Photoperiodic regulation of avian physiology: From external coincidence to seasonal reproduction.

Seasonal cycles of environmental cues generate variation in the timing of life-history transition events across taxa. It is through the entrainment of internal, endogenous rhythms of organisms to these external, exogenous rhythms in environment, such as cycling temperature and daylight, by which organisms can regulate and time life history transitions. Here, we review the current understanding of how photoperiod both stimulates and terminates seasonal reproduction in birds. The review describes the role of external coincidence timing, the process by which photoperiod is proposed to stimulate reproductive development. Then, the molecular basis of light detection and the photoperiodic regulation of neuroendocrine timing of seasonal reproduction in birds is presented. Current data indicates that vertebrate ancient opsin is the predominant photoreceptor for light detection by the hypothalamus, compared to neuropsin and rhodopsin. The review then connects light detection to well-characterized hypothalamic and pituitary gland molecules involved in the photoperiodic regulation of reproduction. In birds, Gonadotropin-releasing hormone synthesis and release are controlled by photoperiodic cues via thyrotropin-stimulating hormone-β (TSHβ) independent and dependent pathways, respectively. The review then highlights the role of D-box and E-box binding motifs in the promoter regions of photoperiodic genes, in particular Eyes-absent 3, as the key link between circadian clock function and photoperiodic time measurement. Based on the available evidence, the review proposes that at least two molecular programs form the basis for external coincidence timing in birds: photoperiodic responsiveness by TSHβ pathways and endogenous internal timing by gonadotropin synthesis.