Neither retinal nor pineal photoreceptors mediate photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea)

Abstract

AbstractUsing sighted (SIG) and bilaterally enucleated (BOE) female tree sparrows, SIG, BOE, pinealectomized (SIG‐PX), and bilaterally enucleated‐pinealectomized (BOE‐PX) male tree sparrows, and intact and castrated male tree sparrows implanted epicranially with continuously emitting light sources or nonemitting blanks, I tested the hypothesis that extraretinal, extrapineal encephalic photoreceptors mediate photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea). SIG females and BOE females displayed similar patterns of plasma luteinizing hormone (LH) responses to a photoregimen designed to induce LH secretion and later photorefractoriness, to restore photosensitivity, and to reinitiate the photosexual reflex. The testicular length profiles for SIG males, BOE males, SIG‐PX males, and BOE‐PX males likewise revealed similar patterns of responses (i.e., testicular growth, regression, photorefractoriness, and recovery of photosensitivity) to an essentially identical photoregimen. These data show, for the first time in an obligately photoperiodic species, that a simulated annual reproductive cycle can be generated in the absence of both the eyes and the pineal gland and argue that neither retinal nor pineal photoreceptors are obligatorily linked to the neuroendocrine mechanism that controls seasonal reproduction. When evaluated within the context of the failure of bilateral ocular enucleation and pinealectomy to disrupt seasonal reproduction, the observations that continuously emitting light sources implanted atop the skull induced testicular growth and later photorefractoriness in intact males, induced LH secretion and later photorefractoriness in castrated males, and blocked recovery of photosensitivity in photorefractory males make a compelling case for extraretinal, extrapineal encephalic photoreception in the mechanism that controls seasonal reproduction in tree sparrows.