The green peach aphid, M. persicae (Sulzer), is one of the most important pests of horticultural crops worldwide. In Chile, M. persicae causes severe losses in peach and herbaceous crops. Understanding aphid population dynamics across its primary (peach) and secondary (weed) hosts is fundamental to developing a more effective pest control strategy. To investigate the spatial genetic connectivity of M. persicae populations between cultivated and non-cultivated hosts, we conducted a longitudinal survey in three commercial peach orchards in central Chile. Apterous aphid colonies were repeatedly sampled from peach trees and weed hosts located both within and outside orchards, and population genetic structure and clonal diversity were characterized using six polymorphic microsatellite loci. Genetic differentiation was low between weed populations inside and outside orchards, whereas greater differentiation was observed between peach trees and weeds outside orchards. Three recurrent multilocus genotypes persisted across multiple seasons, orchards, and host plants, indicating substantial spatiotemporal persistence of particular clonal lineages. Comparison with insecticide-resistance profiles further showed that neutral population structure and resistance-associated variation were not necessarily concordant. These findings support an important role for non-cultivated hosts in maintaining recurrent M. persicae lineages within peach agroecosystems and highlight the value of considering surrounding vegetation in integrated pest management.

Nudiviruses are double-stranded DNA viruses that infect invertebrate species, ranging from aquatic arthropods to insects from diverse orders. Remnants of nudiviral infections have been found as introgressions in the genome of several insect hosts, such as aphids pest species (Hemiptera: Aphididae). However, a nudivirus infecting aphids has yet to be reported. Here, we describe the complete genome sequences of two nudiviruses found in the aphid Neuquenaphis staryi, a species that branched out early in the Aphididae family and is endemic to southern beech forests in South America. These nudiviruses (NsNV-1 and NsNV-2) share 98% of nucleotide identity between them and belong to the Alphanudivirus genus. Notably, we found that the prevalence of NsNV-1 was 16 times higher than NsNV-2 in natural N. staryi populations, and co-infections were not observed. Furthermore, we show that horizontal gene transfer between aphids and nudiviruses has been bidirectional, providing evidence of their dynamic co-evolutionary relationship. This study provides the first documentation of nudivirus infections in aphids and expands our understanding of the evolutionary interactions between nudiviruses and their insect hosts.

Facultative bacterial endosymbionts are key components of aphid biology, influencing host performance and ecological interactions. We investigated how facultative endosymbionts affect competitive interactions between aphid clones of the cereal aphid Sitobion avenae (Fabricius) in Chilean wheat fields. We assessed the population development and life‐history traits of the two dominant genotypes (G1 and G2) under single‐clone rearing, intra‐ and inter‐genotypic competition scenarios, with and without the facultative endosymbiont Regiella insecticola shaping these interactions. Our findings reveal that R. insecticola does not significantly alter inter‐genotypic competition outcomes: clone G2 consistently outcompeted G1 regardless of infection status. However, under intra‐genotypic competition, R. insecticola ‐infected G1 aphids outperformed their uninfected counterparts, while the opposite trend was observed in G2. R. insecticola influenced winged morph production and aphid weight in a genotype‐dependent manner. Aphids harbouring R. insecticola induced less physiological stress on host plants, as evidenced by lower root/shoot ratios. These results suggest that facultative endosymbionts may confer clone‐specific advantages, shaping aphid performance and aphid clone‐endosymbiont‐plant dynamics in multifaceted ways.

Bacterial endosymbionts are key components of aphid biology, as they modify several traits of their insect hosts. Here we studied how bacterial facultative endosymbionts affect the competitive interactions between aphid clones. To address this, we studied intraclonal and interclonal interactions between the two most common clones (G1 and G2) of the cereal aphid Sitobion avenae (Fabricius), including the role of the facultative endosymbiont Regiella insecticola in the outcome of these interactions in a shared host (wheat). The results of this study reveal significant variability in the population growth rates of aphid clones under competitive and non-competitive environments. That trade-off in competitive interactions among aphid clones can influence the dynamics of aphid populations and impact on plant growth and structure. While facultative endosymbionts like R. insecticola do not play a significant role in directly mediating the competitive interactions of aphid clones or affecting specific plant traits, their presence does enhance aphid performance. Aphids harbouring R. insecticola showed higher growth rates in various coexistence scenarios and across different clones with a concurrently reduced capacity to damage host plants, which suggests that R. insecticola produces ecologically relevant consequences for aphids in cereal fields.

