Participant Support Costs: CAREER: Signal to Noise: How Complex Social Information Regulates Brain Genomics and Behavior

Animals have a remarkable ability to adjust their behavior in response to information from their environment. However, it remains difficult to predict which sources of information will have lasting impacts on behavior, and how prior experiences influence an animal’s response to new information. The overall objective of the current study is to assess whether the mechanisms that embed an experience and cause behavioral change can predict an experience’s persistence, and thus its significance. This study evaluates two hypotheses from behavioral genomics about the types of embedding mechanisms that predict lasting behavioral change. The first proposes that experiences causing lasting changes in brain gene expression predict lasting behavioral outcomes, and further, that epigenetic regulatory mechanisms (e.g., DNA methylation) give rise to these effects. The second suggests that, while environmental cues may induce temporary brain gene expression changes, dynamics at higher organizational levels in the brain and periphery predict persistent behavioral effects. These hypotheses have not been widely examined, so many critical knowledge gaps remain. The current study addresses two of these: 1) most studies have assessed the impact of a single experience, without determining how that experience alters the response to new information, 2) few studies have directly compared these hypotheses in a single system; such an approach is needed because these hypotheses may not be mutually exclusive. The current study evaluates these hypotheses simultaneously using honey bee defensive aggression. In this system, there is extensive knowledge of how different, single sources of social information regulate behavior, and the duration of these effects; notably however, it is unknown how multiple sources of information work together to shape aggression. This lays the groundwork to assess whether experiences that result in persistent changes in brain DNA methylation and/or peripheral tissue structure predict the response to new information. Researchers will manipulate social experience and generate individuals with persistent differences in brain DNA methylation, peripheral tissue structure, neither, or both. Researchers will then measure how individuals respond to new information about threats to the hive in terms of behavior, brain genome dynamics (gene expression and DNA methylation patterns), and dynamics at higher levels of organization in the brain and periphery (brain mitochondrial bioenergetics and fatbody lipid content). This approach creatively leverages a well-studied system to intricately dissect the mechanisms that regulate brain gene expression and behavior to determine how these mechanisms predict the persistence of experience and the response to new information. Research objectives are integrated with an educational component focused on improving career guidance for students in agricultural STEM. Collaborative teams composed of graduate and undergraduate students and local beekeepers will complete the proposed research objectives. Moreover, these teams, in collaboration with colleagues across the state in academia, government, business, and agricultural non-profits, will participate in a youth pollinator summit aimed at exposing high school students in Kentucky to STEM agriculture research and careers opportunities. By interacting with beekeepers, agriculture professionals, and other students at different academic stages, students will gain knowledge about career opportunities in agricultural STEM, mentoring relationships with agriculture community members, networking connections, new communication and beekeeping skills, and insights into the practical applications of research findings. Participating beekeepers will gain knowledge of the scientific process, honey bee biology, and hive best management practices, and an improved ability to communicate needs of the beekeeping community to researchers. These educational objectives harness the strength of the Kentucky agriculture community to provide important career guidance for students in STEM. Dr. Rittschof’s expertise in honey bee behavior and genomics, experience mentoring high school, undergraduate, and graduate students, and research and outreach connections with agricultural leaders throughout the state, is well-prepared to complete these objectives. Intellectual Merit. This study explicitly evaluates two often cited but rarely tested hypotheses to explain how the mechanisms that embed an experience predict the persistence of behavioral change. Findings are relevant to behavioral genomics studies of behavioral plasticity, evolution, neuroscience, and human health, as well as information integration modeling studies in behavioral ecology. Broader Impacts. High school, undergraduate, and graduate students and members of the public will be reached in this study. Objectives will improve public scientific literacy, improve STEM education and enhance STEM workforce diversity, improve partnerships inside and outside of academia, and improve potential for sustainable agriculture production in the future.