European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America

We consider the possibility of an extensive invasional meltdown occurring in central North America involving eleven Eurasian species. The scenario begins with the potential co-facilitation between the European earthworm Lumbricus terrestris and European buckthorn, Rhamnus cathartica. Once introduced, European buckthorn has served as the overwintering host for two important invasive crop pests, oat crown rust, Puccinea coronata and the soybean aphid, Aphis glycines. The spread of R. cathartica itself may have been aided by seed dispersal by the European starling, Sturnus vulgaris, and the presence of L. terrestris has likely facilitated the invasion of Bipalium adventitium, an Asian predatory flatworm that specializes on earthworms. Beyond this, the soybean aphid is consumed by a number of introduced species, including the lady beetle Harmonia axyridis, the ground beetle Agonum muelleri and the parasitoid Aphelinus certus. We hypothesize that the presence of soybean aphid increases regional abundances of these species. We discuss both the evidence for this multi-species invasional meltdown scenario and potential implications of meltdown dynamics for invasive species management. The particular management issues that we discuss are: (1) opportunities for managing multiple invasive species simultaneously by targeting facilitator species, and (2) implications of meltdown dynamics for biological control introductions against the soybean aphid.     

Effect of parasitism on flight behavior of the soybean aphid, Aphis glycines

Many aphid species possess wingless (apterous) and winged (alate) stages, both of which can harbor parasitoids at various developmental stages. Alates can either be parasitized directly or can bear parasitoids eggs or larvae resulting from prior parasitism of alatoid nymphs. Winged aphids bearing parasitoid eggs or young larvae eventually still engage in long-distance flights, thereby facilitating parasitoid dispersal. This may have a number of important implications for biological control of aphids by parasitoids. In this study, we determined the effect of parasitism by Aphelinus varipes (Hymenoptera: Aphelinidae) on wing development and flight of the soybean aphid, Aphis glycines (Hemiptera: Aphididae). We also quantified the influence of aphid flight distance on subsequent A. varipes development. Parasitism by A. varipes was allowed at different A. glycines developmental stages (i.e., alatoid 3rd and 4th-instar nymphs, alates) and subsequent aphid flight was measured using a computer-monitored flight mill. Only 35% of aphids parasitized as L3 alatoid nymphs produced normal winged adults compared to 100% of L4 alatoids. Flight performance of aphids parasitized as 4th-instar alatoid nymphs 24 or 48 h prior to testing was similar to that of un-parasitized alates of identical age, but declined sharply for alates that had been parasitized as 4th-instar alatoid nymphs 72 and 96 h prior to testing. Flight performance of aphids parasitized as alate adults for 24 h was not significantly different from un-parasitized alates of comparable ages. Flight distance did not affect parasitoid larval or pupal development times, or the percent mummification of parasitized aphids. Our results have implications for natural biological control of A. glycines in Asia and classical biological control of the soybean aphid in North America.     

Characterization and genetics of multiple soybean aphid biotype resistance in five soybean plant introductions

Key message

Five soybean plant introductions expressed antibiosis resistance to multiple soybean aphid biotypes. Two introductions had resistance genes located in the Rag1, Rag2, and Rag3 regions; one introduction had resistance genes located in the Rag1, Rag2, and rag4 regions; one introduction had resistance genes located in the Rag1 and Rag2 regions; and one introduction had a resistance gene located in the Rag2 region.

Abstract

Soybean aphid (Aphis glycines Matsumura) is the most important soybean [Glycine max (L.) Merr.] insect pest in the USA. The objectives of this study were to characterize the resistance expressed in five plant introductions (PIs) to four soybean aphid biotypes, determine the mode of resistance inheritance, and identify markers associated with genes controlling resistance in these accessions. Five soybean PIs, from an initial set of 3000 PIs, were tested for resistance against soybean aphid biotypes 1, 2, 3, and 4 in choice and no-choice tests. Of these five PIs, PI 587663, PI 587677, and PI 587685 expressed antibiosis against all four biotypes, while PI 587972 and PI 594592 expressed antibiosis against biotypes 1, 2, and 3. F₂ populations derived from PI 587663 and PI 587972 were evaluated for resistance against soybean aphid biotype 1, and populations derived from PIs 587677, 587685, and 594592 were tested against biotype 3. In addition, F_2:3 plants were tested against biotypes 2 and 3. Genomic DNA from F₂ plants was screened with markers linked to Rag1, Rag2, Rag3, and rag4 soybean aphid-resistance genes. Results showed that PI 587663 and PI 594592 each had three genes with variable gene action located in the Rag1, Rag2, and Rag3 regions. PI 587677 had three genes with variable gene action located in the Rag1, Rag2 and rag4 regions. PI 587685 had one dominant gene located in the Rag1 region and an additive gene in the Rag2 region. PI 587972 had one dominant gene located in the Rag2 region controlling antixenosis- or antibiosis-type resistance to soybean aphid biotypes 1, 2, or 3. PIs 587663, 587677, and 587685 also showed antibiosis-type resistance against biotype 4. Information on multi-biotype aphid resistance and resistance gene markers will be useful for improving soybean aphid resistance in commercial soybean cultivars.

