Soybean Aphid Research Articles

Constitutive and induced resistance in soybean interact to affect the performance of a herbivore and its parasitoid

This study examined how the induced defenses of soybean cultivars that vary in levels of constitutive resistance affect the developmental performance of the tobacco cutworm, Spodoptera litura, and its parasitoid, Meteorus pulchricornis. Both soybean cultivars were injured to induce defenses by either the beet armyworm, Spodoptera exigua, or by the aphid Aphis glycines. Both types of feeding on soybean plants had a negative effect on S. litura development, extending development time, reducing larva-to-pupa survival and decreasing adult body size. The impact of induction treatments increased linearly with increasing levels of constitutive resistance. Induction by the chewing herbivore was stronger than induction by the sucking herbivore in negatively affecting developmental parameters at both low and medium levels of soybean constitutive resistance, but had similar impacts on S. litura survival and adult body weight at the high level of constitutive resistance. Induction by both chewing and sucking herbivores extended parasitoid development time and decreased survival and fecundity, with effects on both development time and fecundity increasing linearly with levels of constitutive resistance, but without any effect on offspring survival. Thus, induction by the two herbivore types differed in impact on parasitoid performance depending on the level of constitutive resistance expressed in the soybean cultivar. The chewing herbivore was more effective than the sucking herbivore at low and medium levels of constitutive resistance, but there were no differences in parasitoid performance at the high level of constitutive resistance. Overall, whereas both chewing and sucking herbivores had negative effects on the development of S. litura and its parasitoid, the chewing herbivore was more effective than the sucking herbivore at low and medium levels of constitutive resistance, but similar to it at the high level.

Reaping benefits from an invasive species: role of Harmonia axyridis in natural biological control of Aphis glycines in North America

Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is an invasive species present in numerous agroecosystems in North America. Despite adverse impacts as a threat to native biodiversity, a nuisance household invader and a pest in fruit production, H. axyridis also plays a beneficial role as a major component of assemblages of generalist predators in several agricultural crops. Here, we review the role of H. axyridis as a natural enemy of Aphis glycines Matsumura (Hemiptera: Aphididae), an invasive pest of soybean, Glycine max (L.) Merrill (Fabales: Fabaceae), in North America. Harmonia axyridis is often the most abundant predator species attacking A. glycines in soybean agroecosystems. This predator has the potential to both prevent and suppress A. glycines outbreaks. Further studies are needed to fully understand and utilize the potential of H. axyridis as a natural enemy in the management of A. glycines and other agricultural pests in agroecosystems worldwide.

Soybean Aphid Response to their Alarm Pheromone E-ß-Farnesene (EBF)

When attacked by natural enemies some insect pests, including many aphid species, alert neighboring conspecifics with alarm pheromones. Cornicle secretions with pheromones benefit the attacked aphid but are costly to produce, while alarm pheromone benefits probably fall largely on alerted conspecifics. Given these variable benefits, the likelihood of a secretion may change depending on aphid density. Thus, we first hypothesized that the common alarm pheromone in aphids, E-s-farnesene (EBF), was present in soybean aphid (Aphis glycines Matsumura) cornicle secretions and would elicit an alarm response in aphids exposed to it. Second, since aphids other than the secretor also benefit from cornicle secretions, we hypothesized that the likelihood of secretion would increase concurrently with the density of neighboring clonal conspecifics. Third, because alarm reaction behavior (e.g. feeding cessation) is probably costly, we hypothesized that alarm reaction behavior would decrease as conspecific density (i.e. alternative prey for an attacking natural enemy) increased. We found that soybean aphids 1) produce cornicle secretions using EBF as an alarm pheromone, 2) are less likely to release cornicle secretions when alone than in a small group (~10 individuals), but that the rate of secretion does not increase further with additional conspecific density, and 3) also exhibit alarm reaction behavior in response to cornicle secretions independent of aphid density. We show that soybean aphids can use their cornicle secretions to warn their neighbors of probable attack by natural enemies, but that both secretion and alarm reaction behavior does not change as density of nearby conspecifics rises above a few individuals.

