Source: OHIO STATE UNIVERSITY submitted to
BOTTOM-UP TROPHIC CASCADES: HOW A CHANGING CLIMATE CAN SHIFT PLANT-PEST-NATURAL ENEMY DYNAMICS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
NEW
Funding Source
Reporting Frequency
Annual
Accession No.
1029742
Grant No.
2023-67013-39157
Project No.
OHO03106-CG
Proposal No.
2022-08738
Multistate No.
(N/A)
Program Code
A1112
Project Start Date
Feb 1, 2023
Project End Date
Jan 31, 2026
Grant Year
2023
Project Director
Michel, A. P.
Recipient Organization
OHIO STATE UNIVERSITY
1680 MADISON AVENUE
WOOSTER,OH 44691
Performing Department
(N/A)
Non Technical Summary
Host plant resistant (HPR) crops provide an effective and sustainable form of insect pest management. Yet, some insects have adapted to overcome these defenses (i.e. virulence), threatening the efficacy of HPR crop cultivars. Abiotic stressors associated with global climate change may also impact HPR trait expression, which potentially introduces a selective pressure onto virulent and avirulent insect populations. Using soybeans and soybean aphids as a model system, this project takes a combined experimental and mathematic approach to quantity how water stress alters virulent and avirulent aphid population dynamics. Specific aims include comparing the effect of host plant water stress on virulent and avirulent fitness (Obj. 1) and aphid interactions with a parasitoid wasp (Obj. 2). We also will track changes in the relative frequency of virulent and avirulent aphids under different water stress scenarios using both laboratory mesocosms (Obj. 3) and quantitative modeling (Obj. 4), which will allow us to simulate changes in aphid populations in response to a wider array of biotic and abiotic variables over the course of a growing season. Understanding these processes will advance climate-resilient, integrated resistance management programs that ensure HPR durability.
Animal Health Component
0%
Research Effort Categories
Basic
80%
Applied
20%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2111820113050%
2113110107050%
Goals / Objectives
Abiotic stressors linked to global climate change frequently alter plant defensive trait expression, subsequently affecting a plant's susceptibility to insect herbivores. Using soybeans and soybean aphids (Aphis glycines) as a model system, this project will explore the longer-term evolutionary consequences of these biotic - abiotic interactions, particularly the differential impact of host plant water stress on virulent (i.e. resistant to natural plant defenses) and avirulent (i.e. susceptible to natural plant defenses) insect biotypes. Long term, this work will expand our understanding about the potential risk for abiotic stress to accelerate selection for insect virulence. Drawing upon a combined experimental and mathematical modeling approach, this project will address four main objectives:1) Compare the effect of host plant water stress on virulent and avirulent soybean aphid fitness2) Evaluate how host plant water stress impacts aphid interactions with a parasitoid wasp3) Track changes in virulent and avirulent aphid frequency under different water stress scenarios within experimental mesocosms4) Develop mathematical models to simulate changes in aphid population dynamics over the course of an entire growing season and in response to a wider array of biotic and abiotic stressors
Project Methods
Objective 1. We will employ a life-table approach to track individual aphids and to calculate how key aphid population demographics, including survivorship, fecundity, and aphid development rates, change under different types of host plant water stress. These experiments will be performed inside a temperature and humidity controlled growth chamber using a full-factorial experimental, randomized complete block design that evaluates how three experimental factors interact: soybean aphid biotype (virulent or avirulent), soybean cultivar (aphid-resistant or aphid-susceptible), and host plant water stress (flooding, drought, or optimal water control).Objective 2. Using the same treatment combinations described in Objective 1, we will systematically compare how "bottom-up" effects from water stress impact biocontrol services in virulent and avirulent soybean aphid by examining different aspects of the tri-trophic interactions between soybean aphids, soybean plants, and one parasitoid species (A. colemani). We will measure the quality of aphids as a host for developing parasitoid larvae as a function of aphid body size, the quantitative and qualitative nutritional composition of aphids, and aphid metabolite accumulation. Additionally, we will conduct laboratory assays that quantify parasitoid fitness in response to different treatment combinations, including parasitoid emergence rate, parasitoid development time, emerged parasitoid body size / sex ratio, and the parasitoid functional response.Objective 3. We will conduct laboratory mesocosm assays to explore the evolutionary consequences of biotic (i.e. host plant water availability) and abiotic (i.e. parasitism) stressors on virulent and avirulent aphid populations dynamics. Mixed aphid biotype populations will be held on aphid-resistant or aphid-susceptible soybean and exposed to different combinations of parasitism and host plant water stress. Using molecular markers, we will calculate the relative proportion of each aphid biotype present within a mesocosm after one week. These mesocosm experiments will track evolutionary changes in aphid populations over the course of a single generation, generating data that will validate subsequent modeling efforts in Objective 4.Objective 4. We will develop mathematic models to explore how a broader suite of stressors, including host plant water stress, soybean cultivar, parasitism, and induced susceptibility, interact to alter aphid population dynamics over the course of a whole growing season. Models will be developed using time dynamical methods and will consider the impact of both individual and combined stress.

