Source: GEORGIA INSTITUTE OF TECHNOLOGY submitted to
EFFECTS OF PESTICIDE EXPOSURE ON DEVELOPMENTAL GENETICS IN BUMBLEBEES
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
AFRI COMPETITIVE GRANT
Reporting Frequency
Annual
Accession No.
1030452
Grant No.
2023-67012-39886
Cumulative Award Amt.
$225,000.00
Proposal No.
2022-09642
Multistate No.
(N/A)
Project Start Date
Jun 1, 2023
Project End Date
May 31, 2026
Grant Year
2023
Program Code
[A1113]- Pollinator Health: Research and Application
Recipient Organization
GEORGIA INSTITUTE OF TECHNOLOGY
(N/A)
ATLANTA,GA 30332
Performing Department
(N/A)
Non Technical Summary
Social insect pollinators are critical to successful agricultural practices. Specifically, bees provide "buzz-pollination" to essential food crops. However, natural populations of bees may be harmed by anthropogenic pesticide use in the environment. Unfortunately, the indirect effects of pesticide exposure on the integrated development found in social insect societies remains poorly understood. In particular, pesticides may lead to unusual developmental effects in social insects because queens, workers, and males all arise from the same genome. Our lack of understanding of how environmental contaminants, such as pesticides, affect the developmental genetics of social pollinators represents a major gap in our understanding of the effects of pesticides on pollinators, specifically, and social insects, in general. This project will investigate how pesticides affect the integrated developmental processes that social insect pollinators require by examining changes in genetic correlations of morphology and gene expression when pesticides stress the colony. This research will provide novel insight into how environmental toxicants affect the developmental processes displayed by social insect pollinators.
Animal Health Component
10%
Research Effort Categories
Basic
90%
Applied
10%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
3033085108060%
3143085115040%
Knowledge Area
303 - Genetic Improvement of Animals; 314 - Toxic Chemicals, Poisonous Plants, Naturally Occurring Toxins, and Other Hazards Affecting Animals;

Subject Of Investigation
3085 - Other bees (non-Apis bees) - All bees except Apis cerana; includes Bombas, Alfalfa leaf-cutter;

Field Of Science
1080 - Genetics; 1150 - Toxicology;
Goals / Objectives
Food and agricultural systems require social insect pollinators, like bees. However, anthropogenic-driven environmental change, such as pesticide use, may have negative impacts on bee populations. Substantial research suggests that the direct effects of pesticides may lead to significant reductions of natural bee populations. However, the indirect effects of pesticides on the integrated development of phenotypically and functionally distinct social insect castes remain poorly understood. Because castes of social insects arise from the same genome, development of the castes will be correlated and elicit unusual effects in response to environmental stressors. However, our lack of knowledge of whether genetically correlated development occurs represents a major gap in our understanding of social systems, in general, and the effects of pesticides on pollinators, in particular. Our research will investigate how different pesticides affect the integrated development of bumblebees through changes in morphology, sex ratios, gene expression, and genetic correlations. Thus, this research will answer the question as to how the genetic correlations between castes affect pollinator development. Further, this postdoctoral fellowship will support my training as a future leader and independent researcher in agriculture.
Project Methods
We propose to study the effects of pesticides on B. impatiens bumblebeesusing a variety of morphological and genetic approaches. Our overall hypothesis is that pesticide exposure will negatively affect development and lead to changes in morphology of queens and workers and associated patterns of gene expression. In addition, and of greater novel interest, we predict that pesticide exposure will change genetic correlations between traits for queens and workers. We expect that pesticide exposure will increase genetic correlations and further impair independent development of the castes. To test this hypothesis, we will expose lab-reared bumblebee colonies to a range of concentrations of thiamethoxam, imidacloprid, or sulfoxaflor through contaminated sugar water. We will then address the following two aims empirically:Aim 1: Test how pesticides affect caste ratios, morphology, and genetic correlations for morphology.Overview: In this aim, we plan to test how pesticides affect caste ratios, morphology, and genetic correlations for morphology when exposed to pesticides during development. First, we will determine how pesticides affect sex ratio, a very important trait affecting social insect colony fitness. Second, we will obtain information on how pesticides affect morphological traits of both workers and queens. These data will provide direct information on changes associated with environmental perturbations. Finally, we will determine how pesticides affect genetic correlations between castes for morphological traits. These results will provide novel information on how genetic architecture underlying development responds to pesticide exposure and allow us to test important predictions regarding development:Prediction #1A: Pesticide exposure will impair colony development by inducing male-biased sex ratios.Prediction #1B: Pesticide exposure will cause the development of smaller adult bee phenotypes with fluctuating asymmetry.Prediction #1C: Genetic correlations for morphological traits will become more positive with pesticide exposure and produce less optimal phenotypes among castes.Aim 2: Determine how exposure to pesticides affects gene expression and genetic correlations for gene expressionOverview: We will determine how exposure to pesticides affects gene expression and genetic correlations for gene expression. Our experiments will allow us to identify the direct effects of pesticide exposure on gene expression and the indirect effects on genetic correlations and ultimately, molecular evolution. Importantly, gene expression, which can be considered a standard quantitative phenotypic trait, is one way for intralocus conflict to be resolved33,47. Thus, increased genetic correlations for gene expression patterns would represent a constraint on intralocus conflict resolution and evolution of distinct phenotypes. Therefore, we propose the following two predictions:Prediction #2A: Genes involved in immune function, detoxification, and growth/reproduction pathways will be altered in bumblebees exposed to pesticides.Prediction #2B: Pesticide exposure will increase genetic correlations of gene expression in ovaries of female bumblebees.

