Multiple wheat genomes reveal global variation in modern breeding.

Advances in genomics have expedited the improvement of several agriculturally important crops but similar efforts in wheat (Triticum spp.) have been more challenging. This is largely owing to the size and complexity of the wheat genome1, and the lack of genome-assembly data for multiple wheat lines2,3. Here we generated ten chromosome pseudomolecule and five scaffold assemblies of hexaploid wheat to explore the genomic diversity among wheat lines from global breeding programs. Comparative analysis revealed extensive structural rearrangements, introgressions from wild relatives and differences in gene content resulting from complex breeding histories aimed at improving adaptation to diverse environments, grain yield and quality, and resistance to stresses4,5. We provide examples outlining the utility of these genomes, including a detailed multi-genome-derived nucleotide-binding leucine-rich repeat protein repertoire involved in disease resistance and the characterization of Sm16, a gene associated with insect resistance. These genome assemblies will provide a basis for functional gene discovery and breeding to deliver the next generation of modern wheat cultivars.

Volatile Organic Compounds Mediate Host Selection of Wheat Midge, Sitodiplosis Mosellana (Géhin) (Diptera: Cecidomyiidae) between Preanthesis and Postanthesis Stages of Wheat.

The orange wheat blossom midge, Sitodiplosis mosellana (Géhin) (Diptera: Cecidomyiidae), is a significant wheat pest in the Prairie Provinces of Canada and northern regions of the USA. Wheat phenology plays a critical role in wheat midge oviposition. We hypothesized that S. mosellana oviposition behaviour is influenced by volatile organic compounds (VOCs) emitted by wheat at two adjacent wheat growth stages: preanthesis and postanthesis. A higher number of S. mosellana eggs laid on preanthesis than postanthesis spikes in an oviposition choice experiment using the susceptible spring wheat cultivar 'Roblin'. In preanthesis, wheat emitted higher amounts of Z-3-hexenyl acetate (Z3-06:OAc) than at the postanthesis stage. Higher amounts of methyl ketones such as 2-tridecanone, 2-pentadecanone, and 2-undecanone were emitted by wheat in the postanthesis stage and these VOCs were sensitive to S. mosellana antennae used in the Gas Chromatography-Electroantennographic Detection. Females were attracted to synthetic Z3-06:OAc but were deterred by 2-tridecanone relative to the solvent control in the vertical Y-tube olfactometer. 2-Undecanone and 2-pentadecanone did not show any attractiveness or deterrence. In a no-choice oviposition experiment, fewer eggs were laid in preanthesis wheat exposed to a synthetic VOC blend of Z3-06:OAc, 2-undecanone, 2-tridecanone, and 2-pentadecanone at the concentrations released by postanthesis spikes. This study shows that the reduction of Z3-06:OAc, in the VOC mix, and possibly the increase in 2-tridecanone, are likely responsible for the reduction in oviposition on postanthesis wheat. These results elucidate for the first time the role of specific VOCs mediating S. mosellana oviposition in preanthesis and postanthesis wheat.

Genetic analysis of oviposition deterrence to orange wheat blossom midge in spring wheat.

KEY MESSAGE: A major QTL for oviposition deterrence to orange wheat blossom midge was detected on chromosome 1A in the Canadian breeding line BW278 that was inherited from the Chinese variety Sumai-3. Orange wheat blossom midge (OWBM, Sitodiplosis mosellana Géhin, Diptera: Cecidomyiidae) is an important insect pest of wheat (Triticum aestivum L.) that reduces both grain yield and quality. Oviposition deterrence results in a reduction of eggs deposited on spikes relative to that observed on a wheat line preferred by OWBM. Quantification of oviposition deterrence is labor-intensive, so wheat breeders require efficient DNA markers for the selection of this trait. The objective of this study was to identify quantitative trait loci (QTL) for oviposition deterrence in a doubled haploid (DH) population developed from the spring wheat cross Superb/BW278. The DH population and check varieties were evaluated for OWBM kernel damage from five field nurseries over three growing seasons. QTL analysis identified major effect loci on chromosomes 1A (QSm.mrc-1A) and 5A (QSm.mrc-5A). Reduced kernel damage was contributed by BW278 at QSm.mrc-1A and Superb at QSm.mrc-5A. QSm.mrc-1A mapped to the approximate location of the oviposition deterrence QTL previously found in the American variety Reeder. However, haplotype analysis revealed that BW278 inherited this oviposition deterrence allele from the Chinese spring wheat variety Sumai-3. QSm.mrc-5A mapped to the location of awn inhibitor gene B1, suggesting that awns hinder OWBM oviposition. Single-nucleotide polymorphisms (SNPs) were identified for predicting the presence or absence of QSm.mrc-1A based upon haplotype. Functional annotation of candidate genes in 1A QTL intervals revealed eleven potential candidate genes, including a gene involved in terpenoid biosynthesis. SNPs for QSm.mrc-1A and fully awned spikes provide a basis for the selection of oviposition deterrence to OWBM.