Efficacy of Foliar-Applied Sulfoxaflor for Control of Soybean Aphid and Impact on Lady Beetles, 2015: Table 1

Soybean aphid (SA) continues to be an important pest of soybean in eastern North Dakota. Insecticide trials continue to examine the efficacy of broad spectrum compounds (primarily pyrethroids), however, new chemistries must also be tested, especially those that have the potential to reduce mortality of beneficial insects. The objectives of this trial were to test the efficacy of foliar-applied sulfoxaflor in controlling SA, and to measure the immediate impact of sulfoxaflor on adult lady beetle (LB) numbers. The trial was conducted at a cooperator’s field approximately five miles east of Moorhead, MN. Test plots were established on 2 Jun using a two-row vacuum precision planter equipped with GPS at a seeding rate of 150,000 live seeds per acre. Each plot was 10 ft wide (4 rows at 30-inch row spacing) × 25 feet long. Two “guard rows” were left between each plot to prevent spray overlap. Plots were arranged in a RCB design with four replications. Foliar insecticide applications were made on 11 Aug using a tractor-mounted CO2 sprayer with …

Phenotyping Techniques and Identification of Soybean Resistance to the Kudzu Bug

The kudzu bug (KZB), Megacopta punctatissima Montandon 1896, is a newly invasive Asian pest of soybean [Glycine max (L.) Merrill] in the southeastern United States. Due to the unique biology of this soybean pest, six screening techniques were tested to identify host plant resistance (HPR) to KZB. Soybean lines previously characterized as resistant to either leaf‐chewing or piercing–sucking insects were used to test screening techniques and to identify potential sources of KZB resistance. Four open field experiments and one field cage experiment were conducted in 2010 to 2013 to screen ‘Benning’ near‐isogenic lines (NILs) for KZB resistance. These NILs possess different combinations of quantitative trait loci (QTLs) for resistance to leaf‐chewing insects from PI 229358 (QTLs M, G, and H) and PI 227687 (QTL E); however, none of these lines were consistently effective at controlling KZB. Additionally, 30 plant introductions (PIs) with previously observed resistance to either the soybean aphid (Aphis glycines Matsumura) or the silverleaf whitefly (Bemisia tabaci Gennadius) were screened in the field for KZB resistance. Six lines were identified as potential sources of resistance to KZB from this field using a KZB index. A no‐choice (antibiosis) assay was developed to confirm resistance observations from the field and to characterize the type of host plant resistance. PI 567336A and PI 567598B were confirmed as the most resistant of the screened PIs, and were characterized as having antibiosis resistance to KZB.

Comparative proteomic analysis in Aphis glycines Mutsumura under lambda-cyhalothrin insecticide stress

Lambda-cyhalothrin is now widely used in China to control the soybean aphid Aphis glycines. To dissect the resistance mechanism, a laboratory-selected resistant soybean aphid strain (CRR) was established with a 43.42-fold resistance ratio to λ-cyhalothrin than the susceptible strain (CSS) in adult aphids. In this study, a comparative proteomic analysis between the CRR and CSS strains revealed important differences between the susceptible and resistant strains of soybean aphids for λ-cyhalothrin. Approximately 493 protein spots were detected in two-dimensional polyacrylamide gel electrophoresis (2-DE). Thirty-six protein spots displayed differential expression of >2-fold in the CRR strain compared to the CSS strain. Out of these 36 protein spots, 21 had elevated and 15 had decreased expression. Twenty-four differentially expressed proteins were identified by MALDI TOF MS/MS and categorized into the functional groups cytoskeleton-related protein, carbohydrate and energy metabolism, protein folding, antioxidant system, and nucleotide and amino acid metabolism. Function analysis showed that cytoskeleton-related proteins and energy metabolism proteins have been associated with the λ-cyhalothrin resistance of A. glycines. The differential expression of λ-cyhalothrin responsive proteins reflected the overall change in cellular structure and metabolism after insecticide treatment in aphids. In summary, our studies improve understanding of the molecular mechanism resistance of soybean aphid to lambda-cyhalothrin, which will facilitate the development of rational approaches to improve the management of this pest and to improve the yield of soybean.