     

Inheritance of soybean aphid resistance in 21 soybean plant introductions

Key Message

The Rag2 region was frequently identified among 21 F ₂ populations evaluated for soybean aphid resistance, and dominant gene action and single-gene resistance were also commonly identified.

Abstract

The soybean aphid [Aphis glycines Matsumura (Hemiptera: Aphididae)] is one of the most important insect pests of soybean [Glycine max (L.) Merr] in the northern USA and southern Canada, and four resistance loci (Rag1–rag4) have been discovered since the pest was identified in the USA in 2000. The objective of this research was to determine whether resistance expression in recently identified soybean aphid-resistant plant introductions (PIs) was associated with the four Rag loci using a collection of 21 F₂ populations. The F₂ populations were phenotyped with soybean aphid biotype 1, which is avirulent on plants having any of the currently identified Rag genes, using choice tests in the greenhouse and were tested with genetic markers linked to the four Rag loci. The phenotyping results indicate that soybean aphid resistance is controlled by a single dominant gene in 14 PIs, by two genes in three PIs, and four PIs had no clear Mendelian inheritance patterns. Genetic markers flanking Rag2 were significantly associated with aphid resistance in 20 PIs, the Rag1 region was significantly identified in five PIs, and the Rag3 region was identified in one PI. These results show that single dominant gene action at the Rag2 region may be a major source for aphid resistance in the USDA soybean germplasm collection.     

The Endosymbiont Arsenophonus Is Widespread in Soybean Aphid,Aphis glycines,but Does Not Provide Protection from Parasitoids or a Fungal Pathogen

Aphids commonly harbor bacterial facultative symbionts that have a variety of effects upon their aphid hosts, including defense against hymenopteran parasitoids and fungal pathogens. The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is infected with the symbiont Arsenophonus sp., which has an unknown role in its aphid host. Our research goals were to document the infection frequency and diversity of the symbiont in field-collected soybean aphids, and to determine whether Arsenophonus is defending soybean aphid against natural enemies. We performed diagnostic PCR and sequenced four Arsenophonus genes in soybean aphids from their native and introduced range to estimate infection frequency and genetic diversity, and found that Arsenophonus infection is highly prevalent and genetically uniform. To evaluate the defensive role of Arsenophonus, we cured two aphid genotypes of their natural Arsenophonus infection through ampicillin microinjection, resulting in infected and uninfected isolines within the same genetic background. These isolines were subjected to parasitoid assays using a recently introduced biological control agent, Binodoxys communis [Braconidae], a naturally recruited parasitoid, Aphelinus certus [Aphelinidae], and a commercially available biological control agent, Aphidius colemani [Braconidae]. We also assayed the effect of the common aphid fungal pathogen, Pandora neoaphidis (Remaudiere & Hennebert) Humber (Entomophthorales: Entomophthoraceae), on the same aphid isolines. We did not find differences in successful parasitism for any of the parasitoid species, nor did we find differences in P. neoaphidis infection between our treatments. Our conclusion is that Arsenophonus does not defend its soybean aphid host against these major parasitoid and fungal natural enemies.     

