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The southern green stink bug (SGSB), Nezara viridula (L.), is an important agricultural pest in the United States. Limited information is available on the morphology of the female’s reproductive system in relation to morphological changes associated with the number of eggs produced and egg masses oviposited. The ability to assess reproductive health and reproductive status based on ovarian morphology (i.e., physiological age-grading) can be an important tool for evaluating field populations and laboratory colonies intended for the application of different management strategies and experimental trials. Thus, the goal of this study was to develop a physiological age-grading system for SGSB. Females aged from 0 to 79 d chronologically randomly selected from laboratory colonies and dissected to assess ovarian morphology. Specific morphological differences in ovarian structures including differentiation of the ovarioles, deposition of yolk in the most proximal follicle, quantity and appearance of follicular relics, expansion of the lateral oviducts, and number of developing follicles per ovariole were related to chronological age, the number of eggs produced and number of egg masses. Based on specific combinations of these morphological characteristics, the continuum of ovarian development was divided into three nulliparous (i.e., ‘no eggs’; N1, N2, and N3) and three parous stages (i.e., ‘with eggs’; P1, P2, and P3). Direct relationships were noted between number of eggs produced and physiological age with over 7-fold higher number of eggs and 14-fold higher number of egg masses associated with the P2 and P3 stages, respectively.

Development of insecticide resistance has been a serious concern worldwide, whose mechanisms have been attributed to evolutionary changes in pest insect genomes such as alteration of drug target sites, up-regulation of degrading enzymes, and enhancement of drug excretion. Here, we report a previously unknown mechanism of insecticide resistance: Infection with an insecticide-degrading bacterial symbiont immediately establishes insecticide resistance in pest insects. The bean bug Riptortus pedestris and allied stinkbugs harbor mutualistic gut symbiotic bacteria of the genus Burkholderia, which are acquired by nymphal insects from environmental soil every generation. In agricultural fields, fenitrothion-degrading Burkolderia strains are present at very low densities. We demonstrated that the fenitrothion-degrading Burkholderia strains establish a specific and beneficial symbiosis with the stinkbugs and confer a resistance of the host insects against fenitrothion. Experimental applications of fenitrothion to field soils drastically enriched fenitrothion-degrading bacteria from undetectable levels to >80% of total culturable bacterial counts in the field soils, and >90% of stinkbugs reared with the enriched soil established symbiosis with fenitrothion-degrading BURKHOLDERIA: In a Japanese island where fenitrothion has been constantly applied to sugarcane fields, we identified a stinkbug population wherein the insects live on sugarcane and ≈8% of them host fenitrothion-degrading BURKHOLDERIA: Our finding suggests the possibility that the symbiont-mediated insecticide resistance may develop even in the absence of pest insects, quickly establish within a single insect generation, and potentially move around horizontally between different pest insects and other organisms.

Taxon-restricted genes make up a considerable proportion of genomes, yet their contribution to phenotypic evolution is poorly understood. We combined gene expression with functional and behavioral assays to study the origin and adaptive value of an evolutionary innovation exclusive to the water strider genus Rhagovelia: the propelling fan. We discovered that two taxon-restricted genes, which we named geisha and mother-of-geisha, specifically control fan development. geisha originated through a duplication event at the base of the Rhagovelia lineage, and both duplicates acquired a novel expression in a specific cell population prefiguring fan development. These gene duplicates played a central role in Rhagovelia’s adaptation to a new physical environment, demonstrating that the evolution of taxon-restricted genes can contribute directly to evolutionary novelties that allow access to unexploited ecological niches.

Global warming impacts diverse organisms not only directly but also indirectly via other organisms with which they interact. Recently, the possibility that elevated temperatures resulting from global warming may substantially affect biodiversity through disrupting mutualistic/parasitic associations has been highlighted. Here we report an experimental demonstration that global warming can affect a pest insect via suppression of its obligate bacterial symbiont. The southern green stinkbug Nezara viridula depends on a specific gut bacterium for its normal growth and survival. When the insects were reared inside or outside a simulated warming incubator wherein temperature was controlled at 2.5°C higher than outside, the insects reared in the incubator exhibited severe fitness defects (i.e., retarded growth, reduced size, yellowish body color, etc.) and significant reduction of symbiont population, particularly in the midsummer season, whereas the insects reared outside did not. Rearing at 30°C or 32.5°C resulted in similar defective phenotypes of the insects, whereas no adult insects emerged at 35°C. Notably, experimental symbiont suppression by an antibiotic treatment also induced similar defective phenotypes of the insects, indicating that the host’s defective phenotypes are attributable not to the heat stress itself but to the suppression of the symbiont population induced by elevated temperature. These results strongly suggest that high temperature in the midsummer season negatively affects the insects not directly but indirectly via the heat-vulnerable obligate bacterial symbiont, which highlights the practical relevance of mutualism collapse in this warming world. IMPORTANCE Climate change is among the biggest environmental issues in the contemporary world, and its impact on the biodiversity and ecosystem is not only of scientific interest but also of practical concern for the general public. On the basis of our laboratory data obtained under strictly controlled environmental conditions and our simulated warming data obtained in seminatural settings (elevated 2.5°C above the normal temperature), we demonstrate here that Nezara viridula , the notorious stinkbug pest, suffers serious fitness defects in the summer season under the simulated warming conditions, wherein high temperature acts on the insect not directly but indirectly via suppression of its obligate gut bacterium. Our finding highlights that heat-susceptible symbionts can be the “Achilles’ heel” of symbiont-dependent organisms under climate change conditions. Climate change is among the biggest environmental issues in the contemporary world, and its impact on the biodiversity and ecosystem is not only of scientific interest but also of practical concern for the general public. On the basis of our laboratory data obtained under strictly controlled environmental conditions and our simulated warming data obtained in seminatural settings (elevated 2.5°C above the normal temperature), we demonstrate here that Nezara viridula , the notorious stinkbug pest, suffers serious fitness defects in the summer season under the simulated warming conditions, wherein high temperature acts on the insect not directly but indirectly via suppression of its obligate gut bacterium. Our finding highlights that heat-susceptible symbionts can be the “Achilles’ heel” of symbiont-dependent organisms under climate change conditions.