Aphidicidal activity of a novel botanical insecticide made by alkalization of bamboo tar

Bamboo tar is a water-insoluble semi-solid waste generated from bamboo charcoal processing, and its increasing accumulation threatens environment and sustainability of the charcoal industry that enhances the economic value of bamboo forestry in southern China. Here we converted bamboo tar to a completely water-soluble sodium salt through full alkalization with NaOH and evaluated its insecticidal activity against the cotton aphid Aphis gossypii, the soybean aphid Aphis glycines and the green peach aphid Myzus persicae in laboratory bioassays and field trials. The tar salt LC50s against the three global aphid pests decreased to 35–93 μg/ml on day 7 from 246 to 486 μg/ml on day 3. In three field trials, the tar salt at the application rates of 338–675 g/ha controlled the aphid pests as efficaciously as but more persistently than pymetrozine (a synthetic aphidicide) at the recommended rate. Our results highlight an easy approach to converting bamboo tar to a promising botanical aphidicide but extensive further work to determine its toxicity and environmental and crop safety is needed.

Registration of ‘Wyandot‐14’ Soybean with Resistance to Soybean Aphid and Powdery Mildew

‘Wyandot‐14’ soybean [Glycine max (L.) Merr.] (Reg. No. CV‐520, PI 676304) with resistance to soybean aphid (Aphis glycines) biotypes 1 and 2 and resistance to powdery mildew (caused by Microsphaera diffusa Cooke & Peck) was jointly released by the USDA‐ARS and The Ohio Agricultural Research and Development Center as a late maturity group (MG) II (2.9) food‐grade conventional cultivar. Soybean aphid is a major insect pest of soybean in the United States. The objective of this research was to incorporate soybean aphid and powdery mildew resistance into the popular food‐grade soybean cultivar Wyandot. Wyandot‐14 was developed by backcrossing the Rag2 and Rmd_PI243540 alleles for resistance to soybean aphid and powdery mildew, respectively, from PI 243540 into Wyandot. Compared to Wyandot, Wyandot‐14 showed no yield drag in the absence of soybean aphid and/or powdery mildew pressures. In soybean aphid‐infested fields, Wyandot‐14 had significantly (p ≤ 0.05) higher yield than Wyandot. Like Wyandot, Wyandot‐14 has white flowers, gray pubescence, brown pods, round seed with a shiny yellow seed coat, and a yellow (clear) hilum, and it has an indeterminate growth habit. Wyandot‐14 should be an excellent replacement for Wyandot.

Jasmonate-dependent plant defenses mediate soybean thrips and soybean aphid performance on soybean

Insect herbivores from different feeding guilds induce different signaling pathways in plants. In this study, we examined the effects of salicylic acid (SA)- and jasmonic acid (JA)-mediated defenses on performance of insect herbivores from two different feeding guilds: cell-content feeders, soybean thrips and phloem feeders, soybean aphids. We used a combination of RT-qPCR analysis and elicitor-induced plant resistance to determine induction of SA and JA signaling pathways and the impact on herbivore performance. In the early interaction between the host plant and the two herbivores, SA and JA signaling seems to occur simultaneously. But overall, soybean thrips induced JA-related marker genes, whereas soybean aphids increased SA and ABA-related marker genes over a 24-h period. Populations of both soybean thrips and soybean aphids were reduced (47 and 25 %, respectively) in methyl jasmonate (MeJA)-pretreated soybean plants. SA treatment has no effect on either herbivore performance. A combination pretreatment of SA and MeJA did not impact soybean thrips population but reduced soybean aphid numbers which was comparable with MeJA treatment. Our data suggest that SA–JA antagonism could be responsible for the effect of hormone pretreatment on thrips performance, but not on aphid performance. By linking plant defense gene expression and elicitor-induced resistance, we were able to pinpoint the role for JA signaling pathway in resistance to two herbivores from different feeding guilds.

