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Research Project: Ecologically-based Management of Arthropods in the Maize Agroecosystem

Location: Corn Insects and Crop Genetics Research

2022 Annual Report

Objectives
Objective 1: Improve knowledge of the genetics, genomics, ecology, and behavior of key maize insect pests as they affect abundance and pest resistance to insecticidal agents, including those expressed in transgenic maize. Sub-objective 1.A. Determine genomic architecture of phenotypic traits within and among reproductive and ecological variants of European corn borer. Sub-objective 1.B. Determine how insect movement and genetics impact potential for development of resistance to GE insecticidal toxins. Sub-objective 1.C. Develop genomic and computational resources for study of key maize pests. Objective 2: Identify and functionally dissect contributions of maize alleles that confer host plant resistance to lepidopteran pests. Sub-objective 2.A. Identify contributing alleles and specialized metabolites conferring resistance to silk-feeding by corn earworm. Sub-objective 2.B. Characterize resistance and develop doubled haploid inbred lines of maize with leaf activity against fall armyworm. Objective 3: Determine potential impacts of farming practices in maize agro-ecosystems on the ecology and management of both arthropod pests and non-pests such as monarch butterflies and bees. Sub-objective 3.A. Develop a risk-based decision support tool for managing sporadic insect pests of seedling maize. Sub-objective 3.B. Develop strategies for improving monarch butterfly and bee habitat in agricultural landscapes.

Approach
European corn borer, corn rootworm, and western bean cutworm are the most serious pests of maize in the Corn Belt, while corn earworm and fall armyworm are major pests in the southern half of the United States. Genetically-engineered (GE) maize is an important management tool for these insect pests, but they have evolved resistance to GE crops in many areas, seriously threatening their continued effectiveness. This project will take an integrated approach toward developing management strategies and tools to use against these insect pests with emphases on insect resistance management to GE maize, insect ecology, insect genetics and genomics, and native host plant resistance. We will address critical knowledge gaps including maize insect pest population genetic dynamics and genomic function, dispersal behavior, efficacy of insect resistance monitoring, and insect resistance management strategies, including ways to incorporate a diversity of pest suppression tactics. Native host plant resistance to control insect pests can serve the latter function, and provide a cost-efficient sustainable management tool for growers who choose not to use GE maize. This project will study native resistance in maize to insect pests, particularly corn earworm and fall armyworm, so that low-input control options can be developed. Given concerns on the indirect effects of farming practices on non-target arthropods, including bees and monarch butterflies, project scientists will work with stakeholders to develop strategies for increasing habitat for monarch butterflies to counter loss of milkweeds in maize and soybean fields. In addition, researchers will provide growers a decision support tool to allow realistic assessment of when the use of seeds coated with neonicotinoid insecticide is justified in their particular fields to control sporadic seedling pests and when it is not, reducing overall insecticide input. Collectively, this research will result in maize pest management systems that are stable and reliable, cost effective for producers, and safe for growers, consumers and the environment.