The English grain aphid, Sitobion avenae, is a significant agricultural pest affecting wheat, barley, and oats. In Chile, the most prevalent and persistent clone (superclone) of S. avenae harbours the facultative endosymbiont bacterium Regiella insecticola. To determine the role of this bacteria in the ecological success of this superclone, the presence of R. insecticola was manipulated to evaluate the impact on 1) the reproductive performance of this clone in two host plant species (wheat and barley), 2) the production of winged morphs, 3) changes in the proteomic profile of insects, and 4) root/shoot ratio of plant. It was determined that this superclone of S. avenae proliferates differentially in the host plants studied depending on the presence of the facultative bacterial endosymbiont, observing that the clone develops better in wheat when it is infected with R. insecticola while the opposite occurs when it develops in barley. Aphid biomass was higher when harbouring R. insecticola, particularly in barley. Individuals infected with R. insecticola, in both host plants, showed higher proportion of winged individuals. The protein regulation of aphids on wheat was comparatively lower and stable than that on barley. A higher root/shoot biomass ratio was detected in wheat than in oats in plants attacked with aphids harbouring R. insecticola. R. insecticola significantly affects the reproductive and proteomic performance of the S. avenae superclone, changes influenced by the host plant, suggesting that the host plant x facultative endosymbiont interaction can drive host specialization intraclonally, partly the ecological success of the superclones.

The English grain aphid, Sitobion avenae, is a significant agricultural pest affecting wheat, barley, and oats. In Chile, the most prevalent and persistent clone (superclone) of S. avenae harbors the facultative endosymbiont bacterium Regiella insecticola. To determine the role of this bacterium in the reproductive success of this superclone, the presence of R. insecticola was manipulated to assess its impact on (1) the reproductive performance of this clone on two host plant species (wheat and barley), (2) the production of winged morphs, (3) changes in the insects' proteomic profiles, and (4) the root/shoot ratio of plant. It was found that the reproductive performance of this S. avenae superclone varied across host plants, depending on the presence of the facultative bacterial endosymbiont. Aphids infected with R. insecticola showed higher reproductive success on wheat, while the opposite effect was observed on barley. Aphid biomass was greater when infected with R. insecticola, particularly on barley. Additionally, aphids harboring R. insecticola exhibited a higher proportion of winged individuals on both host plants. Protein regulation in aphids on wheat was lower compared to those on barley. A higher root/shoot biomass ratio was observed in wheat plants compared to barley when infested by R. insecticola-infected aphid. Thus, R. insecticola significantly influences the reproductive performance and proteomic profile of a S. avenae superclone, with these effects shaped by the host plant. This suggests that the interaction between the host plant and the facultative endosymbiont contributes to the ecological success of this superclone.

BACKGROUND: Facultative bacterial endosymbionts have the potential to influence the interactions between aphids, their natural enemies, and host plants. Among the facultative symbionts found in populations of the grain aphid Sitobion avenae in central Chile, the bacterium Regiella insecticola is the most prevalent. In this study, we aimed to investigate whether infected and cured aphid lineages exhibit differential responses to wheat cultivars containing varying levels of the benzoxazinoid DIMBOA (2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one), which is a xenobiotic compound produced by plants. Specifically, we examined the reproductive performance responses of the most frequently encountered genotypes of Sitobion avenae when reared on wheat seedlings expressing low, medium, and high concentrations of DIMBOA.RESULTS: Our findings reveal that the intrinsic rate of population increase (r(m) ) in cured lineages of Sitobion avenae genotypes exhibits a biphasic pattern, characterized by the lowest r(m) and an extended time to first reproduction on wheat seedlings with medium levels of DIMBOA. In contrast, the aphid genotypes harbouring Regiella insecticola display idiosyncratic responses, with the two most prevalent genotypes demonstrating improved performance on seedlings featuring an intermediate content of DIMBOA compared to their cured counterparts.CONCLUSION: This study represents the first investigation into the mediating impact of facultative endosymbionts on aphid performance in plants exhibiting varying DIMBOA contents. These findings present exciting prospects for identifying novel targets for aphid control by manipulating the presence of aphid symbionts.(c) 2023 Society of Chemical Industry.

