Precipitation change accentuates or reverses temperature effects on aphid dispersal.

Global temperatures are generally increasing, and this is leading to a well documented advancement and extension of seasonal activity of many pest insects. Effects of changing precipitation have received less attention, but might be complex because rain and snow are increasing in some places but decreasing in others. This raises the possibility that altered precipitation could accentuate, or even reverse, the effects of rising temperatures on pest outbreaks. We used >592 K aphid suction-trap captures over 15 years, in the heavily farmed central USA, to examine how the activity of Aphis glycines (soybean aphid), Rhopalosiphum maidis (corn aphid), and Rhopalosiphum padi (bird cherry-oat aphid) changed with variation in both temperature and precipitation. Increasing precipitation caused late-season flight activity of A. glycines and early-season activity of R. padi to shift earlier, while increasing temperature did the same for early-season activity of A. glycines and R. maidis. In these cases, precipitation and temperature exhibited directionally similar, but independent, effects. However, precipitation sometimes mediated temperature effects in complex ways. At relatively low temperatures, greater precipitation generally caused late-season flights of R. maidis to occur earlier. However, this pattern was reversed at higher temperatures with precipitation delaying late-season activity. In contrast, greater precipitation delayed peak flights of R. padi at lower temperatures, but caused them to occur earlier at higher temperatures. So, in these two cases the interactive effects of precipitation on temperature were mirror images of one another. When projecting future aphid flight phenology, models that excluded precipitation covariates consistently underpredicted the degree of phenological advance for A. glycines and R. padi, and underpredicted the degree of phenological delay for R. maidis under expected future climates. Overall, we found broad evidence that changing patterns of aphid flight phenology could only be understood by considering both temperature and precipitation changes. In our study region, temperature and precipitation are expected to increase in tandem, but these correlations will be reversed elsewhere. This reinforces the need to include both main and interactive effects of precipitation and temperature when seeking to accurately predict how pest pressure will change with a changing climate.

Complex life histories predispose aphids to recent abundance declines.

Many animals change feeding habits as they progress through life stages, exploiting resources that vary in space and time. However, complex life histories may bring new risks if rapid environmental change disrupts the timing of these switches. Here, we use abundance times series for a diverse group of herbivorous insects, aphids, to search for trait and environmental characteristics associated with declines. Our meta dataset spanned three world regions and >300 aphid species, tracked at 75 individual sites for 10-50 years. Abundances were generally falling, with median changes of -8.3%, -5.6%, and -0.1% per year in the central USA, northwestern USA, and United Kingdom, respectively. Aphids that obligately alternated between host plants annually and those that were agricultural pests exhibited the steepest declines, relative to species able to persist on the same host plant year-round or those in natural areas. This suggests that host alternation might expose aphids to climate-induced phenology mismatches with one or more of their host plant species, with additional risks from exposure to insecticides and other management efforts. Warming temperatures through time were associated with milder aphid declines or even abundance increases, particularly at higher latitudes. Altogether, while a warming world appeared to benefit some aphid species in some places, most aphid species that had time-sensitive movements among multiple host plants seemed to face greater risk of decline. More generally, this suggests that recent human-induced rapid environmental change is rebalancing the risks and rewards associated with complex life histories.

Soybean aphid biotype 1 genome: Insights into the invasive biology and adaptive evolution of a major agricultural pest.

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) is a serious pest of the soybean plant, Glycine max, a major world-wide agricultural crop. We assembled a de novo genome sequence of Ap. glycines Biotype 1, from a culture established shortly after this species invaded North America. 20.4% of the Ap. glycines proteome is duplicated. These in-paralogs are enriched with Gene Ontology (GO) categories mostly related to apoptosis, a possible adaptation to plant chemistry and other environmental stressors. Approximately one-third of these genes show parallel duplication in other aphids. But Ap. gossypii, its closest related species, has the lowest number of these duplicated genes. An Illumina GoldenGate assay of 2380 SNPs was used to determine the world-wide population structure of Ap. Glycines. China and South Korean aphids are the closest to those in North America. China is the likely origin of other Asian aphid populations. The most distantly related aphids to those in North America are from Australia. The diversity of Ap. glycines in North America has decreased over time since its arrival. The genetic diversity of Ap. glycines North American population sampled shortly after its first detection in 2001 up to 2012 does not appear to correlate with geography. However, aphids collected on soybean Rag experimental varieties in Minnesota (MN), Iowa (IA), and Wisconsin (WI), closer to high density Rhamnus cathartica stands, appear to have higher capacity to colonize resistant soybean plants than aphids sampled in Ohio (OH), North Dakota (ND), and South Dakota (SD). Samples from the former states have SNP alleles with high FST values and frequencies, that overlap with genes involved in iron metabolism, a crucial metabolic pathway that may be affected by the Rag-associated soybean plant response. The Ap. glycines Biotype 1 genome will provide needed information for future analyses of mechanisms of aphid virulence and pesticide resistance as well as facilitate comparative analyses between aphids with differing natural history and host plant range.

