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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.

Both inhibitory and stimulatory (known as hormesis) effects of the sublethal flupyradifurone, a butenolide insecticide, on Myzus persicae Sulzer (Hemiptera: Aphididae) were investigated for incorporating it into integrated pest management (IPM). A leaf-dip bioassay showed that flupyradifurone was very toxic against adult M. persicae with a 48 h LC50 of 8.491 mg/L. Using the age-stage two-sex life table approach, we assessed the effects of LC25 of flupyradifurone on adult M. persicae and its progeny (F1 and F2). On the one hand, aphids exposed to flupyradifurone had significantly negative effects on the life history traits acrossing the generations, such as reduced the adult longevity and fecundity of F0, shortened the duration of third instar and fourth instar nymphs, preadult period and the pre-reproductive period of F1, and decreased the reproductive days and adult longevity of F2. On the other hand, stimulatory effects on the duration of pre-adult, adult reproductive days, and reproduction of F1 were observed in the flupyradifurone-treated aphids. Consistently with the stimulation on individual traits, a higher net reproductive rate (R0) of F1 and a shorter mean generation time (T) of F2 were observed in the flupyradifurone-treated aphids, although the other population parameters including the intrinsic rate of increase (r), finite rate of increase (λ) and T of F1 and R0, r and λ of F2 were not significantly affected. These results revealed that adult M. persicae exposed to sublethal concentration of flupyradifurone can induce hormetic effects on F1, and also cause negative effects on F2. Our results would be useful for assessing the overall effects of flupyradifurone on M. persicae and the hormetic effects should take into consideration when use flupyradifurone for control M. persicae.

We collected developmental, survival, and reproduction data for Aphis fabae Scopoli (Hemiptera: Aphididae) reared on faba bean, Vicia faba L. ‘Sevilla’ at four constant temperatures (15, 20, 25, and 30°C), 70% relative humidity, and a photoperiod of 16:8 (L:D) h. The highest intrinsic rate of increase (r = 0.4347 d-1) and finite rate (λ = 1.5445 d-1) were observed at 25°C. The population projection based on the age-stage, two-sex life table quantitatively revealed the growth potential and stage structure of the aphid. We have included the following suggestions to aid researchers in life table studies: 1) The bootstrap method should be used to estimate the variance and SEs of developmental time, survival rate, fecundity, and population parameters. 2) The required number of bootstraps is dependent on the life table data—the higher the variation among individuals, the higher the number of bootstraps should be. In most cases, we suggest that 100,000 bootstraps should be used to obtain a stable estimate of variance and SEs. 3) Computer projection based on the age-stage, two-sex life table should be used to reveal the stage structure during population growth. 4) We used a simple equation based on the total fecundity, survival rate to adult stage, and first reproductive age to detect possible errors in life table parameters. 5) To assist readers in comprehending results, life table studies should include the cohort size, preadult survival rate, number of emerged female adults, mean fecundity, survival and fecundity curves, and population parameters.

Arbuscular mycorrhizal fungi may promote growth and stress resilience of plants, particularly under water-deficit conditions. However, interactions among mycorrhizal fungi, wheat plants, and aphids like the English grain aphid Sitobion avenae (Hemiptera: Aphididae) under water-deficit stress are still not well understood. Here, we examined the colonization of the fungus Claroideoglomus etunicatum (Glomerales: Claroideoglomeraceae) on wheat, and its effects on development and behavior of S. avenae under different water regimes. The symbiosis between C. etunicatum and wheat tended to increase the total developmental times of S. avenae nymphs under water deficit, but decreased adult lifespans. Irrespective of water conditions or wheat cultivars (Xinong-979 and Chang-6794), this symbiosis tended to cause higher adult weights and fecundities of S. avenae. These findings suggested that inoculation of this fungus could induce some life history trait trade-offs for S. avenae. Inoculation of C. etunicatum caused significant increases in contents of total amino acids in Xinong-979, and contents of some individual amino acids (e.g., glutamine) in both cultivars. This aphid preferred settling on symbiotic plants, with alate individuals attracted to well-watered Xinong-979 from 4 and Chang-6794 from 24 h postrelease. Increased phloem feeding and reduced pathway phase time for S. avenae were found in symbiotic plants. The fungus C. etunicatum also significantly enhanced wheat growth, especially under water deficit, and increased contents of nonessential and essential amino acids in Xinong-979. Our results highlight complex interactions among fungus symbiosis, wheat cultivars, and water conditions, emphasizing the potential to boost wheat crop resilience in the context of global climate change.

Abstract Transitions toward simplified life cycles can reshape evolutionary trajectories, yet their impact on the rate of molecular evolution remains poorly understood. In aphids, host alternation (heteroecy) entails obligate seasonal migration between highly distinct plant hosts—typically woody and herbaceous species—and has been repeatedly lost, giving rise to monoecious species with simplified life cycles. Using comparative genomics across 46 aphid species, we tested whether transitions from heteroecy to monoecy alter evolutionary dynamics at the gene level. We identified 9,304 orthologs and estimated evolutionary rates (dN/dS) and shifts in selection regimes in the diverse Aphidinae subfamily. We found that 715 orthologs evolved faster in monoecious species, primarily due to relaxed selection, while heteroecious species showed signatures of intensified selection. Genes under relaxed selection in monoecious species were enriched for functions related to environmental sensing, signaling, nutritional adjustments, morph determination, and migration related—traits likely central for host alternation. These results suggest that the loss of a complex life cycle leads to reduced selective constraints as a consequence of ecological simplification. This study provides a robust evolutionary framework for understanding how life cycle transitions shape molecular evolution and drive gene decay following trait loss.