Sex‐specific dispersal by a parasitoid wasp in the field

AbstractAlthough parasitoid wasps are important regulators of herbivorous insect populations, very little is known regarding their movement under field conditions. Here, we examined the vertical and cardinal directionality of dispersal by Binodoxys communis (Gahan) (Hymenoptera: Braconidae: Aphidiinae), an exotic Asian parasitoid released as a biological control agent of the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae: Aphidinae), in North American soybeans, Glycine max (L.) Merr. (Fabaceae). The patterns are consistent with time‐dependent, sex‐specific dispersal strategies; whereas males show flight that is devoid of vertical or cardinal directionality, females consistently move at or above soybean canopy height toward the east and north. Male capture rates also appear to be more correlated with local conditions than those of females. These results suggest that females actively cross the flight boundary layer (the space above which insect flight is largely wind‐driven as opposed to self‐directed) and follow air currents away from soybean fields, whereas males engage in more localized movement. The data also suggest differing response potentials of the sexes to changing local resource conditions (host availability, female availability, host plant cultivar). We discuss the implications for sex‐specific movement on the basic biology of introduced parasitoid species, and their applied role as potential agents in importation biological control programs.

Water Stress Modulates Soybean Aphid Performance, Feeding Behavior, and Virus Transmission in Soybean.

Little is known about how water stress including drought and flooding modifies the ability of plants to resist simultaneous attack by insect feeding and transmission of insect-vectored pathogen. We analyzed insect population growth, feeding behaviors, virus transmission, and plant amino acid profiles and defense gene expression to characterize mechanisms underlying the interaction between water stress, soybean aphid and aphid-transmitted, Soybean mosaic virus, on soybean plants. Population growth of non-viruliferous aphids was reduced under drought stress and saturation, likely because the aphids spent less time feeding from the sieve element on these plants compared to well-watered plants. Water stress did not impact population growth of viruliferous aphids. However, virus incidence and transmission rate was lowest under drought stress and highest under saturated conditions since viruliferous aphids took the greatest amount time to puncture cells and transmit the virus under saturated conditions and lowest time under drought stress. Petiole exudates from drought-stressed plants had the highest level of total free amino acids including asparagine and valine that are critical for aphid performance. Aphids did not benefit from improved phloem sap quality as indicated by their lower densities on drought-stressed plants. Saturation, on the other hand, resulted in low amino acid content compared to all of the other treatments. Drought and saturation had significant and opposing effects on expression of marker genes involved in abscisic acid (ABA) signaling. Drought alone significantly increased expression of ABA marker genes, which likely led to suppression of salicylic acid (SA)- and jasmonic acid (JA)-related genes. In contrast, ABA marker genes were down-regulated under saturation, while expression of SA- and JA-related genes was up-regulated. We propose that the apparent antagonism between ABA and SA/JA signaling pathways contributed to an increase in aphid densities under drought and their decrease under saturation. Taken together, our findings suggests that plant responses to water stress is complex involving changes in phloem amino acid composition and signaling pathways, which can impact aphid populations and virus transmission.

Evidence for Compensatory Photosynthetic and Yield Response of Soybeans to Aphid Herbivory.

