Seasonal reproduction enables animals outside tropical regions to rear offspring in a favourable environment. Increasing day length triggers a hypothalamic relay involving thyrotropin, type-2 deiodinase and thyroid hormone, which activates the hypothalamic-pituitary-gonadal axis to induce reproductive competence. Photoperiod regulates calcium metabolism and egg-laying in Japanese quails (Coturnix japonica). We hypothesised that activity of this relay would have major consequences for the skeleton. Quails were housed in long (20h light/4h dark) or short (6h light/18h dark) day conditions for up to 12 weeks. Skeletal consequences were determined by X-ray microradiography, micro-CT, electron microscopy, histomorphometry and biomechanical testing (n=10/sex/group). Both ovary and testis weights increased >10-fold (P<0.001, ANOVA) after exposure to long days compared to short days. Long day females displayed massive increases in bone mineral content (P<0.001, Kolmogorov-Smirnov; KS), and bone strength and stiffness (P<0.001, ANOVA), due to medullary bone formation. In contrast, medullary bone was absent in short day females and never seen in males. Medullary bone was highly vascular and dynamic, with osteoclast resorption pits and mineral apposition fronts covering almost the entire bone surface. Reversal of photoperiod resulted in (i) rapid ovarian regression and loss of medullary bone in females previously exposed to long days, and (ii) rapidly increased ovarian size and medullary bone formation in females previously exposed to short days. Overall, the skeleton is exquisitely sensitive to photoperiod during avian seasonal reproduction, and central actions of thyroid hormone are essential for medullary bone formation. Furthermore, to investigate the dynamics of calcium mobilisation and eggshell formation, long day females were examined every 4 hours during one 24h reproductive cycle. Bone mineral content was highest after ovulation, and decreased rapidly during shell calcification (P<0.001, KS). Elucidation of the cellular mechanisms involved may identify novel pathways coupling rapid formation/resorption of medullary bone; an important model for osteoporosis.