Epigenetic regulation of seasonal behavior in insects

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Many animals change their behavior in response to seasonal changes in the environment. The molecular nature of the changes that occur in the brain to alter behavior in a seasonal manner remains poorly understood. This project will examine epigenetic changes, i.e. changes in external modifications to DNA, that turn behavior-regulating genes on or off in a season-dependent manner. The work will be carried out using behavioral approaches and DNA sequencing of the genome of the long-distance migratory monarch butterfly, Danaus plexippus. The monarch exhibits extreme seasonal behavioral changes at the individual level in response to changing daylength and temperature. Migratory monarch butterflies accomplish an extraordinary journey of 2,000 miles from the United States to their overwintering sites in Mexico by flying southward in the fall. In the spring, migratory butterflies flip their flight orientation northward and return to the United States. This project will reveal seasonal epigenetic changes to the genome in the brains of these seasonal forms. These findings will provide insight into the molecular mechanisms underlying seasonal migration and the production of distinct seasonal flight orientations, and may be applicable to other migratory species. They could also have implications for conservation strategies to help preserve the iconic monarch migration, a spectacular yet threatened biological phenomenon. The project will provide valuable research training for students interested in animal behavior, neuroscience, and bioinformatics, including students from groups underrepresented in STEM fields. The researchers will also develop outreach activities devoted to increase public awareness for the need of monarch habitat conservation efforts.Seasonal behavioral adaptations are key to the ecological success of many animals. The behavioral plasticity observed in individuals in response to seasonal changes in the environment strongly suggests that epigenetics play a crucial role in shaping seasonal behavior. However, the epigenetic changes that link brain function to seasonal regulation of behavior remain largely unknown. This project will leverage the remarkable seasonal plasticity of monarch butterfly migratory behavior in response to seasonal changes in the environment (daylength, temperature) to delineate the genome-wide epigenetic architecture in the brain that underlies seasonal migratory behavior and flight orientation. The goal of the project is to identify active cis-regulatory elements (CREs) and putative transcription factors (TFs) that mediate differential gene expression in the brains of non-migrants, fall migrants and spring remigrants. The researchers will use fall migrants and fall migrants reprogrammed into spring remigrants in controlled conditions and a combination of next-generation sequencing technologies. Genes differentially expressed in the brains of these seasonal forms will be identified by RNA-seq, and open genomic regulatory regions and CREs that mediate this differential expression will be identified by ATAC-seq and ChIP-seq of histone marks. Candidate transcription factors (TFs) responsible for the seasonal behavioral reprogramming will ultimately be identified through DNA genomic footprinting within CREs. The project will have broad societal impacts through outreach activities devoted to increase public awareness for the need of monarch habitat conservation efforts, and research training of students interested in animal behavior, neuroscience, and bioinformatics.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.