While male-killing bacteria are known to infect across arthropods, ladybird beetles represent a known hotspot. In some host species, there are multiple different symbionts that vary in presence and frequency between populations. To further our understanding of spatial and frequency variation, we tested for the presence of three male-killing bacteria: Wolbachia, Rickettsia and Spiroplasma, in two Adalia ladybird species from a previously unexplored UK population. The two-spot ladybird, A. bipunctata is known to harbour all three male-killers, and we identified Spiroplasma infection in the Merseyside population for the first time. However, in contrast to previous studies on ladybirds from continental Europe, evidence from egg hatch rates indicates this Spiroplasma strain does not cause embryonic male-killing in the Merseyside population. In the related ten-spot ladybird, A. decempunctata, there is only one previous record of a male-killing symbiont, a Rickettsia, which we did not detect in the Merseyside sample. However, PCR assays indicated the presence of a Spiroplasma in a single A. decempunctata. Marker sequence indicated that this Spiroplasma was divergent from that found in sympatric A. bipunctata. Genome sequencing of the Spiroplasma-infected A. decempunctata additionally revealed the presence of cobionts in the form of a Centistes parasitoid wasp and the parasitic fungi Beauveria. Further study of A. decempunctata from this population is needed to resolve whether it is the ladybird or wasp cobiont that harbours Spiroplasma, and to establish the phenotype of this strain. These data indicate first that microbial symbiont phenotype should not be assumed from past studies conducted in different locations, and second that cobiont presence may confound screening studies aimed to detect the frequency of a symbiont in field collected material from a focal host species.

Aphids are important herbivorous insects that can cause significant crop damage, leading to yield reduction and economic loss. One avenue being explored to reduce aphid impacts is the development of aphid-resistant plants. Under projected climate scenarios, it is expected that plants will be exposed to greater biotic and abiotic stress, including increased herbivorous insect infestation and exposure to prolonged periods of environmental stress, particularly drought. In response to these projections, plant-aphid interactions under drought conditions have been a subject of growing interest; however, few studies have looked at the impact of drought stress on plant resistance to aphids despite the potential importance for plant breeding. Here, we examine the latest scientific advances regarding variation in plant resistance to aphids under drought, emphasizing underlying mechanisms and functional trade-offs and propose a conceptual model relating plant tolerance to drought with plant resistance to aphids.

Leucoptera sinuella (Reutti) (Lepidoptera: Lyonetiidae) is a leaf miner specialist on Salicaceae recently introduced to Chile and Argentina, where it is causing economic damage to poplar plantations. We report a field survey in a poplar nursery naturally infested showing that regardless of the poplar hybrid taxon, high variability in resistance was observed among clones within families for oviposition and leaf-mining damage. A group of susceptible and resistant hybrid poplar clones was then selected for a laboratory evaluation of oviposition (antixenosis) and leaf-mining damage (antibiosis) on potted, rooted shoot cuttings. The concentration of condensed tannins (CTs) and salicinoid phenolic glucosides (SPGs) of the leaves of the selected clones from the laboratory study was also measured. Total oviposited eggs were positively correlated with leaf area, with the lowest oviposition on TMxT 11372 clone. The lowest percentage of mined leaf area was obtained for clones TMxT 11372, TMxT 11463, and TDxD 17574, but surprisingly no correlation between the percentage of mined leaf area and concentration of CTs and SPGs was found. Resistant poplar hybrids of our study could be suitable for breeding programs aimed for L. sinuella integrated pest management.

Despite decades of research resulting in a comprehensive understanding of epicuticular wax metabolism, the function of these almost ubiquitous metabolites in plant-herbivore interactions remains unresolved. In this study, we examined the effects of CRISPR-induced knockout mutations in four Nicotiana glauca (tree tobacco) wax metabolism genes. These mutations cause a wide range of changes in epicuticular wax composition, leading to altered interactions with insects and snails. Three interaction classes were examined: chewing herbivory by seven caterpillars and one snail species, phloem feeding by Myzus persicae (green peach aphid) and oviposition by Bemisia tabaci (whitefly). Although total wax load and alkane abundance did not affect caterpillar growth, a correlation across species, showed that fatty alcohols, a minor component of N. glauca surface waxes, negatively affected the growth of both a generalist caterpillar (Spodoptera littoralis) and a tobacco-feeding specialist (Manduca sexta). This negative correlation was overshadowed by the stronger effect of anabasine, a nicotine isomer, and was apparent when fatty alcohols were added to an artificial lepidopteran diet. By contrast, snails fed more on waxy leaves. Aphid reproduction and feeding activity were unaffected by wax composition but were potentially affected by altered cutin composition. Wax crystal morphology could explain the preference of B. tabaci to lay eggs on waxy wild-type plants relative to both alkane and fatty alcohol-deficient mutants. Together, our results suggest that the varied responses among herbivore classes and species are likely to be a consequence of the co-evolution that shaped the specific effects of different surface wax components in plant-herbivore interactions.