Microbial symbioses are essential for many animals, but their outcomes are often context dependent. For example, rising temperatures can disrupt symbioses by eliminating thermally sensitive symbionts. The temperature tolerance of a symbiont may therefore limit the temperature range of its host, but switching to a more thermally tolerant partner could expand this range. Eastern leaf footed bugs (Leptoglossus phyllopus) depend on symbiotic Caballeronia bacteria which they must acquire from the environment early in development. Could this result in intergenerational partner switching that improves host outcomes under changing conditions? As a first step towards answering this question, we tested the hypothesis that host outcomes in this symbiosis vary among symbiont strains in a temperature-dependent manner. Nymphs were provided with one of six Caballeronia strains with varying thermal optima and reared at temperatures from 24–40°C. We observed temperature- and strain-dependent tradeoffs in host outcomes, with different strains conferring improved host weight, development time, and survival at cooler versus warmer temperatures. Differences in host outcomes were most pronounced at high temperatures, with some strains imposing severe costs. However, Caballeronia’s in vitro thermal optima did not predict in vivo outcomes. Regardless, strain- and temperature- dependent outcomes suggest that environmental symbiont acquisition could mitigate the effects of thermal stress on host populations. It is often assumed that vertical transmission of a beneficial symbiont from parent to offspring is the optimal strategy, but our results suggest that environmental acquisition could offer unique benefits under changing conditions.

Evidence accumulates that the functional plasticity of insulin and insulin-like growth factor signaling in insects could spring, among others, from the multiplicity of insulin receptors (InRs). Their multiple variants may be implemented in the control of insect polyphenism, such as wing or caste polyphenism. Here, we present a comprehensive phylogenetic analysis of insect InR sequences in 118 species from 23 orders and investigate the role of three InRs identified in the linden bug, Pyrrhocoris apterus, in wing polymorphism control. We identified two gene clusters (Clusters I and II) resulting from an ancestral duplication in a late ancestor of winged insects, which remained conserved in most lineages, only in some of them being subject to further duplications or losses. One remarkable yet neglected feature of InR evolution is the loss of the tyrosine kinase catalytic domain, giving rise to decoys of InR in both clusters. Within the Cluster I, we confirmed the presence of the secreted decoy of insulin receptor in all studied Muscomorpha. More importantly, we described a new tyrosine kinase-less gene (DR2) in the Cluster II, conserved in apical Holometabola for ∼300 My. We differentially silenced the three P. apterus InRs and confirmed their participation in wing polymorphism control. We observed a pattern of Cluster I and Cluster II InRs impact on wing development, which differed from that postulated in planthoppers, suggesting an independent establishment of insulin/insulin-like growth factor signaling control over wing development, leading to idiosyncrasies in the co-option of multiple InRs in polyphenism control in different taxa.