Intraguild predation of the aphid parasitoid Aphelinus certus by Coccinella septempunctata and Harmonia axyridis

Coincidental intraguild predation is expected to be less disruptive to biological control than omnivorous intraguild predation, and strong intraguild predation is not expected to occur in natural systems. Coincidental intraguild predation in a foodweb involving introduced pest and natural enemy species was examined to determine whether intraguild predation would be disruptive of biological control services in soybean agroecosystems. Introduced natural enemies are important regulators of soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), populations in North America. Seven-spotted lady beetles, Coccinella septempunctata L., and multicolored Asian lady beetles, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), are key predators of soybean aphid in North America while the chalcidoid wasp, Aphelinus certus Yasnosh (Hymenoptera: Aphelinidae), is the most common parasitoid of soybean aphid in Ontario, Canada. Predation of parasitized soybean aphids at two stages (newly parasitized aphids and mummified aphids) by adults and third instar larvae of both C. septempunctata and H. axyridis was examined in laboratory experiments. In choice experiments, all stages of lady beetles preferred non-parasitized aphids over mummified aphids. In cage experiments, third instar larvae and male and female adults of both lady beetles did not discriminate between newly parasitized and non-parasitized aphids. The influence of coincidental intraguild predation on the efficacy of parasitoids as biological control agents, and implications for soybean aphid management decisions based on natural enemies, are discussed.     

Performance and prospects of Rag genes for management of soybean aphid

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is an invasive insect pest of soybean [Glycine max (L.) Merr. (Fabaceae)] in North America, and it has led to extensive insecticide use in northern soybean‐growing regions there. Host plant resistance is one potential alternative strategy for managing soybean aphid. Several Rag genes that show antibiosis and antixenosis to soybean aphid have been recently identified in soybean, and field‐testing and commercial release of resistant soybean lines have followed. In this article, we review results of field tests with soybean lines containing Rag genes in North America, then present results from a coordinated regional test across several field sites in the north‐central USA, and finally discuss prospects for use of Rag genes to manage soybean aphids. Field tests conducted independently at multiple sites showed that soybean aphid populations peaked in late summer on lines with Rag1 or Rag2 and reached economically injurious levels on susceptible lines, whereas lines with a pyramid of Rag1 + Rag2 held soybean aphid populations below economic levels. In the regional test, aphid populations were generally suppressed by lines containing one of the Rag genes. Aphids reached putative economic levels on Rag1 lines for some site years, but yield loss was moderated, indicating that Rag1 may confer tolerance to soybean aphid in addition to antibiosis and antixenosis. Moreover, no yield penalty has been found for lines with Rag1, Rag2, or pyramids. Results suggest that use of aphid‐resistant soybean lines with Rag genes may be viable for managing soybean aphids. However, virulent biotypes of soybean aphid were identified before release of aphid‐resistant soybean, and thus a strategy for optimal deployment of aphid‐resistant soybean is needed to ensure sustainability of this technology.     

Pyramiding different aphid-resistance genes in elite soybean germplasm to combat dynamic aphid populations

The soybean aphid (Aphis glycines Matsumura), an invasive species, has posed a significant threat to soybean [Glycine max (L.) Merr.] production in North America since 2001. Use of resistant cultivars is an effective tactic to protect soybean yield. However, the variability and dynamics of aphid populations could limit the effectiveness of host-resistance gene(s). Gene pyramiding is a promising way to sustain host-plant resistance. The objectives of this study were to determine the prevalent aphid biotypes in Michigan and to assess the effectiveness of different combinations of aphid-resistance genes. A total of 11 soybean genotypes with known resistance gene(s) were used as indicator lines. Based on their responses, Biotype 3 was a major component of Michigan aphid populations during 2015–2016. The different performance of Rag-“Jackson” and Rag1-“Dowling” along with the breakdown of resistance in plant introductions (PIs) 567301B and 567324 may be explained by Biotype 3 or an unknown virulent biotype establishing in Michigan. With the assistance of flanking markers, 12 advanced breeding lines carrying different aphid-resistance gene(s) were developed and evaluated for effectiveness in five trials across 2015 to 2017. Lines with rag1c, Rag3d, Rag6, Rag3c?+?Rag6, rag1b?+?rag3, rag1c?+?rag4, rag1c?+?rag3?+?rag4, rag1c?+?Rag2?+?rag3?+?rag4, and rag1b?+?rag1c?+?rag3?+?rag4 demonstrated strong and consistent resistance. Due to the variability of virulent aphid populations, different combinations of Rag genes may perform differently across geographies. However, advanced breeding lines pyramided with three or four Rag genes likely will provide broader and more durable resistance to diverse and dynamic aphid populations.     

