against R. padi, and as a post-ingestive deterrent against M. persicae using the relatively low 0.1% concentration. While in A. pisum the deterrent effects of hesperidin were manifested as early as during aphid probing in peripheral plant tissues, in M. persicae, the avoidance of plants was probably the consequence of consuming the hesperidin-containing phloem sap.

Phenotypic plasticity results in a diversity of phenotypes from a single genotype in response to environmental cues. To understand the molecular basis of phenotypic plasticity, studies have focused on differential gene expression levels between environmentally determined phenotypes. The extent of alternative splicing differences among environmentally determined phenotypes has largely been understudied. Here, we study alternative splicing differences among plastically produced morphs of the pea aphid using RNA-sequence data. Pea aphids express two separate polyphenisms (plasticity with discrete phenotypes): a wing polyphenism consisting of winged and wingless females and a reproduction polyphenism consisting of asexual and sexual females. We find that pea aphids alternatively splice 34% of their genes, a high percentage for invertebrates. We also find that there is extensive use of differential spliced events between genetically identical, polyphenic females. These differentially spliced events are enriched for exon skipping and mutually exclusive exon events that maintain the open reading frame, suggesting that polyphenic morphs use alternative splicing to produce phenotype-biased proteins. Many genes that are differentially spliced between polyphenic morphs have putative functions associated with their respective phenotypes. We find that the majority of differentially spliced genes is not differentially expressed genes. Our results provide a rich candidate gene list for future functional studies that would not have been previously considered based solely on gene expression studies, such as ensconsin in the reproductive polyphenism, and CAKI in the wing polyphenism. Overall, this study suggests an important role for alternative splicing in the expression of environmentally determined phenotypes.

Many insects engage in symbiotic associations with diverse assemblages of bacterial symbionts that can deeply impact on their ecology and evolution. The intraspecific variation of symbionts remains poorly assessed while phenotypic effects and transmission behaviors, which are key processes for the persistence and evolution of symbioses, may differ widely depending on the symbiont strains. Serratia symbiotica is one of the most frequent symbiont species in aphids and a valuable model to assess this intraspecific variation since it includes both facultative and obligate symbiotic strains. Despite evidence that some facultative S. symbiotica strains exhibit a free-living capacity, the presence of these strains in wild aphid populations, as well as in insects with which they maintain regular contact, has never been demonstrated. Here, we examined the prevalence, diversity, and tissue tropism of S. symbiotica in wild aphids and associated ants. We found a high occurrence of S. symbiotica infection in ant populations, especially when having tended infected aphid colonies. We also found that the S. symbiotica diversity includes strains found located within the gut of aphids and ants. In the latter, this tissue tropism was found restricted to the proventriculus. Altogether, these findings highlight the extraordinary diversity and versatility of an insect symbiont and suggest the existence of novel routes for symbiont acquisition in insects.

Aphids in the Svalbard archipelago are limited to a few highly specialized species adapted to extreme Arctic conditions. Among them, the endemic species historically identified as Sitobion (Metobion) calvulum remains poorly studied. Its systematic placement has been uncertain due to the lack of fresh material, and key aspects of its reproductive biology and endosymbionts remain unknown. Here, using an integrative approach combining molecular phylogenetics, morphology, and reproductive system analysis, we clarify its taxonomy and biology. Phylogenetic analyses based on mitochondrial COI and nuclear EF-1α sequences reveal its close relationship to Nearctic Macrosiphum species, leading to the establishment of the new taxon combination Macrosiphum calvulum comb. nov. Simultaneously, morphological observations uncover several atypical traits that challenge the established boundaries within Macrosiphini. Ultrastructural studies highlight unique reproductive adaptations, including secretion patterns in male accessory glands and oviparous female spermathecae. The absence of known facultative endosymbionts aligns M. calvulum with other aphids in Svalbard. We used SEM to detail the morphology of the sexual generation and applied TEM and, for the first time in aphids, micro-CT imaging to analyze their reproductive system. Given that Svalbard is among the most climate-threatened regions globally, studying M. calvulum is essential for understanding and conserving Arctic biodiversity.

In this study we examined the role of sorghum flavonoids in providing resistance against corn leaf aphid (CLA) Rhopalosiphum maidis. In sorghum, accumulation of these flavonoids is regulated by a MYB transcription factor, yellow seed1 (y1). Functional y1 alleles accumulate 3-deoxyflavonoids (3-DFs) and 3—deoxyanthocyanidins (3-DAs) whereas null y1 alleles fail to accumulate these compounds. We found that significantly higher numbers of alate CLA adults colonized null y1 plants as compared to functional y1 plants. Controlled cage experiments and pairwise choice assays demonstrated that apterous aphids preferred to feed and reproduce on null y1 plants. These near-isogenic sorghum lines do not differ in their epicuticular wax content and were also devoid of any leaf trichomes. Significantly higher mortality of CLA was observed on artificial aphid diet supplemented with flavonoids obtained from functional y1 plants as compared to null y1 plants or the relevant controls. Our results demonstrate that the proximate mechanism underlying the deleterious effects on aphids is y1-regulated flavonoids which are important defense compounds against CLA.

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.

(1) Background: Genistein is a naturally occurring flavonoid with a rich spectrum of biological activities, including plant-herbivore interactions. The aim of the study was to evaluate the effect of exogenous application of genistein on aphid behavior during probing in plant tissues. (2) Methods: Vicia faba, Brassica rapa ssp. pekinensis, and Avena sativa were treated transepidermally with a 0.1% ethanolic solution of genistein, and the probing behavior of generalist aphid species Aphis fabae, Myzus persicae, and Rhopalosiphum padi was monitored on their respective treated and untreated host plants using electropenetrography (=electrical penetration graph technique, EPG); (3) Results: Genistein did not deter aphid probing activities in non-phloem tissues. In A. fabae and R. padi, a trend towards reduction and in M. persicae a trend towards increase in phloem sap ingestion occurred on genistein-treated plants, but these trends were not statistically significant. (4) Conclusions: Genistein is not a deterrent chemical against generalist aphid species studied; therefore, it is not recommended for practical application.