Factors Affecting Population Dynamics of Thrips Vectors of Soybean vein necrosis virus.

Thrips-infesting soybeans were considered of minor economic importance, but recent evidence of their ability to transmit a newly identified soybean virus, Soybean vein necrosis virus (SVNV), has raised their profile as pests. Season-long surveys were conducted using suction traps to determine the effects of temperature and precipitation on the spatiotemporal patterns of three vector species of SVNV, Neohydatothrips variabilis (Beach) (Thysanoptera: Thripidae) (soybean thrips), Frankliniella tritici (Fitch) (Thysanoptera: Thripidae) (eastern flower thrips), and Frankliniella fusca (Hinds) (Thysanoptera: Thripidae) (tobacco thrips) in soybean fields in Indiana in 2013 and 2014. In addition, soybean fields were surveyed for presence of SVNV in both years. We found that the magnitude and timing of thrips activity varied greatly for the three species. N. variabilis activity peaked in mid-August each year. The peak activity for F. tritici occurred between late-June, and a second peak in activity was observed in early-August, while F. fusca activity remained more or less the same with no peak. There was no gradient in thrips populations from southern to northern locations. This suggests that these insects are not migratory and may overwinter in soil or perennial noncrop host plants and other weed hosts in Indiana. The capture rates of N. variabilis and F. tritici were only related to temperature, and capture rates of F. fusca were not related to either variable. SVNV was first detected in mid-late August, which coincided with the peak of the primary vector, N. variabilis. The virus was not detected earlier in the season despite peaks in F. tritici activity. Our results may be used in weather-based models to predict both thrips dynamics as well as SVNV outbreaks.

Variable Isotopic Compositions of Host Plant Populations Preclude Assessment of Aphid Overwintering Sites.

Soybean aphid (Aphis glycines Matsumura) is a pest of soybean in the northern Midwest whose migratory patterns have been difficult to quantify. Improved knowledge of soybean aphid overwintering sites could facilitate the development of control efforts with exponential impacts on aphid densities on a regional scale. In this preliminary study, we explored the utility of variation in stable isotopes of carbon and nitrogen to distinguish soybean aphid overwintering origins. We compared variation in bulk 13C and 15N content in buckthorn (Rhamnus cathartica L.) and soybean aphids in Wisconsin, among known overwintering locations in the northern Midwest. Specifically, we looked for associations between buckthorn and environmental variables that could aid in identifying overwintering habitats. We detected significant evidence of correlation between the bulk 13C and 15N signals of soybean aphids and buckthorn, despite high variability in stable isotope composition within and among buckthorn plants. Further, the 15N signal in buckthorn varied predictably with soil composition. However, lack of sufficient differentiation of geographic areas along axes of isotopic and environmental variation appears to preclude the use of carbon and nitrogen isotopic signals as effective predictors of likely aphid overwintering sites. These preliminary data suggest the need for future work that can further account for variability in 13C and 15N within/among buckthorn plants, and that explores the utility of other stable isotopes in assessing likely aphid overwintering sites.

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.

Aphis (Hemiptera: Aphididae) species groups found in the Midwestern United States and their contribution to the phylogenetic knowledge of the genus.

A phylogeny of the genus Aphis Linnaeus, 1 758 was built primarily from specimens collected in the Midwest of the United States. A data matrix was constructed with 68 species and 41 morphological characters with respective character states of alate and apterous viviparous females. Dendrogram topologies of analyses performed using UPGMA (Unweighted Pair Group Method with Arithmetic Mean), Maximum Parsimony and Bayesian analysis of Cytochrome Oxidase I, Elongation Factor 1-α and primary endosymbiont Buchnera aphidicola 16S sequences were not congruent. Bayesian analysis strongly supported most terminal nodes of the phylogenetic trees. The phylogeny was strongly supported by EF1-α, and analysis of COI and EF1-α molecular data combined with morphological characters. It was not supported by single analysis of COI or Buchnera aphidicola 16S. Results from the Bayesian phylogeny show 4 main species groups: asclepiadis, fabae, gossypii, and middletonii. Results place Aphis and species of the genera Protaphis Börner, 1952, Toxoptera Koch, and Xerobion Nevsky, 1928 in a monophyletic clade. Morphological characters support this monophyly as well. The phylogeny shows that the monophyletic clade of the North American middletonii species group belong to the genus Protaphis: P. debilicornis (Gillette & Palmer, 1929), comb. nov., P. echinaceae (Lagos and Voegtlin, 2009), comb. nov., and P. middletonii (Thomas, 1879). The genus Toxoptera should be considered a subgenus of Aphis (stat. nov.). The analysis also indicates that the current genus Iowana Frison, 1954 should be considered a subgenus of Aphis (stat. nov.).