Crop pests and predators exhibit inconsistent responses to surrounding landscape composition.

The idea that noncrop habitat enhances pest control and represents a win-win opportunity to conserve biodiversity and bolster yields has emerged as an agroecological paradigm. However, while noncrop habitat in landscapes surrounding farms sometimes benefits pest predators, natural enemy responses remain heterogeneous across studies and effects on pests are inconclusive. The observed heterogeneity in species responses to noncrop habitat may be biological in origin or could result from variation in how habitat and biocontrol are measured. Here, we use a pest-control database encompassing 132 studies and 6,759 sites worldwide to model natural enemy and pest abundances, predation rates, and crop damage as a function of landscape composition. Our results showed that although landscape composition explained significant variation within studies, pest and enemy abundances, predation rates, crop damage, and yields each exhibited different responses across studies, sometimes increasing and sometimes decreasing in landscapes with more noncrop habitat but overall showing no consistent trend. Thus, models that used landscape-composition variables to predict pest-control dynamics demonstrated little potential to explain variation across studies, though prediction did improve when comparing studies with similar crop and landscape features. Overall, our work shows that surrounding noncrop habitat does not consistently improve pest management, meaning habitat conservation may bolster production in some systems and depress yields in others. Future efforts to develop tools that inform farmers when habitat conservation truly represents a win-win would benefit from increased understanding of how landscape effects are modulated by local farm management and the biology of pests and their enemies.

Interactions between exotic and native lady beetle species stabilize community abundance.

A 23-year time-series of abundance for 13 lady beetle species (Coccinellidae) was used to investigate community stability. The community exhibited persistence in ten habitats, no overall trend in abundance, and low temporal variability quantified as Population variability (PV) = 0.33 on a scale from 0 to 1 that declined to 0.16 in the past 8 years. This high level of stability occurred as exotic lady beetles disrupted populations of the native species. For hypothetical communities of pairs of species (with randomly generated annual abundances in the range for lady beetles), PV increased linearly with the correlation coefficients between individual time series, illustrating a "portfolio effect". PV for the real community and the negative correlation between the abundance of exotics and natives fit this relationship precisely. A gradual decline of natives matched by an equal gradual rise in the abundance of exotics contributed to the negative correlation that stabilized the community. The abundance of the dominant species, an exotic, was negatively correlated with other exotics and most natives, and its stability increased over time, helping to stabilize the community. The community was most stable in habitats where beetle abundance was high (crops, particularly perennial crops) and, unexpectedly, was least stable in habitats with high diversity and stability of vegetation cover (forests). These data are consistent with the hypothesis that competition between exotic and native species, with release from competition for natives in some years, stabilized the abundance of this community. Stability may not last if populations of native species continue declining.

Landscape-scale pest suppression is mediated by timing of predator arrival.

There is increasing evidence that biological control of agricultural pests is affected by the landscape context, although the mechanisms behind this pattern have received little attention. Ecological theory predicts that one key mechanism mediating successful pest suppression is early predator immigration to agricultural fields. However, the importance of this population process under different landscape contexts remains unknown. Here, we elucidate the relative importance of landscape context and timing of predator immigration on aphid suppression by manipulating exposure to predation in agroecosystems located across a gradient of landscape complexity in a subtropical horticultural region in Australia. Aphid suppression varied with landscape context, from populations escaping control to almost complete pest suppression. In general, we found higher aphid suppression when predators were allowed immediate and continuous access to aphids than when predators were delayed or excluded for a week, but responses varied in each landscape. Contrary to previous reports from temperate agricultural landscapes, aphid suppression was neutral or negatively associated with natural and seminatural vegetation, whereas aphid suppression was positively associated with landscapes with a higher proportion of alfalfa. When landscapes were classified according to their levels of complexity, we showed that early predation resulted in similar levels of pest suppression in simplified landscapes (i.e., with low proportions of alfalfa and habitat diversity) as late predation in complex landscapes (i.e., with high proportions of alfalfa and habitat diversity). Our data show that timing of predator arrival to agricultural fields is as important as landscape complexity for mediating pest control in agroecosystems. Furthermore, our results suggest that key distributions of suitable habitats that facilitate natural enemy movement can enhance biological control in simplified landscapes.

