The neuroendocrine control of seasonal breeding in vertebrates depends upon a TSH/DIO2-3 pathway located in the medio-basal hypothalamus. In male quail, early data demonstrated that this photoperiodic control is independent of testosterone. At least two strong predictions arise from this. First, testosterone is unlikely to exert any significant feedback upon the expression of Tshb/Dio2/Dio3. Second, in situations where photoperiod is invariable but reproductive output differs amongst individuals, differential expression of Tshb and/or Dio2/Dio3 may be expected. Here, we validate these two predictions. First, using castration/implantation in male quails maintained under a long photoperiod, we show that the expression of Tshb/Dio2/Dio3 is testosterone independent, while aggressiveness and cognitive behaviours are testosterone driven. Second, taking advantage of the large inter-individual variability in the response of the gonadal axis to short days (i.e. phenotypic morphs), we demonstrate that the magnitude of the decrease in testes mass, size of the cloacal gland and testosterone plasma level is positively associated with levels of induction of Dio3 and repression of Dio2. In contrast, a uniformly low expression of Tshb expression is found in all morphs. These data provide strong evidence that the TSH/DIO2-3 pathway governs the reproductive axis in male quail independently of testosterone. Furthermore, our findings are consistent with the notion that substantial uncoupling in the photoperiodic TSH/DIO2-3 pathway is responsible for the reproductive polyphenisms.