Diapause history 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 non-migratory monarchs. Here we further investigate the phenotypic effects of diapause experience on monarch butterflies. Monarchs reared under different pre-adult conditions, either natural fall (diapause inducing) or laboratory summer-like (non-diapause development), were shifted to identical natural fall conditions upon eclosion and then assayed for adult brain transcription under identical controlled conditions. We find that fall conditions during pre-adult development are necessary to induce diapause. Diapause history is a strong predictor of adult brain transcription. Post-diapause individuals retained signatures of diapause maintenance-like processes, such as altered protein production, mitochondrial metabolism, and lipid regulation. However, the post-diapause response is transcriptionally distinct. Genes related to translation, with particular emphasis on mitochondrial ribosomal proteins, have increased expression post-diapause, while genes enriched for phospholipid metabolism and neurodevelopmental function have decreased expression in post-diapause individuals. Post-diapause individuals also show evidence of enhanced stress response and mechanisms that promote longevity. Overall, diapause history has lasting consequences on environmental response that may impact monarchs’ remigratory flights.