Annual Crops Contribute More Predators than Perennial Habitats during an Aphid Outbreak.

Crops and semi-natural habitats provide predator populations with varying floral and prey resources, but their individual role on predator movement has seldom been studied. Here, we tease apart the role of adjacent habitats, predator abundance in the adjacent habitat, and soybean aphid (Aphis glycines Matsumura) abundance in soybean (Glycine max (L.) Merr.) on predator movement into soybean. We studied 12 soybean fields adjacent to alfalfa (Medicago sativa L.), canola (Brassica napus L.), spring wheat (Triticum aestivum L.), or woody vegetation, during a soybean aphid outbreak. Bidirectional Malaise traps and sticky traps were used to quantify predator movement between and abundance within soybean and adjacent habitats, respectively. Field plant counts were conducted to quantify aphid abundance in soybean. Coccinellidae and Syrphidae were the two most abundant families collected. Coccinellids and Eupeodes americanus (Wiedemann) (Diptera: Syrphidae) had net movement in soybean and their movement increased with aphid abundance. Movement of E. americanus was highest from wheat, coccinellid abundance was higher in wheat than woody vegetation, Toxomerus marginatus (Say) (Diptera: Syrphidae) abundance was highest in canola, and all other predators were more abundant in canola than woody vegetation. In general, our study suggests that annual crops have and provide more predators to soybean during aphid outbreaks than perennial habitats.

Development and validation of node-based sample units for estimating soybean aphid (Hemiptera: Aphididae) densities in field cage experiments.

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is currently the most important insect threat to soybean, Clycine max (L.) Merr., production in the North Central United States. Field cage studies are a key tool in investigating the potential of natural enemies and host plant resistance to control this pest. However, a major constraint in the use of cage studies is the limited number of treatments and replicates that can be used as aphid densities frequently become so large as to limit the number of experimental units that can be quantified. One way to overcome this limitation is to develop methods that estimate whole-plant aphid densities based on a reduced sampling plan. Here, we extend an existing method, node-sampling, used for estimating aphid populations in open field conditions and apply it to caged populations. We show that parameters calculated under open field conditions are inappropriate to estimate caged populations. In contrast, using four independent data sets of caged populations and a cross-validation technique, we demonstrate that a three-node sampling unit and a weighted formula provide accurate and robust estimates of whole-plant aphid density. This method reduced the number of aphids counted per plant by and average of 60%, with greater reductions at higher aphid densities. We further demonstrate that nearly identical statistical results were obtained when whole-plant or node-sampling estimates were used in the analysis of two case studies. The reduced sample unit method developed here saves time without sacrificing efficiency so that more plants, replications, or studies can be conducted that will lead to improved soybean aphid management.

Probability of cost-effective management of soybean aphid (Hemiptera: Aphididae) in North America.

Soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is one of the most damaging pests of soybean, Glycine max (L.) Merrill, in the midwestern United States and Canada. We compared three soybean aphid management techniques in three midwestern states (Iowa, Michigan, and Minnesota) for a 3-yr period (2005-2007). Management techniques included an untreated control, an insecticidal seed treatment, an insecticide fungicide tank-mix applied at flowering (i.e., a prophylactic treatment), and an integrated pest management (IPM) treatment (i.e., an insecticide applied based on a weekly scouting and an economic threshold). In 2005 and 2007, multiple locations experienced aphid population levels that exceeded the economic threshold, resulting in the application of the IPM treatment. Regardless of the timing of the application, all insecticide treatments reduced aphid populations compared with the untreated, and all treatments protected yield as compared with the untreated. Treatment efficacy and cost data were combined to compute the probability of a positive economic return. The IPM treatment had the highest probability of cost effectiveness, compared with the prophylactic tank-mix of fungicide and insecticide. The probability of surpassing the gain threshold was highest in the IPM treatment, regardless of the scouting cost assigned to the treatment (ranging from $0.00 to $19.76/ha). Our study further confirms that a single insecticide application can enhance the profitability of soybean production at risk of a soybean aphid outbreak if used within an IPM based system.

