Bird eyes distinguish summer from winter: Retinal response to acute photoperiod change in the night-migratory redheaded bunting.

Eyes are the part of the circadian timekeeping system but not involved in the photoperiod regulated seasonal physiology in songbirds. Here, two experiments tested whether eyes detect and respond to seasonal change in the photoperiod environment, by examining gene and protein expressions in the retinas of redheaded buntings exposed to a single long day (LD, 16L:8D), with controls on short days (SD, 8L:16D). In the first experiment, mRNA expression of genes implicated in the light perception (opsins, rhodopsin, neuropsin, melanopsin, peropsin) and photoperiod induction (eya3, tsh-β, dio2, dio3) was measured at hours 15 and 19 (hour 0 = light on) on the first long day. There was a significant increase in the eya3, tsh-β and dio2 mRNA expression, albeit with a temporal difference, and decrease in the neuropsin mRNA expression in buntings on the first long day. There was no change in the dio3, rhodopsin, melanopsin and peropsin mRNA expressions on exposure to long days. The second experiment immunohistochemically examined the eya3, tsh-β and rhodopsin peptide expressions. eya3 was expressed in both light conditions, but with a significant higher levels in the retinal photoreceptor layer (PRL) under LD, as compared to SD. Similarly, tsh-β was expressed in the PRL of LD retinas only. Rhodopsin levels were not significantly different between SD and LD conditions, however. These results for the first time show photoperiod-dependent molecular switches in the bunting retina, similar to the well documented thyroid hormone response genes based molecular cascades in the avian hypothalamus.