Soybean aphid intrabiotype variability based on colonization of specific soybean genotypes

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is one of the most destructive insect pests on soybeans in the United States. One method for managing this pest is through host plant resistance. Since its arrival in 2000, 4 aphid biotypes have been identified that are able to overcome soybean aphid resistance (Rag) genes. A soybean aphid isolate collected from Moline, Illinois readily colonized soybean plants with the soybean aphid resistance gene Rag2, unlike biotypes 1 and 2, but similar to soybean aphid biotype 3. Two no‐choice experiments compared the virulence of the Moline isolate with biotype 3. In both experiments, differences in aphid population counts were not significant (P > 0.05) on soybean genotypes LD08–12957a (Rag2) and LD11–5413a (Rag2), but the aphid counts for the Moline isolate were significantly (P < 0.05) lower than the aphid counts for the biotype 3 isolate on the soybean genotypes Dowling (Rag1), LD05–16611 (Rag1), LD11–4576a (Rag1), and PI 567598B (rag1b and rag3). The Moline isolate was a variant of aphid biotype 3, which is the first report showing that soybean aphid isolates classified as the same biotype, based on virulence against specific Rag genes, can differ in aggressiveness or ability to colonize specific host genotypes.     

Parasitoid spectrum (Hymenoptera: Braconidae; Aphelinidae) of the soybean aphid Aphis glycines (Homoptera: Aphididae) in Japan and Indonesia (Java and Bali)

Aphidiine and aphelinid parasitoids collected from the soybean aphid, Aphis glycines, on Glycine max in Japan and Indonesia (Java and Bali) were identified to clarify the parasitoid spectrum of the aphid there. Nine parasitoid species from Japan (Aphidiinae: Aphidius gifuensis, Aphidius sp., Binodoxys communis, Diaeretiella rapae, Lipolexis gracilis, Lysiphlebia japonica; Aphelinidae: Aphelinus asychis, A. gossypii, A. varipes) and two parasitoid species from Indonesia (B. communis, A. gossypii) were found to be associated with A. glycines.     

Seasonal abundance of resident parasitoids and predatory flies and corresponding soybean aphid densities, with comments on classical biological control of soybean aphid in the Midwest

Seasonal abundance of resident parasitoids and predatory flies, and corresponding soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), densities were assessed in soybean fields from 2003 to 2006 at two locations in lower Michigan. Six parasitoid and nine predatory fly species were detected in 4 yr by using potted plants infested with soybean aphid placed in soybean fields. The parasitoid Lysiphlebus testaceipes Cresson (Hymenoptera: Braconidae) and the predatory flies Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae), and Allograpta obliqua Say (Diptera: Syrphidae) were most numerous. Generally, L. testaceipes was more abundant late in the soybean growing season, but it also occurred during soybean vegetative growth; A. obliqua was more abundant during vegetative growth; and A. aphidimyza was common throughout the season. Soybean plants were visually inspected to estimate densities of soybean aphid, mummified aphids, and immature predatory flies. From 2003 to 2006, parasitism rates were inversely correlated with aphid density: percentage of parasitism was always very low (< or = 0.1%) at high aphid densities (> 100 aphids per plant), and higher parasitism, up to 17%, was observed at very low aphid densities (< 1 aphid per plant). Populations of immature predatory flies, particularly A. aphidimyza, generally increased in soybean fields with increasing soybean aphid populations, but aphids always outnumbered immature flies by 100-21,000-fold when flies were detected. Rearing field-collected aphid in 2006 substantiated that parasitism varied widely, with parasitism in most cases < 10%. Based on findings of low parasitism and predation, positive response to changing aphid densities by predatory flies but not parasitoids, early season abundance primarily of predatory flies, and past findings on these taxa's diversity and abundance, we discuss the potential use of exotic parasitoids and predatory flies to enhance soybean aphid biological control.     