Progress 06/01/23 to 05/31/24

Outputs
Target Audience:My primary target audience during this reporting period was underrepresented individuals in STEM. I worked closely with three undergraduate students and one master's student part of several different groups that are underrepresented in STEM including female students, LGBTQ students, and students of ethnic minorities. My mentoring and instruction of these students matters because it increases participation of these groups in research, improves their collegiate experience, and improves my ability to be a strong mentor and leader in research. Another target audience was the Atlanta, GA community. Our lab participated in the Atlanta Science Festival, bringing hands-on educational opportunities about social insects and pollinators to community members of all ages and walks of life. This matters because we are improving general public education on important, agriculturally relevant topics and improving the visibility of our research. Changes/Problems:We are on track to complete our proposed aims. However, we found that our Bombus impatiens colonies were all monandrous. Therefore, we continued to use B. impatiens for studies related to pesticide exposure in bumblebees. This included examining caste differences in sensitivity to sulfoxaflor, differences in thiamethoxam and sulfoxaflor toxicity, behavioral and reproductive outputs after chronic exposure to sulfoxaflor, and more. And we are now using the polyandrous, social wasp, Vespula maculifrons, to answer questions about genetically correlated development between castes. Finally, we recently ordered and began training on an artificial insemination tool to attempt to obtain polyandrous colonies of B. impatiens. Successful development of artificial insemination techniques in Bombus would open up entirely new avenues of research and study. What opportunities for training and professional development has the project provided?I have taken advantage of many different training and professional development opportunities. I completed a Project Management Certificate Program through Georgia Tech's Postdoctoral Services, which included over 40 hours of instruction and a final portfolio. I have also spent a lot of time developing my mentorship, leadership, and management skills in the lab working with graduate and undergraduate students. I have taken advantage of many presentation and networking opportunities through invited seminars and national conferences. I taught as a guest lecturer in the Physics of Living Systems class at Georgia Tech in early 2024. Overall, this project has significantly contributed to my training and professional development as an early-career scientist. How have the results been disseminated to communities of interest?The results have been disseminated to communities of interest in several different ways. First, I presented our results 8 times in formal oral or poster presentations at invited seminars, national conferences, and local poster symposium. Further, our results have been discussed informally at lab meetings, joint lab meetings, and with the general public at the Atlanta Science Festival or other public events. What do you plan to do during the next reporting period to accomplish the goals?Our goals are achievable within the next reporting period, and I feel very confident that the methods and techniques developed will allow me to accomplish a lot. For example, we have streamlined bumblebee husbandry and received new artificial insemination tools to improve our genetic experimental goals. We also have a large study that is currently ongoing that will address several of our primary goals including assessing how pesticide exposure affects caste development, morphology, and sex ratios. Further, I currently have three publications under review and at least two additional projects that will eventually be written into manuscripts. I also plan to continue presenting, networking, mentoring, guest lecturing, and growing as a scientist. One primary goal that I plan to address in this next reporting period is to interact with stakeholders. With a strong suite of results about the risks to pollinators on crops using sulfoxaflor, I look forward to collaborating with local farmers.