Host plant recognition are highly dependent on chemosensory perception, which involves chemosensory proteins (CSPs) that bind key chemical compounds the host plants. In this work, we hypothesize that two closely related aphid taxa, which differ in diet breadth, also differ in their CSPs. We detected a non-synonymous difference (lysine for asparagine) between M. persicae sensu stricto (Mpp) and the subspecies M. p. nicotianae (Mpn) in the sequence of a CSP (CSP5). We modeled in silico the binding capacity of both CSP5s variants with 163 different potential ligands from their host plants (120 unique from tobacco, 29 unique from peach, and 14 common ligands). After docking analysis with all ligands, we selected the three best ligands for each variant to perform molecular dynamics (tobacco: 2-cyclopentene-1,4-dione, salicylaldehyde, and benzoic acid; peach: phenol, valeric acid, and benzonitrile). The binding energy of the MpnCSP5 model to the studied ligands was, in all cases, lower than with the MppCSP5 model. The ligands from the host plants showed more stable binding with MpnCSP5 than with MppCSP5. This result suggests that the set of CSPs studied among M. persicae s. str. and M. p. nicotianae are very similar, but focusing on the CSP5 protein, we found a single key mutation that increases affinities for host compounds for M. p. nicotianae, which might have contributed to the specialization to tobacco. This study provides new insights into an evolutionary trend toward specificity in a binding protein.

The English grain aphid, Sitobion avenae, is a cosmopolitan pest that feeds on cereals, provoking substantial yield losses by injuring plant tissue and by vectoring plant viruses. Here we report a highly complete, de novo draft genome of the grain aphid using long-read sequencing. We generated an assembly of 2740 contigs with a N50 of 450 kb. We compared this draft genome with that of other aphid species, inspecting gene family evolution, genome-wide positive selection, and searched for horizontal gene transfer events. In addition, we described a recent copy number variant expansion of gene families involving aconitase, ABC transporter, and esterase genes that could be associated with resistance to insecticides and plant chemical defenses. This S. avenae genome obtained from a predominant invasive genotype can provide a framework for studying the spatial-temporal success of these clonal lineages in invaded agroecosystems.

The grain aphid Sitobion avenae (Fabricius) is one of the most important cereal pests, damaging crops through sap sucking and virus transmission. Sitobion avenae harbors the secondary endosymbiont Regiella insecticola, which is highly prevalent in populations in south-central Chile and other regions of the world. In order to develop ecological alternatives for biological control, we studied the effect of applying the spores of a strain of the bacterium Bacillus subtilis on the survival and fecundity of the most prevalent genotype of S. avenae in central Chile. The strain selected was one that in previous studies had shown the ability to outcompete other bacteria. Using clones of this aphid genotype infected and uninfected with R. insecticola, we found that applying B. subtilis spores through artificial diets and spraying on leaves decreased both adult survival and nymph production. The detection of spores within the aphid body was negatively correlated with nymph production and was lower in the presence of R. insecticola when applied in diets. B. subtilis spores applied on leaves reduced the number of aphids, an effect that was stronger on aphids harboring R. insecticola. A possible interaction between endosymbiotic bacteria and bacterial antagonists within the aphid body is discussed.

The aphid Myzus persicae is a destructive agricultural pest that displays an exceptional ability to develop resistance to both natural and synthetic insecticides. To investigate the evolution of resistance in this species we generated a chromosome-scale genome assembly and living panel of >110 fully sequenced globally sampled clonal lines. Our analyses reveal a remarkable diversity of resistance mutations segregating in global populations of M. persicae . We show that the emergence and spread of these mechanisms is influenced by host–plant associations, uncovering the widespread co‐option of a host-plant adaptation that also offers resistance against synthetic insecticides. We identify both the repeated evolution of independent resistance mutations at the same locus, and multiple instances of the evolution of novel resistance mechanisms against key insecticides. Our findings provide fundamental insights into the genomic responses of global insect populations to strong selective forces, and hold practical relevance for the control of pests and parasites.