Identification and molecular mapping of two soybean aphid resistance genes in soybean PI 587732

Soybean [Glycine max (L.) Merr.] continues to be plagued by the soybean aphid (Aphis glycines Matsumura: SA) in North America. New soybean resistance sources are needed to combat the four identified SA biotypes. The objectives of this study were to determine the inheritance of SA resistance in PI 587732 and to map resistance gene(s). For this study, 323 F₂ and 214 F₃ plants developed from crossing PI 587732 to two susceptible genotypes were challenged with three SA biotypes and evaluated with genetic markers. Choice tests showed that resistance to SA Biotype 1 in the first F₂ population was controlled by a gene in the Rag1 region on chromosome 7, while resistance to SA Biotype 2 in the second population was controlled by a gene in the Rag2 region on chromosome 13. When 134 F₃ plants segregating in both the Rag1 and Rag2 regions were tested with a 1:1 mixture of SA Biotypes 1 and 2, the Rag2 region and an interaction between the Rag1 and Rag2 regions were significantly associated with the resistance. Based on the results of the non-choice tests, the resistance gene in the Rag1 region in PI 587732 may be a different allele or gene from Rag1 from Dowling because the PI 587732 gene showed antibiosis type resistance to SA Biotype 2 while Rag1 from Dowling did not. The two SA resistance loci and genetic marker information from this study will be useful in increasing diversity of SA resistance sources and marker-assisted selection for soybean breeding programs.     

Combined effects of host-plant resistance and intraguild predation on the soybean aphid parasitoid Binodoxys communis in the field

Soybean varieties that exhibit resistance to the soybean aphid Aphis glycines have been developed for use in North America. In principle, host-plant resistance to soybean aphid can influence the interactions between the soybean aphid and its natural enemies. Resistance could change the quality of soybean aphids as a food source, the availability of soybean aphids, or resistance traits could directly affect aphid predators and parasitoids. Here, we focus on the effect of soybean aphid resistance on the interactions between soybean aphids, the parasitoid Binodoxys communis (Hymenoptera: Braconidae), and predators of these two species. We determined whether host-plant resistance affected within-season persistence of B. communis by releasing parasitoids into resistant and susceptible soybean plots. We observed higher B. communis densities in susceptible soybean plots than in resistant plots. There were also higher overall levels of intraguild predation of B. communis in susceptible plots, although the per-capita risk of intraguild predation of B. communis was affected neither by plant genotype nor by aphid density. We discuss these effects and whether they were caused by direct effects of the resistant plants on B. communis or indirect effects through soybean aphid or predators.     

Impact of Rag1 aphid resistant soybeans on Binodoxys communis (Hymenoptera: Braconidae), a parasitoid of soybean aphid (Hemiptera: Aphididae)

Multiple strategies are being developed for pest management of the soybean aphid, Aphis glycines Matsumura; however, there has been little published research thus far to determine how such strategies may influence each other, thereby complicating their potential effectiveness. A susceptible soybean (Glycine max L.) variety without the Rag1 gene and a near isogenic resistant soybean variety with the Rag1 gene were evaluated in the laboratory for their effects on the fitness of the soybean aphid parasitoid, Binodoxys communis (Gahan). The presence or absence of the Rag1 gene was verified by quantifying soybean aphid growth. To test for fitness effects, parasitoids were allowed to attack soybean aphids on either a susceptible or resistant plant for 24 h and then aphids were kept on the same plant throughout parasitoid development. Parasitoid fitness was measured by mummy and adult parasitoid production, adult parasitoid emergence, development time, and adult size. Parasitoids that attacked soybean aphids on susceptible plants produced more mummies, more adult parasitoids, and had a higher emergence rate compared with those on resistant plants. Adult parasitoids that emerged from resistant plants took 1 d longer and were smaller compared with those from susceptible plants. This study suggests that biological control by B. communis may be compromised when host plant resistance is widely used for pest management of soybean aphids.     

Mapping and validation of a gene for soybean aphid resistance in PI 567537

The soybean aphid (Aphis glycines Matsumura) is a major pest on soybean [Glycine max (L.) Merr.] in North America. Aphid resistance has been found on plant introduction (PI) 567537, but its genetic characterization is unknown. The objectives of this study were to identify the resistance genes in PI 567537 using molecular markers and validate them in a different genetic background. A mapping population of 86 F4 lines from a cross between PI 567537 and a susceptible parent E00003 was investigated for aphid resistance in both greenhouse and field trials. A genomic region associated with the aphid resistance in PI 567537 was revealed on chromosome 16 (linkage group J) with molecular markers. This locus was coincidently located in the same region as Rag3 and explained most of the phenotypic variation, ranging from 87.4 % in the greenhouse trial to 78.9 % in the field trial. This resistance gene was further confirmed in an F2 population derived from a cross of PI 567537 × Skylla. The segregation of the F2 population indicated that the aphid resistance in PI 567537 was most likely controlled by a single dominant gene, which was the one we mapped in the F4-derived population. This gene was designated Rag3b since it is located in the same region as Rag3. The mapping of the aphid resistance gene in PI 567537 could be useful in marker-assisted selection when employing PI 567537 as an aphid resistance source.     

