Diapause experience has lasting effects on adult brain gene expression in monarch butterflies

Diapause is an environmentally induced, transcriptionally driven alternative developmental program that enables organisms to withstand adverse environmental conditions. The lasting consequences of diapause experience once development is resumed in permissible conditions have not been extensively explored. The monarch butterfly provides an interesting system to address this question as reproductive diapause is a critical component of their annual North American migration. Post diapause female monarchs remigrate to the southern US after mating at overwintering sites in Mexico yet show evidence of potentially increased robustness, greater reproductive capacity and longevity, compared to summer monarchs that are not migratory. Here we further investigate the phenotypic effects of diapause experience on monarch butterflies. Monarchs reared under different conditions prior to adulthood, either natural fall diapause inducing or laboratory summer like direct development, were shifted to identical natural fall conditions upon eclosion and then assayed for adult brain transcription under identical controlled conditions. We find that natural fall conditions prior to adult development are necessary to induce diapause and diapause experience, versus reproductive status, is a strong predictor of adult brain transcription. Post diapause individuals retained signatures of diapause like stress tolerance response. Transcripts related to DNA repair and maintenance, cellular stress response, and nucleic acid metabolism were upregulated in post diapause individuals. Females not in diapause showed upregulation of transcripts related to proteolysis, primary metabolic processes and chromatin organization. Broad correlated transcriptional profile differences between post diapause and direct developing individuals suggest a difference in neural activity between groups. Our results indicate that diapause experience has lasting consequences on environmental response that may enable monarchs robust remigratory flights.