The pea aphid, Acyrthosiphon pisum Harris, is able to colonize various habitats and form genetically distinct biotypes worldwide. In Chile, few genotypes are dominating in space and time and are qualified as "superclones". Here, we compared in the laboratory different biological features of the most common clones of A. pisum collected from pea (Ap1) and alfalfa (Ap2) fields, in order to gain some insight on their differential ability to colonize broad bean plants. We also studied their probing behavior, profiled their proteome and characterized their community of endosymbionts. We found that the Ap1 genotype performed better on Vicia faba and realized more salivation events in phloem than Ap2. In addition, Ap1 presented a higher prevalence of the endosymbiont Serratia symbiotica. Among the total of 40 proteins that were differentially expressed, 14 and 26 were upregulated in Ap1 and Ap2 genotypes, respectively. The symbionin from Buchnera aphidicola was found to be upregulated in Ap1. A field experiment showed that both genotypes were able to colonize wild legumes, with Ap1 reproducing better on Vicia nigricans than Ap2. However, Ap2 exhibited higher reproduction in the other three wild legumes, suggesting higher invasiveness capacity on wild plants. Variation in the ability to colonize, feeding behavior and the putative involvement of differentially regulated proteins between Ap1 and Ap2 are discussed in relation to their respective endosymbiotic composition, nutritional lifestyle and consequences on their "superclone" status.

The codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae), is a major pest introduced to almost all main pome fruit production regions worldwide. This species was detected in Chile during the last decade of the 19th century, and now has a widespread distribution in all major apple-growing regions. We performed an analysis of the genetic variability and structure of codling moth populations in Chile using five microsatellite markers. We sampled the codling moth along the main distribution area in Chile on all its main host-plant species. Low genetic differentiation among the population samples (FST = 0.03) was found, with only slight isolation by distance. According to a Bayesian assignment test (TESS), a group of localities in the coastal mountain range from the Bío-Bío Region formed a distinct genetic cluster. Our results also suggest that the codling moth that invaded the southernmost locality (Aysén Region) had two origins from central Chile and another unknown source. We did not find significant genetic differentiation between codling moth samples from different host-plant species. Our results indicate high genetic exchange among codling moth populations between the different Chilean regions and host plants.

The effects of microorganisms on plant-insect interactions have usually been underestimated. While plant growth-promoting rhizobacteria (PGPR) are known to induce plant defenses, endosymbiotic bacteria hosted by herbivorous insects are often beneficial to the host. Here, we aimed to assess whether PGPR-induced defenses in broad bean plants impact the pea aphid, depending on its genotype and the presence of endosymbionts. We estimated aphid reproduction, quantified defense- and growth-related phytohormones by GC-MS, and measured different plant growth and physiology parameters, after PGPR treatment. In addition, we recorded the feeding behavior of aphids by electropenetrography. We found that the PGPR treatment of broad bean plants reduced the reproduction of one of the pea aphid clones. We highlighted a phenomenon of PGPR-induced plant defense priming, but no noticeable plant growth promotion. The main changes in aphid probing behavior were related to salivation events into phloem sieve elements. We suggest that the endosymbiont Hamiltonella defensa played a key role in plant-insect interactions, possibly helping aphids to counteract plant-induced resistance and allowing them to develop normally on PGPR-treated plants. Our results imply that plant- and aphid-associated microorganisms add greater complexity to the outcomes of aphid-plant interactions.

The author would like to include the following changes in the published article.

Myzus persicae es considerado la tercera plaga de importancia económica de varios cultivos en Chile. Su variabilidad genética es influenciada por la disponibilidad del hospedante primario. Este insecto ha adquirido resistencia a la mayoría de los insecticidas utilizados para su control. El presente trabajo tuvo como objetivo evaluar la diversidad genética y la presencia de mecanismos de resistencia de M. persicae en cultivos como duraznero y pimentón. El estudio se realizó en doce localidades: seis en la región de O'Higgins y seis en la región del Maule en Chile central. Para evaluar la diversidad genética neutral, se utilizaron siete marcadores microsatélites, y la identificación de mecanismos se realizó mediante ensayos de discriminación alélica. La mayor diversidad genética se presentó en poblaciones del duraznero > 0,80 en promedio. En pimentón y arvenses, esta diversidad fue 0,36 en promedio. La frecuencia de individuos con mecanismos de resistencia fue baja y en forma predominantemente heterocigota en los hospedantes evaluados, lo que sugiere que la forma de reproducción sexual del áfido influye en los niveles de resistencia a insecticida. La presencia de mecanismos de resistencia en M. persicae depende del hospedante, región geográfica y momento de muestreo en el que son evaluados. Existe suficiente evidencia de que las poblaciones de M. persicae están compuestas por muy pocos grupos genéticos, presentando diferentes dinámicas de resistencia a insecticidas en la misma temporada agrícola.