Progress Report
Objective 1: Research continued on understanding genetic and genomic aspects of key maize pests in relation to population and ecological dynamics, and subsequent impacts on the development and spread of resistance to control tactics. Genetically engineered (GE) maize varieties that express one or more Bacillus thuringiensis (Bt) pesticidal proteins are used by farmers to manage damage by the western corn rootworm (WCR), European corn borer (ECB), corn earworm (CEW) and western bean cutworm. However, all these pests have developed resistance to one or more Bt proteins, resulting in economic losses and threatening the sustainability of GE maize. One ecological variant of ECB differs in the chemical sex-attractant (pheromone) emitted by females with associated response by males, and another variant differs in larval development time which determines the number of reproductive generations per summer. Genes responsible for these ecological differences were previously co-discovered by ARS researchers in Ames, Iowa and Tufts University and all except those responsible for female pheromone production are located on the same chromosome. Current research determined that genomic divergence between ECB variants is concentrated near the responsible (causal) genes, and that the level of divergence increases as the number of ecological differences increases. Although these ecological differences reduce mating between the variant populations, the results also indicate high genetic exchange in genome regions not physically close to the causal genes. This suggests resistance genes will move unhindered between the different ecological variant populations when they mate with each other. Adaptation of a pest insect to farmer control tactics, including Bt, can occur via changes in genome structure and expression of genes. The genome sizes of WCR and northern corn rootworm (NCR) were estimated to be nearly twice that of southern corn rootworm (SCR), and analyses of sequence data demonstrated that expansion of the WCR and NCR genomes is due to increased number of mobile DNA elements capable of self-replication and proliferation. A separate study in collaboration with researchers from Iowa State University and University of Florida showed that DNA from a novel virus had integrated into NCR and SCR genomes. This information will be important for evaluating how changes in genome size influence differences in maize host specificity of WCR and NCR compared to the broader range of host plants used by SCR. Additional research showed that the expression of genes involved in cell survival and repair increased when WCR larvae were fed Bt maize compared to those fed non-Bt maize, providing novel insight into gene pathways affecting WCR recovery after exposure to Bt maize. In research with Iowa State University collaborators and funded by USDA-National Institute of Food and Agriculture, four separate mutations were identified in a gene expressed in the nervous system of insects that confers differing levels of resistance to pyrethroid insecticides. A chromosome-level genome assembly, annotated with probable gene functions, was generated for a Bt resistant strain of CEW through the ARS Ag100Pest Initiative. These changes provide insight into the genetic changes in pest insects that may directly impact effectiveness of current pest management tactics. Objective 2: Research continued on the use of host plant resistance to control key moth pests of maize. Field work was conducted in 2021 to grow, pollinate, and harvest new seed to ensure preservation of over 400 insect resistant breeding lines and other important maize genotypes needed for research on plant resistance to fall armyworm and corn earworm. All germplasm maintenance efforts were conducted under selection pressure from the pest to preserve the integrity of resistance in the maize genotypes. In collaboration with ARS researchers from Mississippi State, MS, we completed a two-year study evaluating maize germplasm from Belize, French Guiana, Guyana, and Suriname for resistance to leaf feeding fall armyworm. Artificially infested plants grown in the field were scored for leaf feeding damage at 7 and 14 days post infestation. Scores for maize germplasm Ames 28786 (‘GIN II’) at 7 and 14 days and NSL 283834 (‘Guyana 807’) at 14 days did not differ from the resistant check, Mp708. Both ‘GIN II’ and ‘Guyana 807’ originate from Guyana, where only four maize genotypes were available from the USDA-ARS National Plant Germplasm System for testing. To acquire additional Guyana-originating maize genotypes for testing, the databases from tropical maize seed banks (e.g., CIMMYT) will be searched. In collaboration with researchers from Iowa State University, we tested a series of experimental lines derived from maize parent XL370A for resistance to fall armyworm leaf feeding. A two-year study was completed that evaluated all XL370Aderived maize germplasms developed by the USDA-ARS Germplasm Enhancement of Maize project for resistance to leaf feeding by fall armyworm. In replicated field trials, germplasm GEMN-0095 showed resistance to fall armyworm leaf feeding but at a lower level than the resistant check, Mp708. Variability in response was observed in GEMN-0095 and individual plants were selected and self-pollinated. In 2021, seed from these self-pollinated plants were grown ear-to-row and evaluated for leaf feeding resistance. Two rows were highly resistant to fall armyworm with damage scores equal to the resistant check, Mp708. A seed increase was made and these two rows are included in a replicated trial in Summer 2022. Objective 3: Research continued on the impacts of farming practices in maize agro-ecosystems on non-pests such as monarch butterflies. The eastern North American population of monarch butterflies has declined significantly over the last two decades. Loss of the larval host plant, milkweed, in agricultural landscapes is one of the primary drivers of this decline. Conservation efforts call for landscape-scale restoration of milkweed and flowering forbs to support sustainable monarch populations. Understanding how individual monarchs perceive and locate these resources is critical to determining how to effectively restore habitat across the landscape. In collaboration with researchers at Iowa State University and University of Memphis, we conducted experiments designed to elucidate the range at which breeding adults detect nectar-bearing forbs (food resources) and common milkweed (for egg-laying). Wild-caught monarchs were tethered to an outdoor flight mill that allowed directional body movement, and their orientation toward resource patches placed at different distances upwind was quantified. Responses were compared across distances and against a no-resource control group. Results showed that monarch orientation was strongly associated with the mean upwind direction regardless of the presence or distance to a resource patch. After normalizing for wind direction, there was no evidence that variation in flight orientation differed across the no-resource and distance groups. Though unable to estimate perceptual range, the strong upwind orientation response lends insight into improved habitat placement in agricultural landscapes. Specifically, placing habitat patches along the prevailing wind trajectory may facilitate inter-patch detection, movement, and utilization among breeding monarchs.

Accomplishments
1. Identification of genes potentially involved in novel mechanisms of western corn rootworm (WCR) survival when exposed to transgenic Bacillus thuringiensis (Bt) maize roots. WCR feeding damage to maize results in economically significant yield losses to farmers in the United States. Farmers rely on maize varieties that express one or more insecticidal Bt proteins to control WCR, but this pest is increasingly difficult to manage because it has developed resistance across wide areas of the United States. The molecular mechanisms by which Bt proteins cause death of susceptible WCR larvae remain unknown. ARS researchers in Ames, Iowa and an international team of collaborators investigated the changes in gene expression among Bt susceptible WCR larvae fed maize varieties that expressed different types of Bt proteins. Larvae fed Bt maize increased expression of genes involved in stress responses and metabolism compared to larvae fed non-Bt maize. Stress response genes included those involved in determining if cells should be destroyed or can recover from damage, and the balance determines if WCR survive. The findings of this study identify novel genes that help WCR recover from exposure to Bt maize and point to novel mechanisms by which resistance may evolve. This information will help guide research of university, government, and industry scientists for evaluating and improving insect resistance management strategies to maintain the effectiveness of Bt maize for the control of WCR.

2. Monarch butterflies do not avoid laying eggs on milkweed treated with neonicotinoid insecticide. Monarch butterfly populations have declined over the last two decades, attributed in part to declines in milkweed, its larval host plant, across its main breeding range in the U.S. Midwest. Conservation efforts call for restoration of 1.3 billion milkweed plants into the Midwestern landscape, but this will require habitat establishment in marginal croplands where there is a high potential for exposure to neonicotinoid insecticides, which are commonly used on corn and soybeans as seed treatments or foliar sprays to provide protection against insect pests. ARS scientists in Ames, Iowa investigated whether egg-laying monarchs discriminate against milkweed plants exposed to a neonicotinoid insecticide, when either 1) taken up by the plant's vascular system and spread internally through the plant, which is the way seed treatments work; or 2) as an external spray treatment on the surface of the leaves. Egg-laying preference was evaluated by egg-count and video data. The results indicated that neither internal nor external treatment with neonicotinoid influenced egg-laying behavior. Thus, eggs and larvae will likely be exposed to neonicotinoids in habitats immediately adjacent to treated crop fields. This information will help guide monarch butterfly conservation efforts by non-profit organizations and regulatory agencies to strategically place restored habitat in agriculture-dominated landscapes.

U.S. DEPARTMENT OF AGRICULTURE

Corn Insects and Crop Genetics Research: Ames, IA