Seasonal reproduction enables animals outside tropical regions to rear offspring in a favourable environment. Increasing day length triggers a hypothalamic relay involving thyrotropin, the type 2 deiodinase enzyme and thyroid hormone, which activates the hypothalamic-pituitary-gonadal axis to induce reproductive competence. Photoperiod regulates calcium metabolism and the egg-laying cycle in the Japanese quail (Coturnix japonica), and we hypothesised that activity of this relay would have major consequences for bone mineralisation and strength. Quails were housed in long (20 h light, 4 h dark) or short (6 h light, 18 h dark) day conditions for up to 12 weeks and skeletal consequences were determined by X-ray microradiography, micro-CT, electron microscopy, histomorphometry and biomechanical testing (n=10 per sex, per group). Both ovary and testis weights increased >10-fold (P<0.001, ANOVA) after long day compared to short day exposure. Long day exposure in females resulted in massive increases in bone mineral content and mineralisation (P<0.001, Kolmogorov-Smirnov test), and bone strength and stiffness (P<0.001, ANOVA), as a consequence of medullary bone formation. By contrast, medullary bone was absent in females exposed to short day length and never seen in males. Medullary bone was a highly vascular and dynamic tissue, characterised by 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 day conditions, and (ii) rapidly increased ovarian size and induction of medullary bone formation in females previously exposed to short days. These data demonstrate that the skeleton is exquisitely sensitive to photoperiod during avian seasonal reproduction and the central actions of thyroid hormone are essential for medullary bone formation. Elucidation of mechanisms that mobilise calcium and synchronise egg shell formation during the daily reproductive cycle may identify novel pathways that couple bone resorption and formation.