Chemical control is currently the main strategy for managing brown marmorated stink bug, Halyomorpha halys (Stål). However, chemical pesticides can harm nontarget species, including natural enemies of H. halys. Pesticides with high toxicity to H. halys and low toxicity to its parasitoids need to be identified to support H. halys management. This is not only for natural biological control but also for preemptive classical biological control of H. halys by parasitoids. Here, we assessed the contact toxicity of residues of eight insecticides against H. halys and three of its main parasitoid species (Anastatus japonicus Ashmead (Hymenoptera: Eupelmidae), Trissolcus japonicus Ashmead (Hymenoptera: Scelionidae), Trissolcus cultratus Mayr (Hymenoptera: Scelionidae)). This study aims to provide valuable insights for preemptive classical biological control of H. halys using these parasitoids. Our results showed that A. japonicus exhibited higher tolerance to the tested pesticides, while T. japonicus was the most sensitive species. Among the pesticides, chlorantraniliprole had the lowest overall impact on all three parasitoid species. Additionally, acetamiprid, azadirachtin, and rotenone were found to be harmless to A. japonicus. Acetamiprid, however, was slightly harmful to T. cultratus. The remaining pesticides showed moderate to significant harmful effects on the parasitoids. For H. halys adults and fifth instars, the pesticides tested caused no mortality within the 24 h exposure. However, young nymphs were susceptible to the tested pesticides. Fenpropathrin had the highest toxicity to H. halys, killing 83.3%, 52.8%, and 19.4% of second, third, and fourth instars in a 24 h exposure. Fenpropathrin, acetamiprid, cyfluthrin, azadirachtin, and dinotefuran were all slightly harmful to the first instar nymphs. The other pesticides were harmless to H. halys in a 24 h exposure. Halyomorpha halys mortality increased with the contact time with the residue. Mortality of fourth and fifth instars of H. halys was >70% for fenpropathrin, cyfluthrin, dinotefuran, abamectin-aminomethyl, and acetamiprid if exposure continued for 7 d. Acetamiprid was effective in controlling H. halys nymphs but exhibited varying levels of toxicity towards the three tested parasitoid species, depending on the residue age and exposure time. Azadirachtin showed lower overall toxicity to beneficial insects, suggesting that these materials could be used to manage H. halys while minimizing harm to key beneficial species.

In the symbiosis of the bean bug Riptortus pedestris with Burkholderia insecticola, the bacteria occupy an exclusive niche in the insect midgut and favor insect development and reproduction. In order to understand how the symbiotic bacteria stably colonize the midgut crypts and which services they provide to the host, we compared the cytology, physiology, and transcriptomics of free-living and midgut-colonizing B. insecticola. The analyses revealed that midgut-colonizing bacteria were smaller in size and had lower DNA content, they had increased stress sensitivity, lost motility, and an altered cell surface. Transcriptomics revealed what kinds of nutrients are provided by the bean bug to the Burkholderia symbiont. Transporters and metabolic pathways of diverse sugars such as rhamnose and ribose, and sulfur compounds like sulfate and taurine were upregulated in the midgut-colonizing symbionts. Moreover, pathways enabling the assimilation of insect nitrogen wastes, i.e. allantoin and urea, were also upregulated. The data further suggested that the midgut-colonizing symbionts produced all essential amino acids and B vitamins, some of which are scarce in the soybean food of the host insect. Together, these findings suggest that the Burkholderia symbiont is fed with specific nutrients and also recycles host metabolic wastes in the insect gut, and in return, the bacterial symbiont provides the host with essential nutrients limited in the insect food, contributing to the rapid growth and enhanced reproduction of the bean bug host.

This research investigated the effects of neem oil on mortality, survival and malformations of the non-target stink bug predator, Podisus nigrispinus . Neurotoxic and growth inhibitor insecticides were used to compare the lethal and sublethal effects from neem oil on this predator. Six concentrations of neem oil were topically applied onto nymphs and adults of this predator. The mortality rates of third, fourth, and fifth instar nymphs increased with increasing neem oil concentrations, suggesting low toxicity to P. nigrispinus nymphs. Mortality of adults was low, but with sublethal effects of neem products on this predator. The developmental rate of P. nigrispinus decreased with increasing neem oil concentrations. Longevity of fourth instar nymphs varied from 3.74 to 3.05 d, fifth instar from 5.94 to 4.07 d and adult from 16.5 and 15.7 d with 0.5 and 50% neem doses. Podisus nigrispinus presented malformations and increase with neem oil concentrations. The main malformations occur in wings, scutellum and legs of this predator. The neem oil at high and sub lethal doses cause mortality, inhibits growth and survival and results in anomalies on wings and legs of the non-traget predator P. nigrispinus indicating that its use associated with biological control should be carefully evaluated.

Stink bugs (Hemiptera: Pentatomidae), including the exotic Halyomorpha halys (Stål), Nezara viridula (L.), and other indigenous species, are pests that damage a variety of agricultural crops. At a study site in the southeastern United States, we measured the density of stink bug species and patterns of parasitism and predation on corn, cotton, and soybean and host trees in an adjacent woodline. We assessed parasitism and predation of naturally laid egg masses in crops and sentinel egg masses in host trees and used pheromone-baited traps to determine H. halys seasonal development. Overall, H. halys and N. viridula were the dominant bugs observed. Adult H. halys were first detected each year on trees, followed by corn, and then cotton and soybean, suggesting that trees served as a source of H. halys dispersing into crops. For H. halys, more nymphs were captured in soybean than in corn or cotton. For N. viridula, more adults were captured in corn and cotton than in soybean, and more nymphs were captured in corn during 2019 and 2021 than in 2020. Percentage parasitism of N. viridula egg masses (74.2%) was higher than than that for H. halys egg masses (54.3%). Accordingly, conservation biological control has the potential to enhance parasitism of indigenous stink bugs and H. halys in field crop agroecosystems.