Fine mapping the soybean aphid resistance gene Rag1 in soybean

The soybean aphid (Aphis glycines Matsumura) is an important soybean [Glycine max (L.) Merr.] pest in North America. The dominant aphid resistance gene Rag1 was previously mapped from the cultivar ‘Dowling’ to a 12 cM marker interval on soybean chromosome 7 (formerly linkage group M). The development of additional genetic markers mapping closer to Rag1 was needed to accurately position the gene to improve the effectiveness of marker-assisted selection (MAS) and to eventually clone it. The objectives of this study were to identify single nucleotide polymorphisms (SNPs) near Rag1 and to position these SNPs relative to Rag1. To generate a fine map of the Rag1 interval, 824 BC₄F₂ and 1,000 BC₄F₃ plants segregating for the gene were screened with markers flanking Rag1. Plants with recombination events close to the gene were tested with SNPs identified in previous studies along with new SNPs identified from the preliminary Williams 82 draft soybean genome shotgun sequence using direct re-sequencing and gene-scanning melt-curve analysis. Progeny of these recombinant plants were evaluated for aphid resistance. These efforts resulted in the mapping of Rag1 between the two SNP markers 46169.7 and 21A, which corresponds to a physical distance on the Williams 82 8× draft assembly (Glyma1.01) of 115 kilobase pair (kb). Several candidate genes for Rag1 are present within the 115-kb interval. The markers identified in this study that are closely linked to Rag1 will be a useful resource in MAS for this important aphid resistance gene.     

Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M

The soybean aphid [Aphis glycines Matsumura] is an important pest of soybean [Glycine max (L.) Merr.] in North America. Single dominant genes in the cultivars ‘Dowling’ and ‘Jackson’ control resistance to the soybean aphid. The gene in Dowling was named Rag1, and the genetic relationship between Rag1 and the gene in Jackson is not known. The objectives of this study were to map the locations of Rag1 and the Jackson gene onto the soybean genetic map. Segregation of aphid resistance and simple sequence repeat (SSR) markers in F _2:3 populations developed from crosses between Dowling and the two susceptible soybean cultivars ‘Loda’ and ‘Williams 82’, and between Jackson and Loda, were analyzed. Both Rag1 and the Jackson gene segregated 1:2:1 in the F _2:3 populations and mapped to soybean linkage group M between the markers Satt435 and Satt463. Rag1 mapped 4.2 cM from Satt435 and 7.9 cM from Satt463. The Jackson gene mapped 2.1 cM from Satt435 and 8.2 cM from Satt463. Further tests to determine genetic allelism between Rag1 and the Jackson gene are in progress. The SSR markers flanking these resistance genes are being used in marker-assisted selection for aphid resistance in soybean breeding programs. Trade and manufacturers’ names are necessary to report factually on available data; however, the USDA neither guarantees nor warrants the standard of the product, and the use of the name by USDA implies no approval of the product to the exclusion of others that may also be suitable.     

Impacts of thiamethoxam seed treatment and host plant resistance on the soybean aphid fungal pathogen, Pandora neoaphidis

Since the introduction of soybean aphid, Aphis glycines Matsumura, from Asia, insecticide use in soybean has increased substantially in the north central United States. Insecticide seed treatments and aphid resistant soybean varieties are management tactics that may reduce reliance on foliar applications of broad-spectrum insecticides. Exploring potential nontarget impacts of these technologies will be an important step in incorporating them into aphid management programs. We investigated impacts of thiamethoxam seed treatment and Rag1 aphid resistant soybean on a fungal pathogen of soybean aphid, Pandora neoaphidis (Remaudière & Hennebert) Humber, via open plot and cage studies. We found that although thiamethoxam seed treatment did significantly lower aphid pressure in open plots compared with an untreated control, this reduction in aphid density translated into nonsignificant decreases in fungal disease prevalence in aphids. Furthermore, when aphid densities were approximately equal in seed treated and untreated soybean, no impact on aphid fungal disease was observed. In open plots, Rag1 resistant soybean experienced lower aphid pressure and aphid disease prevalence compared with a nonresistant isoline. However, in cages when aphid densities were equivalent in both resistant and susceptible soybean, resistance had no impact on aphid disease prevalence. The addition of thiamethoxam seed treatment to resistant soybean yielded aphid densities and aphid disease prevalence similar to untreated, resistant soybean. These studies provide evidence that thiamethoxam seed treatments and Rag1 resistance can impact P. neoaphidis via decreased aphid densities; however, this impact is minimal, implying use of seed treatments and host plant resistance are compatible with P. neoaphidis.     

