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

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Life experiences change individual behavior through complex interactions between environmental inputs and gene activity in the brain; it is unclear why certain experiences have lasting effects on behavior while other effects are easily reversed. This question is relevant to animal biodiversity, but also human health research, where one goal is to mitigate the behavioral impacts of experiences like social trauma. Though dynamic brain gene activity underlies experience-induced changes in behavior, the exact mechanisms that regulate the persistence of an experience are unclear. For example, experience may chemically alter brain DNA and therefore permanently change gene activity. However, a change in gene activity itself may be temporary, but lead to permanent changes in other factors that influence behavior, like brain structure. This study uses experimental manipulations of gene regulating mechanisms to determine whether certain ones reliably predict the longevity of an experience. The subject of these studies is the honey bee (Apis mellifera), a critical crop pollinator with a well-established relationship between social experience, brain gene activity, and aggressive behavior. Teams composed of students and beekeepers will complete research objectives and organize a summit that introduces high school students to research results and academic, industry, and non-profit career opportunities in Agricultural STEM. In addition to filling critical knowledge gaps in the study of behavioral diversity, this project will improve public science literacy and enhance partnerships among students and professionals inside and outside of academia. These steps contribute to an overall outcome of increased STEM workforce diversity, retention and career success.In honey bees, adult defensive aggression and brain gene expression are persistently changed by social information accrued over the course of several days. To a degree, these phenotypes are also responsive to immediate information about threats to the beehive, enabling researchers to assess the circumstances under which persistent social experiences are updated by new information. Persistent effects are correlated with changes in brain DNA methylation and decreased lipid content in a peripheral endocrine tissue known to impact brain gene expression, the fat body. Thus, the longevity of social experience could be a result of the gene regulatory impacts of brain DNA methylation, endocrine signaling patterns, or both. Researchers use intricate adult social manipulations to produce bees that display similar levels of aggression, but with different gene regulatory underpinnings (variation in brain DNA methylation, fat body lipid content, or both). These bees will be used to examine which regulatory mechanisms predict the strength of response to new information, in terms of behavior, brain physiology (mitochondrial bioenergetics), and genome function (gene expression and chromatin accessibility measured using RNA-seq, bisulfite-seq and ATAC-seq). Larval bees also show persistent behavioral effects of their pre-adult environment. Manipulations of larvae and measures of adult behavior will be used to determine whether the longevity mechanisms identified in adults also apply to a second life stage. This study addresses critical knowledge gaps in the relationship between brain genomics and behavioral plasticity, including how peripheral systems and brain epigenetic mechanisms work together to regulate brain gene expression and behavior.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.