The soybean aphid, Aphis glycines Matsumura, an exotic species in North America that has been detected in 21 U.S. states and Canada, is a major pest for soybean that can reduce maximum photosynthetic capacity and yields. Our existing knowledge is based on relatively few studies that do not span a wide variety of environmental conditions, and often focus on relatively high and damaging population pressure. We examined the effects of varied populations and duration of soybean aphids on soybean photosynthetic rates and yield in two experiments. In a 2011 field study, we found that plants with low cumulative aphid days (CAD, less than 2,300) had higher yields than plants not experiencing significant aphid pressure, suggesting a compensatory growth response to low aphid pressure. This response did not hold at higher CAD, and yields declined. In a 2013 controlled-environment greenhouse study, soybean plants were well-watered and fertilized with nitrogen (N), and aphid populations were manipulated to reach moderate to high levels (8,000-50,000 CAD). Plants tolerated these population levels when aphids were introduced during the vegetative or reproductive phenological stages of the plant, showing no significant reduction in yield. Leaf N concentration and CAD were positively and significantly correlated with increasing ambient photosynthetic rates. Our findings suggest that, given the right environmental conditions, modern soybean plants can withstand higher aphid pressure than previously assumed. Moreover, soybean plants also responded positively through a compensatory photosynthetic effect to moderate population pressure, contributing to stable or increased yield.

Effects of single and mixed infections of Bean pod mottle virus and Soybean mosaic virus on host‐plant chemistry and host–vector interactions

Summary Co‐infection by vector‐borne plant viruses is common, yet few studies have explored the effects of mixed infections on host‐plant phenotypes or plant–vector interactions. We documented the effects of single and mixed infection by Bean pod mottle virus (BPMV) and Soybean mosaic virus (SMV) on key biochemical plant traits and the behaviour and performance of virus vectors (BPMV: Epilachna varivestis, SMV: Aphis glycines) in order to understand how virus‐induced changes in plant phenotypes might influence (i) the acquisition and transmission of each virus by its respective vector in single infections, (ii) the likelihood of secondary infection for plants singly infected with either virus and (iii) the implications of co‐infection for virus transmission by vectors. Single infection by either BPMV or SMV increased host‐plant palatability for E. varivestis, potentially enhancing vector acquisition of BPMV from BPMV‐infected plants as well as the risk of secondary BPMV infection in plants infected with SMV. However, co‐infected plants were no more palatable to beetle vectors than mock‐inoculated plants. BPMV infection had minimal impacts on A. glycines. SMV infection reduced A. glycines population growth, but increased aphid feeding preferences for infected plants, a pattern likely not conducive to the (non‐persistent) transmission of SMV. Co‐infection eliminated the negative effects of single SMV infection on aphid population growth, and aphids exhibited a feeding preference for co‐infected (relative to mock‐inoculated) plants. Our results demonstrate that virus effects on host phenotype and vector behaviour can be modified by the presence of a co‐infecting virus, with potentially important implications for disease transmission.

Differential Reactions of Soybean Isolines With Combinations of Aphid Resistance Genes Rag1 , Rag2 , and Rag3 to Four Soybean Aphid Biotypes.

With the discovery of the soybean aphid ( Aphis glycines Matsumura) as a devastating insect pest of soybean ( Glycine max (L.) Merr.) in the United States, host resistance was recognized as an important management option. However, the identification of soybean aphid isolates exhibiting strong virulence against aphid resistance genes ( Rag genes) has highlighted the need for pyramiding genes to help ensure the durability of host resistance as a control strategy. In this study, soybean isolines with all possible combinations of the resistance and susceptibility alleles at Rag1 , Rag2 , and Rag3 were evaluated for their effectiveness against the four characterized soybean aphid biotypes. All soybean isolines, including the susceptible check carrying none of the resistance alleles (S1/S2/S3), were infested with each biotype in no-choice greenhouse tests, and the aphid populations developed on each isoline were enumerated 14 d after infestation. All gene combinations, with the exception of Rag3 alone, provided excellent protection against biotype 1. Isolines with Rag2 alone or in combination with Rag1 and Rag3 had greater levels of resistance to biotype 2 than those with either Rag1 alone, Rag3 alone, or the Rag1/3 pyramid. For biotype 3, the Rag1/3 and Rag1/2/3 pyramided lines significantly reduced aphid populations compared with all other gene combinations, while the Rag1/2/3 pyramid provided the greatest protection against biotype 4. Overall, the Rag1/2/3 pyramided line conferred the greatest protection against all four biotypes.

