Reciprocal interaction between seasonal testis and thyroid activity in Zembra Island wild rabbits (Oryctolagus cuniculus): effects of castration, thyroidectomy, temperature, and photoperiod.

The reproductive cycle of wild rabbits (Oryctolagus cuniculus) living in Zembra Island (North Tunisia) is dependent on an external factor, the photoperiod: the gonads are inhibited by long days and stimulated by short days or melatonin implants. Here we studied the role of an internal factor, thyroid hormones and the possible thyroid-gonadal interrelationships, in animals captured on Zembra Island and maintained in natural conditions of photoperiod and temperature. We determined the seasonal profile of the thyroid and testis cycles and investigated the effects of castration and thyroidectomy on the seasonal testosterone and thyroxine cycles. Plasma thyroxine and testosterone levels followed similar, parallel seasonal patterns, with a peak in autumn (October) and low values from January to August. In thyroidectomized animals, plasma testosterone levels, although significantly higher than those in controls (P < 0.001), remained low throughout the 13 mo of the experiment, and no testicular reactivation was observed in the fall. In castrated animals, despite the increase in thyroxine concentration in the 3 mo following castration (P < 0.01), plasma thyroxine levels remained low during the 2 yr of the study. We then investigated the combined effects of long days (16L:8D) and moderately high temperature (25 degrees C) on these two endocrine axes. In constant gonado-inhibiting conditions (16L:8D), whether the temperature was kept constantly high or allowed to fluctuate naturally, no reactivation of the thyroid and testicular axes was observed in the fall. In control animals, the peaks of testosterone and thyroxine concentrations observed in September were larger (P < 0.001) than those in animals subjected to the same natural photoperiod conditions but with constantly high temperature. The lower level of autumnal testis stimulation (P < 0.001) in animals maintained in conditions of constant high temperature (25 degrees C) may be attributed to the low thyroxine levels induced by high temperature. These results clearly confirm that the thyroid and testicular cycles display similar seasonal variations and show that the thyroid and gonadal axes are strictly interdependent. This study provides the first demonstration, for a given species, that the seasonal reactivation of gonad activity is controlled by the thyroid, and thyroid activity is controlled by the gonads.

Long-day inhibition of reproduction and circadian photogonadosensitivity in Zembra Island wild rabbits (Oryctolagus cuniculus).

We investigated the effects of photoperiod on testicular activity in wild rabbits (Oryctolagus cuniculus) captured on Zembra Island (North Tunisia) and maintained in experimental photoperiodic conditions. Sexually inactive animals were subjected to alternate 3-mo periods of short days (8L:16D) and long days (16L:8D) for 1 yr. Testicular activity increased significantly and then decreased to levels equivalent to or lower than those measured during sexual quiescence after 1 mo of 8L:16D or 16L:8D, respectively. Eight groups of sexually active animals were also exposed to 8L:16D for 60 days. The light phase was divided into two photofractions (7.5 and 0.5 h). The short photofraction interrupted the dark phase 9.5-18.5 h after the beginning of the main photofraction. Testicular activity was inhibited if the short photofraction interrupted the dark phase 12.5 h or more after the beginning of the main photofraction. These results clearly confirm that photoperiod affects reproduction in this species: Short days stimulate reproduction, whereas long days inhibit it. The asymmetric pattern of skeleton photoperiods used demonstrated the existence of a circadian rhythm for photogonadosensitivity, with the photosensitive phase beginning 12.5 h after dawn. In this species, photoperiod length controls both the beginning and the end of the reproductive period. These results differ from those obtained with continental populations of wild rabbits, in which reproduction is inhibited by short day length. This difference may reflect genetic drift linked to the geographic isolation of this population, which is known to have been present on this small island for more than 2000 yr.

Effects of bilateral ganglionectomy and melatonin replacement on seasonal rhythm of testicular activity in Zembra Island wild rabbits (Oryctolagus cuniculus).

This study examined the effects of subcutaneous melatonin implants on testicular activity (testis volume and plasma testosterone) in wild rabbits (Oryctolagus cuniculus) captured on Zembra Island (North Tunisia) and maintained in natural temperature and photoperiod conditions. The period of testicular activity was 2 months longer in intact animals with melatonin implants than in intact animals without melatonin implants. After bilateral superior cervical ganglionectomy, testicular activity was inhibited and no spontaneous recrudescence in gonadal function was observed during the 13 months of the experiment, demonstrating the absence of an endogenous circannual rhythm of reproductive function in this species. Renewed testicular activity was observed 2 months after the insertion of melatonin implants in ganglionectomized animals. These results confirm that testicular activity is stimulated by short days in late autumn and that melatonin reactivates the reproductive axis in this species. This finding is in contrast to that in continental populations of wild rabbits in which reproduction is inhibited by short days or melatonin. These results are discussed in terms of insularity and may reflect the geographical isolation of this population.

[Testicular activity in Orychtolagus cuniculus, a wild rabbit from Zembra island (Tunisia), during short days and long days. The effect of pineal gland deafferentation]. / Activité testiculaire chez Orychtolagus cuniculus, lapin sauvage de l'île de Zembra (Tunisie), en jours courts et en jours longs. Effet de la désafférentation de la pinéale.

Several male wild rabbits from Zembra island were used to determine the effect of the photoperiod and of the cranial sympathectomy on testicular activity. Two groups were used (G1 and G2), including each 4 control rabbits and 5 cranially sympathectomized by removal of the superior cervical ganglia. The G1 animals were reared in natural photoperiod at room temperature; the others (G2) were exposed to alternating three-month periods of short days (8 L-16 D) and long days (16 L-8 D). The changes in the testicular function (testis volume and plasma testosterone levels) were studied during one year. Our data show that: (1) The control animals, reared in natural photoperiod at room temperature, showed a decrease in testicular activity during the winter season (December to February) characterized by short days. However, testis volume and plasma testosterone seemed to be maintained at low levels during the other months of the year. (2) The artificial short days (8 L-16 D) induced an increase of the testis volume and of the plasma testosterone. A significant decrease of these parameters was observed when transferring the animals to long days (16 L-8 D). (3) The deafferentation of the pineal body by bilateral superior cervical gangliectomy blocked the testicular activity either when the animals were maintained in natural photoperiod or transferred from (8 L-16 D) to (16 L-8 D). Thus the testicular activity of wild rabbits from Zembra island is controlled by the photoperiod. Light action on the pineal is carried via the superior cervical sympathetic ganglia.