Suppression of soybean aphid by generalist predators results in a trophic cascade in soybeans.

Top-down regulation of herbivores in terrestrial ecosystems is pervasive and can lead to trophic cascades that release plants from herbivory. Due to their relatively simplified food webs, agroecosystems may be particularly prone to trophic cascades, a rationale that underlies biological control. However, theoretical and empirical studies show that, within multiple enemy assemblages, intraguild predation (IGP) may lead to a disruption of top-down control by predators. We conducted a factorial field study to test the separate and combined effects of predators and parasitoids in a system with asymmetric IGP. Specifically we combined ambient levels of generalist predators (mainly Coccinellidae) of the soybean aphid, Aphis glycines Matsumura, with controlled releases of the native parasitoid Lysiphlebus testaceipes (Cresson) and measured their impact on aphid population growth and soybean biomass and yield. We found that generalist predators provided strong, season-long aphid suppression, which resulted in a trophic cascade that doubled soybean biomass and yield. However, contrary to our expectations, L. testaceipes provided minor aphid suppression and only when predators were excluded, which resulted in nonadditive effects when both groups were combined. We found direct and indirect evidence of IGP, but because percentage parasitism did not differ between predator exclusion and ambient predator treatments, we concluded that IGP did not disrupt parasitism during this study. Our results support theoretical predictions that intraguild predators which also provide strong herbivore suppression do not disrupt top-down control of herbivores.

Predators exert top-down control of soybean aphid across a gradient of agricultural management systems.

The discovery of soybean aphid, Aphis glycines Matusumura, in North America in 2000 provided the opportunity to investigate the relative strength of top-down and bottom-up forces in regulating populations of this new invasive herbivore. At the Kellogg Biological Station Long Term Ecological Research site in agroecology, we contrasted A. glycines establishment and population growth under three agricultural production systems that differed markedly in disturbance and fertility regimes. Agricultural treatments consisted of a conventional-tillage high-input system, a no-tillage high-input system, and a zero-chemical-input system under conventional tillage. By selectively restricting or allowing predator access we simultaneously determined aphid response to top-down and bottom-up influences. Irrespective of predator exclusion, our agricultural manipulations did not result in bottom-up control of A. glycines intrinsic rate of increase or realized population growth. In contrast, we observed strong evidence for top-down control of A. glycines establishment and overall population growth in all production systems. Abundant predators, including Harmonia axyridis, Coccinella septempunctata, Orius insidiosus, and various predaceous fly larvae, significantly reduced A. glycines establishment and population increase in all trials. In contrast to other systems in which bottom-up forces control herbivore populations, we conclude that A. glycines is primarily controlled via top-down influences of generalist predators under a wide range of agricultural management systems. Understanding the role of top-down and bottom-up forces in this context allows agricultural managers to focus on effective strategies for control of this invasive pest.

Within-plant bottom-up effects mediate non-consumptive impacts of top-down control of soybean aphids.

There is increasing evidence that top-down controls have strong non-consumptive effects on herbivore populations. However, little is known about how these non-consumptive effects relate to bottom-up influences. Using a series of field trials, we tested how changes in top-down and bottom-up controls at the within-plant scale interact to increase herbivore suppression. In the first experiment, we manipulated access of natural populations of predators (primarily lady beetles) to controlled numbers of A. glycines on upper (i.e. vigorous-growing) versus lower (i.e. slow-growing) soybean nodes and under contrasting plant ages. In a second experiment, we measured aphid dispersion in response to predation. Bottom-up and top-down controls had additive effects on A. glycines population growth. Plant age and within-plant quality had significant bottom-up effects on aphid size and population growth. However, top-down control was the dominant force suppressing aphid population growth, and completely counteracted bottom-up effects at the plant and within-plant scales. The intensity of predation was higher on upper than lower soybean nodes, and resulted in a non-consumptive reduction in aphid population growth because most of the surviving aphids were located on lower plant nodes, where rates of increase were reduced. No effects of predation on aphid dispersal among plants were detected, suggesting an absence of predator avoidance behavior by A. glycines. Our results revealed significant non-consumptive predator impacts on aphids due to the asymmetric intensity of predation at the within-plant scale, suggesting that low numbers of predators are highly effective at suppressing aphid populations.