Mapping novel aphid resistance QTL from wild soybean, <Emphasis Type="Italic">Glycine soja</Emphasis> 85-32

Key message

Two novel QTLs conferring aphid resistance were mapped and validated on soybean chromosomes 8 and 16, respectively. Closely linked markers were developed to assist breeding for aphid resistance.

Abstract

Soybean aphid, Aphis glycines Matsumura, is a highly destructive pest for soybean production. E08934, a soybean advanced breeding line derived from the wild soybean Glycine soja 85-32, has shown strong resistance to aphids. To dissect the genetic basis of aphid resistance in E08934, a mapping population (070020) consisting of 140 F₃-derived lines was developed by crossing E08934 with an aphid-susceptible line E00003. This mapping population was evaluated for aphid resistance in a greenhouse trial in 2010 and three field trials in 2009, 2010, and 2011, respectively. The broad-sense heritability across the field trials was 0.84. In the mapping population 070020, two major quantitative trait loci (QTL) were detected as significantly associated with aphid resistance, and designated as Rag6 and Rag3c, respectively. Rag6 was mapped to a 10.5 centiMorgan (cM) interval between markers MSUSNP08-2 and Satt209 on chromosome 8, explaining 19.5–46.4% of the phenotypic variance in different trials. Rag3c was located at a 7.5 cM interval between markers MSUSNP16-10 and Sat_370 on chromosome 16, explaining 12.5–22.9% of the phenotypic variance in different trials. Rag3c had less resistance effect than Rag6 across all the trials. Furthermore, Rag6 and Rag3c were confirmed in two validation populations with different genetic backgrounds. No significant interaction was detected between Rag6 and Rag3c in either the mapping population or the validation populations. Both Rag6 and Rag3c were indicated as conferring antibiosis resistance to aphids by a no-choice test. The new aphid-resistance gene(s) derived from the wild germplasm G. soja 85-32 are valuable in improving soybeans for aphid resistance.

     

Compatibility of aphid resistance in soybean and biological control by the parasitoid Aphidius colemani (Hymenoptera: Braconidae)

Biological control and soybean cultivars bred for increased resistance to the soybean aphid (Aphis glycines) are two approaches used to manage this serious pest of soybeans in North America. However, as with many other pest systems, the compatibility of these two pest management approaches has not been studied in detail. The aphidiine wasp Aphidius colemani is one of several candidate species for biological control of the soybean aphid in soybean in North America. Resistance to the soybean aphid in the USDA soybean cultivar Dowling is largely controlled by a single dominant gene Rag1, which is the focus of plant breeding programs directed against the soybean aphid. In this study, we measured developmental and behavioral differences in the parasitic wasp A. colemani when it attacked soybean aphids feeding on either the aphid-resistant Dowling or aphid-susceptible Glenwood cultivars of soybean. We used a combination of choice and no-choice experiments to examine the effects of host plant cultivar on the number of parasitized aphids formed and the sex ratio and body weights of adult offspring produced. Significantly more aphids were parasitized when they fed on Glenwood compared to Dowling and these offspring were larger when they developed in aphids that fed on Glenwood soybeans. To distinguish between effects on foraging decisions and offspring survivorship, we conducted an additional experiment that followed the oviposition decisions and fate of each parasitized aphid. Foraging female A. colemani spent less time handling individual aphids and encountered and attacked aphids at a higher rate when they fed on aphids feeding on Glenwood soybeans than aphids feeding on Dowling soybeans. Furthermore, wasp survivorship in aphids was greater on Glenwood than Dowling. Taken together, aphid-resistance in soybeans has negative effects on foraging behavior and offspring fitness of A. colemani raising concerns about the compatibility of these two pest management approaches.