Polyphenisms in the reproductive response to short days of male quail are driven by testosterone-independent uncoupling at the photoperiodic TSH-DIO2/DIO3 pathway.

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 Tsh/Dio2/Dio3. Second, in situations where photoperiod is invariable but reproductive output differs amongst individuals, differential expression of Tsh, 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 expression of Tsh/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 to short days (i.e. phenotypic morphs) of the gonadal axis we demonstrate that the magnitude in the decrease of testes weight, size of the cloacal gland and testosterone plasma level, positively associate 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, findings are consistent with the notion that substantial uncoupling in the photoperiodic TSH/DIO2-3 pathway is responsible for the reproductive polyphenisms.