Population Dynamics of the Soybean Aphid (Hemiptera: Aphididae) in Quebec (Canada).

The population dynamics of the soybean aphid ( Aphis glycines Matsumura) was studied over a 12-yr period (2004-2015) from archive and field data collected in the Montérégie area of Quebec (Canada). As observed in the United States, a 2-yr oscillation cycle was observed from 2005 to 2011 in Quebec, with high infestations during odd years, while the opposite was found in 2014 and 2015. A broader pattern could also be observed, with high infestation in two consecutive years every 10 yr. In addition, the infestation intensity observed in high infestation years decreases throughout the years, which questions the evolution of the oscillation cycle in the future.

Parasitoid‐induced transgenerational fecundity compensation in an aphid

AbstractIncreased reproductive effort by organisms in response to attack by consumers (‘fecundity compensation’) is well documented in both plants and animals, although most examples only involve direct compensation by the individuals exposed to consumers. We used the parasitoid waspLysiphlebus orientalisStarý & Rakhshani (Hymenoptera:Braconidae) and the soybean aphid,Aphis glycinesMatsumura (Hemiptera:Aphididae), to determine whether reproduction by parasitized aphids can lead to fecundity compensation. Although parasitism byL. orientalisstrongly decreased fecundity for parasitized aphids, offspring of parasitized aphids reproduced at a greater rate at maturity than did the offspring of non‐parasitized aphids. Also, parasitized aphids contained fewer but larger embryos developing within them. The presence of these larger embryos may explain how the offspring of parasitized aphids can produce more progeny with no apparent reduction in progeny quality. Mature and nearly mature soybean aphids successfully reproduced after parasitism, a prerequisite for transgenerational fecundity compensation, andL. orientalisshowed a preference for these age classes of aphids as hosts when foraging. Transgenerational fecundity compensation may allow for higher than expected densities of both hosts and consumers to persist and may be adaptive for both the host and consumer in this system. The phenomenon could also reduce the strength of biological control interactions.

Impact of large strip cropping system (24 and 48 rows) on soybean aphid during four years in organic soybean

Strip cropping could be used to deliver several eco-services, including reducing pest pressure. The objective of this study was to evaluate the impact of the management of a strip cropping system of soybean, wheat, corn and vetch on soybean aphid Aphis glycines Matsumura, its natural enemies and on the harvest of soybean. Experimental set up of 18m and 36m strips were installed in 2006 on an organic farm at Les Cèdres, Québec, Canada and compared with control plots of 180m of soybean. Each plot was replicated two times on the farm and measured 1km long. Observations of soybean aphid and natural enemies were carried out on 18 plants per replicate strips and control plots during summer 2007–2010. Abundance of soybean aphid was reduced between 33 and 55% in strips compared with the control plots during both high infestation years (2007 and 2009), while natural control (prey/predator ratio and parasitism rate) was more efficient in strips in 2009 and 2010. Land equivalent ratio (LER), an indicator of yield production was higher in 18m strips than in control plots. Strip cropping could be envisaged as an effective managing tool against soybean aphid in North America.

Evaluation of the demographic potential of Aphelinus albipodus (Hymenoptera: Aphelinidae) with Aphis glycines (Homoptera: Aphididae) as alternate host at various temperatures

Aphelinus albipodus Hayat and Fatima (Hymenoptera: Aphelinidae) is a parasitoid wasp that uses aphids as hosts and is a candidate for biological control of aphids that infest commercially important crops. To determine the ideal conditions for large-scale reproduction of A. albipodus, a leaf disc method was used to compare the life history of A. albipodus parasitizing Aphis glycines L. (Homoptera: Aphididae) at 20, 24, 28 and 32 °C. The results were analyzed using the age-stage, two-sex life table and showed that the developmental duration and longevity of A. albipodus decreased significantly with increasing temperature. The mean generation time (T) also decreased as the temperature increased. In contrast, the intrinsic rate of increase (r) of A. albipodus increased with rising temperatures. The net reproductive rate (R 0) showed a more complicated pattern, first increasing in higher temperatures and then dropping off at the highest temperature. We employed bootstrap techniques for estimating the variance and standard error of the population parameters. The r increased significantly as the temperature increased, and R 0 at 28 °C was significantly higher than at 32 °C. Overall, our results showed that 28 °C was the most suitable temperature for reproduction of A. albipodus with A. glycines as the host.