Molecular and morphological differentiation between Aphis gossypii Glover (Hemiptera, Aphididae) and related species, with particular reference to the North American Midwest.

The cotton aphid, Aphis gossypii, is one of the most biologically diverse species of aphids; a polyphagous species in a family where most are host specialists. It is economically important and belongs to a group of closely related species that has challenged aphid taxonomy. The research presented here seeks to clarify the taxonomic relationships and status of species within the Aphid gossypii group in the North American Midwest. Sequences of the mitochondrial cytochrome oxidase 1 (COI), nuclear elongation factor 1-α (EF1-α), and nuclear sodium channel para-type (SCP) genes were used to differentiate between Aphid gossypii and related species. Aphis monardae, previously synonymised with Aphid gossypii, is re-established as a valid species. Phylogenetic analyses support the close relationship of members of the Aphid gossypii group native to North America (Aphid forbesi, Aphid monardae, Aphid oestlundi, Aphid rubifolii, and Aphid rubicola), Europe (Aphid nasturtii, Aphid urticata and Aphid sedi), and Asia (Aphid agrimoniae, Aphid clerodendri, Aphid glycines, Aphid gossypii, Aphid hypericiphaga, Aphid ichigicola, Aphid ichigo, Aphid sanguisorbicola, Aphid sumire and Aphid taraxicicola). The North American species most closely related to Aphid gossypii are Aphid monardae and Aphid oestlundi. The cosmopolitan Aphid gossypii and Aphid sedi identified in the USA are genetically very similar using COI and EF1-α sequences, but the SCP gene shows greater genetic distance between them. We present a discussion of the biological and morphological differentiation of these species.

A new soybean aphid (Hemiptera: Aphididae) biotype identified.

Shortly after its arrival, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), became established as the most important insect pest of soybean, Glycine max L. (Merr.), in the northern part of the North American soybean production region. Soybean resistance is an environmentally sustainable method to manage the pest and new soybean aphid resistant cultivars are beginning to be deployed into production. However, an earlier study identifying a soybean aphid biotype that could colonize plants with the Rag1 resistance gene has raised concerns about the durability of soybean aphid resistance genes. Choice and nonchoice tests conducted in this study characterized the colonization of a soybean aphid isolate, collected from the overwintering host Frangula alnus P. Mill in Springfield Fen, IN, on different aphid resistant soybean genotypes. This isolate readily colonized plants with the Rag2 resistance gene, distinguishing it from the two biotypes previously characterized and indicating that it represented a new biotype named biotype 3. The identification of soybean aphid biotypes that can overcome Rag1 and Rag2 resistance, even before soybean cultivars with the resistance genes have been deployed in production, suggests that there is high variability in virulence within soybean aphid populations present in North America. Such variability in virulence gives the pest a high potential to adapt to and reduce the effective life of resistance genes deployed in production. The search for new soybean aphid resistance genes must, therefore, continue, along with the development of alternative sustainable strategies to manage the pest.

Is there a cryptic species within Aulacorthum solani (Hemiptera: Aphididae)?

Examination of DNA sequences of the 5' end of the mitochondrial cytochrome oxidase I gene of Aulacorthum solani (Kaltenbach) (Hemiptera: Aphididae) reveals little variation between samples from broad geographic provenances. The apparent genetic similarity despite A. solani's morphological and biological differences contrasts with the species complexes of other aphid pests.

Speciation by host-switching in pinyon Cinara (Insecta: Hemiptera: Aphididae).

Parasite-host cospeciation has received much attention as an important mechanism in the diversification of phytophagous insects. However, studies have shown that for certain taxa, it is not host fidelity but host-switching that plays the critical role in speciation. Cinara are aphids (Insecta: Hemiptera: Aphididae: Lachninae) that feed exclusively on the woody parts of conifers of the Cupressaceae and Pinaceae. They are unusual aphids because most Pinaceae play host to several species of Cinara. The aphids show relatively strong host fidelity, and as a consequence historically have been treated based on the taxonomy of their hosts. The historical paradigm of aphid evolution implies that Cinara species have radiated to different parts of the same host species and/or speciated with their host. Using mitochondrial cytochrome oxidase 1 and nuclear elongation factor 1-alpha DNA sequences, we performed molecular phylogenetic analysis of Cinara species, concentrating on those associated with pinyon pines in the southwestern USA. We determined that switching hosts has played a key role in the speciation of the genus, reflected in the polyphyly of pinyon-feeding Cinara. Furthermore, species sharing a common feeding site on different hosts were more closely related to each other than to those sharing the same host but at different feeding sites, suggesting that feeding site fidelity plays a more important role in speciation than does host fidelity in general. This study also elucidated the primary taxonomy of various species: it suggested that Cinara rustica Hottes is a junior synonym of C. edulis (Wilson) and that C. wahtolca Hottes represents two species on the two different pinyon pine species, Pinus edulis Englem. and P. monophylla Torr. & Frem.