Hypothalamic gene switches control transitions between seasonal life history states in a night-migratory photoperiodic songbird

• Photoperiod dependent eya3, tsh β, dio2, pax6 and opsin expression in buntings.
• Reciprocal switching between dio2 and dio3 genes on the day of long light exposure
• Positive correlation of rhodopsin on eya 3 and tshβ mRNA expression.
• High dio3 in refractory buntings, and its levels decline with short day exposure.
• Downstream molecular response is possibly a cumulative effect of genes upstream.

This study investigated photoperiodic plasticity in hypothalamic expression of genes implicated in the photoperiodic light perception (rhodopsin, melanopsin, neuropsin and peropsin), transduction (pax6, bmal1, clock, per2 and casr), induction (eya3, tshβ, dio2 and dio3, gnrh and gnih) and metabolism (NPY, sirtuin1, foxO1, hmgcr, citrate synthase and dehydrogenases) in photosensitive and photorefractory redheaded buntings. There was a significant increase in eya3, tsh β, dio2, pax6 and rhodopsin and decrease in dio3 mRNA expression at hour 15 and/or 19 on the day photosensitive buntings were subjected to a 13- or 16 h, but not to 8- and 11 h light exposure. Downstream reproductive and metabolic gene expression was not altered, except for an increase in those genes coding for succinate and malate dehydrogenase enzymes involved in lipogenesis. Photorefractory buntings had high dio3 mRNA expression which significantly declined after 1 short day exposure, suggesting possible involvement of dio3 in the maintenance of photorefractoriness. Positive correlation of rhodopsin on eya 3 and tshβ indicates its role in photoperiodic timing, perhaps involving the peropsin and pax6 genes. These results suggest that rapid switching of hypothalamic gene expression underlies photoperiod-induced seasonal plasticity and regulates transitions from photosensitive to photostimulated and from photorefractory to photosensitive states in migratory songbirds.