Progress 02/01/23 to 01/31/24

Outputs
Target Audience:The target audience for this proposal includes extension educators and scientists from academia, industry, and the government. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has provided training opportunities for one postdoctoral research scientist (Dr. Margaret Lewis), who assumed primary responsibility for all aspects of the project management starting in August 2023. Four undergraduate students (Dylan Murray, Tori Elek, Jordan Lehman, and Cy Marchese) also assisted with various aspects of data collection for this project. In addition to developing their laboratory research skills, the students also have participated in various professional development opportunities. For example, Lehman and Marchese attended an extension meeting in 2023 that focused on climate change impacts on agriculture. Lehman has also developed a plan for an independent undergraduate research study based off Objective 2 of this project, and she successfully applied for and received a competitive undergraduate research fellowship through OSU. This fellowship provides summer salary support and will allow Lehman to complete her independent research project in Summer 2024. Two graduate students (Aniket Banerjee and Urvashi Verma) also led efforts to develop mathematical models. They have met with Dr. Margaret Lewis on a bi-weekly basis, so as to understand the ecological and entomological features of the various objectives, to model them accurately, in mathematical models. This has greatly benefitted their interdisciplinary training. They have met regularly with Dr. Rana Parshad, to fine tune the modeling nuances, as part of their PhD training. How have the results been disseminated to communities of interest?We have presented our research results at regional, national, and international scientific conferences, including the Entomological Society of America North-Central Branch Annual Meeting (invited talk, April 2023, Oklahoma City, OK), the Society of Industrial and Applied Mathematics sectional meeting (3 talks on the population dynamics of aphids under abiotic stresses, Lincoln, NE), the Entomological Society of America Annual National Meeting (November 2023, Vancouver BC), and the National Meeting for the American Chemical Society (invited talk, August 2023, San Francisco, CA). Additional, project results were also shared at the 2023 Climate Smart Conference, an extension meeting hosted by the Ohio State University that attracted a diverse stakeholder audience, including growers, extension agents, industry representations, and university researchers. Results will also be presented at additional scientific conferences during the upcoming year, including 4 anticipated talks at the Midwest mathematical Biology Conference (May2024, La Crosse, WI) and the Society of Industrial and Applied Mathematics national meeting (June 2024, Portland, OR). What do you plan to do during the next reporting period to accomplish the goals? Finish collecting and analyzing life table data and prepare publication Identify a molecular marker for differentiating between soybean aphid biotypes using RadSeq. Use marker to finish processing mixed soybean aphid mesocosm samples (Objective 3) Conduct laboratory assays to quantify flooding stress impacts on parasitoid preference for soybeans aphids and parasitoid fitness. Collect aphid samples for biochemical analyses to quantify flooding stress impacts on aphids as a host for parasitoids. Begin analyzing samples for quantities of key nutrients, including carbohydrates, proteins, and lipids. Submit modeling manuscripts for publication. Begin to analyze and simulate models with 1) parasitoid biocontrol 2) drift and dispersal of pests between soybean plants due to flooding 3) non-linear differential fitness models for virulent and avirulent aphids.