Defensive metabolites and nutrient restriction of host plants are 2 major obstacles to the colonization of insect herbivores. The green peach aphid (GPA) Myzus persicae (Sulzer) broadly colonizes plants with diverse nutritional and defensive traits. However, how GPA adapts to nutritional and defensive traits within different plants remains largely unknown. To elucidate this, we first investigated the performances and transcriptomes of GPA feeding on cabbage Brassica oleracea and pepper Capsicum annuum. The green peach aphid had lower weight and fecundity when feeding on cabbage than on pepper. The transcriptomic analysis found 824 differentially expressed genes (DEGs), and 13 of the top 20 Kyoto Encyclopedia of Genes and Genomes pathways are related to nutrient metabolism, energy metabolism, and detoxification. Specifically, we found 160 DEGs associated with the metabolism of protein and amino acids, sugar and lipids, and xenobiotic substances, 86 upregulated in cabbage-fed GPA. Fourteen cathepsin B genes were strongly upregulated in cabbage-fed GPA, and were enriched in lysosome pathway and 2 dominated gene ontology terms peptidase activity and proteolysis. In addition, cabbage-fed GPA upregulated sugar and lipid digestion, while downregulated lipid biosynthesis processes. Furthermore, 55 metabolic detoxification enzyme genes were differentially expressed between GPA on 2 hosts, and detoxification enzyme activities of GPA indeed changed accordingly to the host. Then, we found that cabbage has lower amino acids nutrition quality for GPA compared to pepper. Our results suggested that adjustment of nitrogen nutrient metabolism, sugar and lipid metabolism, and metabolic detoxification in a host-specific manner play crucial roles in the adaptations of GPA to different host plants.

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.

Clothianidin is a second-generation neonicotinoid insecticide, widely used against sap-sucking insect pest including melon aphid,Aphis gossypiiGlover (Hemiptera: Aphididae). This pest causes severe economic damage to Cucurbitaceae plants worldwide. In this study, we investigated clothianidin resistance development under continuous selection pressure. Moreover, the age-stage, two-sex life table approach was used to evaluate the impact of clothianidin resistance on the fitness ofA.gossypii. A clothianidin resistant strain (CT-R) with a 23.17-fold resistance level was developed from a susceptible strain (CT-S) after continuous selection for 24 generations. Life table results showed a significant reduction in the relative fitness (0.847) of CT-R strain compared to the CT-S strain ofA.gossypii. The developmental duration, oviposition days, total pre-oviposition period (TPOP), longevity, and fecundity of CT-R strain were found to be significantly lower when compared to CT-S strain. The demographic parameters, including the intrinsic rate of increase (r), finite rate of increase (lambda), net reproductive rate (R-0), and mean generation time (T) were also significantly decreased in CT-R strain compared to the CT-S strain. Both the reproductive and survival rates were affected by clothianidin resistance in CT-R strain compared with the CT-S strain ofA.gossypii. Overall, our results demonstrate that in-depth knowledge about the trade-off at play between resistance degree and fitness cost might be useful to design resistance management strategies againstA.gossypii.

Bell pepper endornavirus (BPEV) Alphaendornavirus capsici (Endornaviridae) is an RNA virus that infects many pepper (Capsicum annuum) horticultural types and is seed transmitted. BPEV does not cause apparent symptoms and is found at every plant developmental stage. During the domestication of bell pepper, plant breeders, unaware of the existence of endornaviruses in the germplasm, selected endornavirus-infected genotypes. This could be an indication that the presence of endornaviruses in this crop is beneficial. Among the possible beneficial effects that endornaviruses may provide to their host could include tolerance or resistance to biotic and abiotic agents and, therefore, may have evolved a symbiotic relationship with their hosts. With this in mind, we set out to determine host preference, host suitability, and population dynamics of green peach aphid Myzus persicae (Sulzer) on BPEV-infected and virus-free bell pepper near-isogenic lines. During choice bioassay experiments, we observed that a higher proportion of M. persicae adults settled on BPEV noninfected leaves as compared to BPEV-infected leaves. Life table analysis revealed that M. persicae performed less well on BPEV-infected leaf tissues, with reductions in longevity, progeny, and intrinsic rate of increase. These results indicate BPEV is beneficial to its host, protecting against an important generalist pest.

Plant-mediated RNA interference (RNAi) has been successfully used as a tool to study gene function in aphids. The persistence and transgenerational effects of plant-mediated RNAi in the green peach aphid (GPA) Myzus persicae were investigated, with a focus on three genes with different functions in the aphid. Rack1 is a key component of various cellular processes inside aphids, while candidate effector genes MpC002 and MpPIntO2 (Mp2) modulate aphid–plant interactions. The gene sequences and functions did not affect RNAi-mediated down-regulation and persistence levels in the aphids. Maximal reduction of gene expression was ~70% and this was achieved at between 4 d and 8 d of exposure of the aphids to double-stranded RNA (dsRNA)-producing transgenic Arabidopsis thaliana. Moreover, gene expression levels returned to wild-type levels within ~6 d after removal of the aphids from the transgenic plants, indicating that a continuous supply of dsRNA is required to maintain the RNAi effect. Target genes were also down-regulated in nymphs born from mothers exposed to dsRNA-producing transgenic plants, and the RNAi effect lasted twice as long (12–14 d) in these nymphs. Investigations of the impact of RNAi over three generations of aphids revealed that aphids reared on dsMpC002 transgenic plants experienced a 60% decline in aphid reproduction levels compared with a 40% decline of aphids reared on dsRack1 and dsMpPIntO2 plants. In a field setting, a reduction of the aphid reproduction by 40–60% would dramatically decrease aphid population growth, contributing to a substantial reduction in agricultural losses.