Impacts
What was accomplished under these goals? I was able to make a lot of progress on our goals over the past year. First, I set up an entire bumblebee lab from scratch by reading, networking, and a lot of trial and error! I established a highly efficient bumblebee lab space with relevant equipment and supplies needed to support animal husbandry. I also conducted a large number of experiments that have contributed to multiple different projects. First, we found that bumblebees prefer sulfoxaflor contaminated food and show caste-specific differences in sulfoxaflor sensitivity. Next, we also found that chronic sulfoxaflor exposure altered nest building, reproductive output, and gene expression in the brains and ovaries of bumblebees.

Publications

  • Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Juneau A, Orr SE, Goodisman MAD. Toxicity of pesticides thiamethoxam and sulfoxaflor on Bombus impatiens. Southeastern Population Ecology and Evolutionary Genetics (SEPEEG) Conference. Pembroke, VA; September 2023. (Won Best Student Poster Award)
  • Type: Other Status: Published Year Published: 2024 Citation: Embracing the Winding Path of Scientific Careers Integrative and Comparative Biology Interview and Blog Post by Esther Okamoto
  • Type: Other Status: Published Year Published: 2023 Citation: USDA Fellow to Study Pesticide Exposure in Key Pollinators Georgia Tech College of Sciences News Story
  • Type: Other Status: Other Year Published: 2024 Citation: Orr SE. Physiological mechanisms of global insect decline. Invited Seminar at Mercer University School of Medicine. Macon, Georgia. January 2024.
  • Type: Other Status: Other Year Published: 2023 Citation: Orr SE. Physiological mechanisms of global insect decline. Invited seminar at University of Georgia. Athens, Georgia. December 2023.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2024 Citation: Orr SE and Goodisman MAD. Hazard of an emerging pesticide on bumblebees. Society for Integrative and Comparative Biology. Seattle, WA. January 2024.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2024 Citation: Orr SE. Effects of the pesticide sulfoxaflor on bumblebee castes and feeding behavior. Southeastern Branch Entomological Society of America Symposium. Augusta, Georgia. March 2024.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2024 Citation: Murray KA, Bossard ELM, Orr SE, and Goodisman MAD. Bombus impatiens bumblebees collectively prefer sulfoxaflor contaminated food. Georgia Tech Undergraduate Research Symposium. Atlanta, GA; April 2024. (Won Peoples Choice Poster Award)
  • Type: Other Status: Other Year Published: 2023 Citation: Orr SE. Physiology and ecology of insects in a changing world. Invited Seminar at Texas Christian University. Fort Worth, Texas. October 2023.
  • Type: Journal Articles Status: Accepted Year Published: 2024 Citation: Orr SE, Hedrick NA, Murray KA, Pasupuleti AK, and Goodisman MAD. Novel insights into paternity skew in a polyandrous social wasp. In press. Insect Science. https://doi.org/10.1111/1744-7917.13343
  • Type: Other Status: Published Year Published: 2023 Citation: Orr SE. Community gardens: a solution to combat food insecurity and promote native bee conservation. The American Entomologist, 69(4):64. Winter Issue 2023. https://doi.org/10.1093/ae/tmad065
  • Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Orr SE and Goodisman MAD. Genetic architecture of social phenotypes in wasps. Entomological Society of America Meeting. National Harbor, Maryland. November 2023.