Identification of single nucleotide polymorphisms in soybean associated with resistance to common cutworm (Spodoptera litura Fabricius)

Common cutworm (CCW; Spodoptera litura Fabricius) is a major leaf-eating insect that affects soybean crops in central and southern China. Understanding CCW-associated traits in soybean will provide insights for improved breeding strategies for resistance. The purpose of this study was to explore the genetic mechanisms underlying resistance to CCW. In this study, one natural population consisting of 219 soybean landraces from a wide geographic range was employed. Three traits, namely larval weight (LW), duration of larval stage (DLS) and pupal weight (PW) were evaluated as indicators for CCW resistance. Using 1536 single nucleotide polymorphisms (SNPs), a genome-wide association analysis was conducted to identify genomic regions associated with LW, DLS and PW in this natural population. Seven SNP-trait associations were identified using a mixed linear model (MLM). Four SNPs were co-associated with two traits. Three loci were significantly associated with CCW-resistance. Most of the detected loci were located within genomic regions previously identified as quantitative trait loci (QTLs) for these traits. The region on chromosome 6, which co-associated with LW and DLS, included several QTLs for reaction to disease or insect, such as Fusarium virguliforme, corn earworm and bean pyralid. On chromosome 7, two SNPs have been reported to associate with CCW, corn earworms, soybean aphid and bean pyralid moth infestations. Two putative genes (MYC2-like and JAM2-like) on chromosome 7 that may be associated with resistance to CCW were identified. These markers, located in previously reported QTLs, are consistent with previous findings and may represent important targets for the identification of CCW resistance-related genes. These results may provide a profound understanding of the genetic basis for resistance to CCW in soybean and the foundation for resistance to biotic stress through marker-assisted selection breeding strategies for CCW.

Stress-induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid.

Bacterial endosymbionts can drive evolutionary novelty by conferring adaptive benefits under adverse environmental conditions. Among aphid species there is growing evidence that symbionts influence tolerance to various forms of stress. However, the extent to which stress inflicted on the aphid host has cascading effects on symbiont community dynamics remains poorly understood. Here we simultaneously quantified the effect of host-plant induced and xenobiotic stress on soybean aphid (Aphis glycines) fitness and relative abundance of its three bacterial symbionts. Exposure to soybean defensive stress (Rag1 gene) and a neurotoxic insecticide (thiamethoxam) substantially reduced aphid composite fitness (survival×reproduction) by 74±10% and 92±2%, respectively, which in turn induced distinctive changes in the endosymbiont microbiota. When challenged by host-plant defenses a 1.4-fold reduction in abundance of the obligate symbiont Buchnera was observed across four aphid clonal lines. Among facultative symbionts of Rag1-stressed aphids, Wolbachia abundance increased twofold and Arsenophonus decreased 1.5-fold. A similar pattern was observed under xenobiotic stress, with Buchnera and Arsenophonus titers decreasing (1.3-fold) and Wolbachia increasing (1.5-fold). Furthermore, variation in aphid virulence to Rag1 was positively correlated with changes in Arsenophonus titers, but not Wolbachia or Buchnera. A single Arsenophonus multi-locus genotype was found among aphid clonal lines, indicating strain diversity is not primarily responsible for correlated host-symbiont stress levels. Overall, our results demonstrate the nature of aphid symbioses can significantly affect the outcome of interactions under stress and suggests general changes in the microbiome can occur across multiple stress types.