Impacts
What was accomplished under these goals? In Fall 2023, we conducted laboratory mesocosm assays to quantify the impact of flooding stress on virulent and avirulent soybean aphid populations. These assays were conducted using two soybean varieties, an aphid-susceptible soybean variety and a near isoline soybean variety that was bred to express Rag1+2 aphid resistance genes. For each soybean variety, plants were either flooded continuously for 10 days or held under optimal water conditions and infested with either 8 virulent or 8 avirulent soybean aphid adults. Total aphid populations were quantified after 10 days of infestation. Flooding decreased avirulent aphid population densities by 28% and 44% on susceptible and Rag1+2 soybean varieties respectively, but it had not impact on virulent aphid populations. These results are consistent with our hypothesis that flooding stress in soybeans only has a negative impact on avirulent soybean aphid populations. This phenotypic data was incorporated into a manuscript that examines flooding impacts on the soybean aphid transcriptomic; the manuscript was submitted to the journal Molecular Ecology in December 2023 and is currently under review. This data has also been used to guide the development of mathematical models that quantify flooding impacts on aphid population dynamics (Objective 4). We began collecting samples for laboratory mesocosm assays with mixed virulent and avirulent aphid populations (Objective 3); these assays will allow us to test how water stress impacts the spread of virulence within an aphid population. In these assays, flooded or optimally watered soybean plants are infested with a mix of four virulent and four avirulent soybean aphid adults; after 10 days, we count the total number of aphids present on each plant and randomly sample 50 aphids, placing each aphid into individual PCR tubes for subsequent DNA extraction and molecular determination of aphid biotype. Aphid samples are currently being stored in a -20C freezer; we are currently working to develop a molecular marker that will allow us to distinguish between biotypes using a PCR or restriction enzyme digest based assay. Once those markers are developed, we will be able to process our freezer aphid samples, allowing us to determine the proportion of virulent and avirulent aphids present in a population under flooding and optimal water conditions. In January 2024, we began conducting life table experiments to compare the effect of water stress on virulent and avirulent soybean aphid population demographics (Objective 1). Because we observed similar responses to flooding regardless of soybean variety, life table experiments were only conducted using susceptible soybean. This reduced the number of treatments and has allowed for more robust replication. We have completed an estimated 20 - 25 replicates to date, with specific replication numbers varying between treatments (any experimental unit that had an aphid escape from the clip cage was excluded). In these life table assays, VC soybean plants were subjected to optimal water conditions or water stress conditions (seven days of continuous flooding followed by mild drought conditions); on each plant, neonate aphid nymphs were confined to individual leaves using clip cages. Aphids were checked daily, and we recorded survival, molting (as a measure of development), and daily nymph production. As the plants grew, aphids and clip cages were moved to newly emerged trifoliate. We anticipate completing all data collection and analysis by the end of summer 2024. We are currently developing and refining mathematical models that predict quantify water stress impacts on virulent and avirulent soybean aphid population dynamics. The classical boom-bust models (with one peak) that are commonly used to replicate/predict aphid population dynamics may not be accurate under global climate change, because abiotic factors could lead to more than one population peak in a growing season. We are therefore investigating models that have multiple peaks, including a basic one species model that uses a variable, time-dependent carrying capacity to replicate flooding stress impacts on aphid population dynamics. Issues with population explosion were identified in this model, so we are now investigating alternate models to submit a comprehensive manuscript for publication. A preprint detailing some of this work and has been submitted (https://doi.org/10.48550/arXiv.2310.03058). Additional modeling efforts have consider pests and beneficial insect dispersal into agricultural cropping fields. A preprint detailing this work has been submitted (https://doi.org/10.48550/arXiv.2310.17003), and is being fine tuned for a journal submission. We are currently investigating the possibility of extending these models to the soybean - soybean aphid system, considering the role that high amounts of rainfall and flooding might play in aphid dispersal.

Publications